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  • Published: 20 December 2021

Challenges and opportunities for infection prevention and control in hospitals in conflict-affected settings: a qualitative study

  • Hattie Lowe   ORCID: orcid.org/0000-0001-7110-3873 1   nAff2 ,
  • Susannah Woodd 1 ,
  • Isabelle L. Lange 1 ,
  • Sanja Janjanin 3 ,
  • Julie Barnet 3 &
  • Wendy Graham 1  

Conflict and Health volume  15 , Article number:  94 ( 2021 ) Cite this article

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A Correction to this article was published on 07 January 2022

This article has been updated

Healthcare associated infections (HAIs) are the most frequent adverse outcome in healthcare delivery worldwide. In conflict-affected settings HAIs, in particular surgical site infections, are prevalent. Effective infection prevention and control (IPC) is crucial to ending avoidable HAIs and an integral part of safe, effective, high quality health service delivery. However, armed conflict and widespread violence can negatively affect the quality of health care through workforce shortages, supply chain disruptions and attacks on health facilities and staff. To improve IPC in these settings it is necessary to understand the specific barriers and facilitators experienced locally.

In January and February of 2020, we conducted semi-structured interviews with hospital staff working for the International Committee of the Red Cross across eight conflict-affected countries (Central African Republic, South Sudan, Democratic Republic of the Congo, Mali, Nigeria, Lebanon, Yemen and Afghanistan). We explored barriers and facilitators to IPC, as well as the direct impact of conflict on the hospital and its’ IPC programme. Data was analysed thematically.

We found that inadequate hospital infrastructure, resource and workforce shortages, education of staff, inadequate in-service IPC training and supervision and large visitor numbers are barriers to IPC in hospitals in this study, similar to barriers seen in other resource-limited settings. High patient numbers, supply chain disruptions, high infection rates and attacks on healthcare infrastructures, all as a direct result of conflict, exacerbated existing challenges and imposed an additional burden on hospitals and their IPC programmes. We also found examples of local strategies for improving IPC in the face of limited resources, including departmental IPC champions and illustrated guidelines for in-service training.


Hospitals included in this study demonstrated how they overcame certain challenges in the face of limited resources and funding. These strategies present opportunities for learning and knowledge exchange across contexts, particularly in the face of the current global coronavirus pandemic. The findings are increasingly relevant today as they provide evidence of the fragility of IPC programmes in these settings. More research is required on tailoring IPC programmes so that they can be feasible and sustainable in unstable settings.

Healthcare associated infections (HAIs) are the most frequent adverse outcome in healthcare delivery worldwide—at least one in 10 patients acquire an infection whilst receiving care in health facilities in low-and-middle-income-countries (LMICs) [ 1 , 2 , 3 , 4 ]. HAIs result in death, disability and costs to health systems and patients, whilst the increased use of antibiotics to manage them contributes to the spread of antimicrobial resistance [ 5 ]. Effective infection prevention and control (IPC) is crucial to ending avoidable HAIs and an integral part of safe, effective, high quality health service delivery [ 6 ]. The World Health Organization (WHO) estimates that effective IPC programmes can reduce HAI rates by 30% [ 7 ].

The WHO guidelines for IPC at the national and facility level, issued in 2016, outline eight core components for the implementation of effective IPC, to be applied across all countries and health facilities [ 8 ]. However, the feasibility of universal application varies greatly by context, and guideline adaptation must be informed by the barriers experienced in the local context.

In low-resource settings, challenges to the implementation of effective IPC programmes have been well documented. Hospitals often experience poor IPC governance at the national and facility level; a lack of political will translates into a scarcity of national level IPC policies, underfunding for IPC activities and dedicated staff, and resource shortages [ 9 , 10 , 11 , 12 , 13 , 14 ]. Additionally, many hospitals suffer from inadequate infrastructure, including poor water, sanitation and hygiene (WASH) facilities [ 9 , 10 , 14 , 15 , 16 ]. Challenges posed by staff shortages can be further hampered by a lack of IPC training for personnel and poor compliance with IPC practices, such as hand hygiene [ 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 ]. Overcrowding [ 9 , 10 , 11 , 12 , 15 ] and inadequate infection surveillance systems [ 10 , 11 , 13 , 14 , 16 ] have also been documented as key constraints to effective IPC in low resource settings.

Conflict-affected settings represent another type of context in which IPC measures must be informed by the specific barriers and facilitators experienced locally. Whilst armed conflict and widespread violence generates an increased demand for emergency medical and surgical care, they also affect the determinants of health including food security, water and sanitation, and access to services [ 17 ]. The availability and quality of care in such settings can be further hampered by workforce shortages, supply chain disruptions and damage to health infrastructure [ 17 , 18 , 19 , 20 ]. The literature on issues relating to IPC in health care facilities in these settings is limited, but the available evidence suggests that HAIs are prevalent, and more specifically, that surgical site infections (SSIs) and antimicrobial resistance (AMR) are common complications [ 21 , 22 , 23 , 24 , 25 ]. Despite this, little work has been done to understand the challenges faced in these settings and what works to improve IPC at the facility level.

The qualitative research presented in this paper sought to explore the context-specific barriers to implementing successful IPC programmes in hospitals in conflict-affected settings, with a focus on how these settings differ from non-conflict, resource-limited settings, and what may work to improve IPC in these contexts. The research was undertaken in the period before the COVID-19 pandemic, and has implications for the current heightened need for effective IPC practices.

Data were collected as part of a larger service evaluation to assess the status of IPC across 16 hospitals supported by the International Committee of the Red Cross (ICRC) in conflict-affected countries. This mixed-methods assessment compromised pre-questionnaire telephone calls, a hospital questionnaire, and semi-structured interviews. In this paper, we present findings from the semi-structured interviews. Information about the study sites draws upon the results from the questionnaire.

Study sites

We selected twelve sites to participate in the interviews. Of the 16 hospitals included in the larger service evaluation, we excluded the three that had taken part in the pre-survey calls and a further one site for security reasons. Two of the twelve selected sites did not take part because of heavy workload during the study period. As such, we conducted ten interviews, and nine consented to inclusion in this analysis. Data collection took place across eight conflict-affected countries: Central African Republic, South Sudan, Democratic Republic of the Congo, Mali, Nigeria, Lebanon, Yemen and Afghanistan. All of the countries have experienced immense humanitarian suffering as a consequence of conflicts, such as mass displacement and refugee crises, widespread food insecurity, and major economic and health crises [ 26 ].

As one component of their humanitarian assistance within these countries, the ICRC provide emergency medical and surgical care to victims of armed conflict and other situations of violence [ 27 ]. All of the hospitals included within this study were either Ministry of Health (MoH) or private hospitals that were being provided with some level of support from the ICRC. In the majority of these facilities, the ICRC supports the provision of care on an existing structure which is determined by the local hospital management. Within this contract, a Memorandum of Understanding outlines the role and responsibilities of the ICRC team. Mobile ICRC teams, consisting of international staff, are present in all hospitals. At some sites, the ICRC directly employ local staff as well as working alongside local hospital employees. At the majority of the sites, the mobile ICRC teams are running surgical projects, and in some instances, they are also supporting other areas of the hospital such as obstetrics and gynaecology, paediatrics, general medicine, and the emergency department. At some sites, the ICRC are also responsible for training and capacity building. The level of financial support provided by the ICRC for the local hospital varied across the different sites. Some facilities were almost entirely supported by ICRC funds, including the provision of all resources (furniture, medical equipment and medicines) and the payment of local staff salaries/incentives. In other cases, the facilities received most of their funds from the MoH and ICRC funds were mainly used to support the specific ICRC activities.

Of the nine hospitals included, three were rural/field hospitals, three were secondary/county level hospitals, and three were tertiary/referral level hospitals. These hospitals differed in capacity, from 40 to 600 beds. They also differed in catchment population—some were the only hospital in a large area and as such treated a huge range of different medical and surgical patients, and others were more specialist sites, such as a field hospital that was specifically for combat-related injuries. A high proportion of the patients that the ICRC treated across all hospital levels were those requiring emergency care for weapon wounds.

The nine hospitals included in this study were very different with regard to their IPC programmes. Quantitative data from the wider service evaluation, specifically the hospital questionnaire, revealed that some hospitals lacked basic infrastructure and equipment for IPC, such as isolation rooms and materials for handwashing, and had staff with very low levels of education. Other hospitals had well established IPC programmes and supportive infrastructure for IPC, but fell down on areas such as infection surveillance. Areas that were particularly poor across a large number of facilities were the establishment of an IPC committee and the monitoring and audit of IPC practices.

Study design and data collection

We conducted semi-structured interviews to explore the barriers to effective IPC through open-ended questions and probing [ 28 ]. Semi-structured interviews also enabled the data collection to build on issues that had been identified in the hospital questionnaire (that was part of the wider service evaluation). The original interview guides focused on three main areas: (1) the impact of conflict on the hospital, (2) challenges to IPC and (3) priorities for improvement. After one interview had been conducted, we added an additional section to the interview guides to be used with hospitals that had scored highly on the questionnaire, indicating they had elements of an IPC programme in place. In this, we asked how they achieved improvements to IPC and what advice they would give to other hospitals. The data collection was an iterative process and we adapted and improved interview guides throughout, for example by removing repetitive questions and rewording questions that were commonly misunderstood.

The nine semi-structured interviews presented in this paper were conducted remotely between January and February 2020 using a mobile instant messaging app. This method was selected by participants because it could be used with poor internet connection. Two members of the research team conducted eight of the interviews in English; one asked questions and one took notes. A third member of the research team conducted one interview in French (this interview was conducted with staff at a hospital in Mali). Before the interviews began, we provided participants with background information on the purpose of the interviews. All participants gave verbal consent to participate and be audio recorded. Interviews lasted between 45 and 75 min. We transcribed the interviews and those conducted in French were translated into English.

We sent an information sheet to all ten sites explaining the purpose of this analysis and describing how confidentiality would be upheld, which was of the utmost importance given the unique challenges of conducting research in conflict-affected settings. All references to specific hospitals and countries within quotes were removed, no participants were identified by name, and descriptions of the study sites were sufficiently abstracted to ensure they could not be identified by the services they provide or by their location. This study received ethical approval from the London School of Hygiene & Tropical Medicine (ref:22563).


All individuals who participated in the interviews were ICRC-funded staff, and selected as they were either the lead ICRC staff or their delegate; three hospital programme managers (HPM), two hospital administrators, two head nurses, one operating theatre nurse and one ward nurse/IPC lead. At three sites, the HPM was joined by a second staff member.

Data analysis

We analysed the data thematically, drawing upon Braun and Clarke's Six Phases of Qualitative Analysis Framework [ 29 ]. Initial discussion of the transcripts between the research team focussed on recurring themes, similarities and differences between transcripts, and the likeness of the data to the existing literature. The transcripts were entered into NVivo 12 for coding, where deductive and inductive approaches were used in tandem [ 30 ]. An initial coding framework was developed from the literature on the challenges to IPC that exist in resource-limited settings and the first author applied these deductive codes to each transcript. The remaining coding followed an inductive approach, driven by the data itself, including conflict-specific data under the codes. The transcripts were coded until no new codes emerged and data under each code were cross checked by a second member of the research team. Following this, the codebook was refined, by removing and merging codes, before grouping codes into themes. Themes were discussed by three members of the research team. The final codebook contained 23 codes, grouped into 5 themes.

Participants described challenges to IPC that are explored along five key (and sometimes overlapping) themes: infrastructure and resources, management, the health workforce, visitors, and the direct effect of conflict on the hospital. Participants also spoke of recent IPC successes and strategies instituted to overcome challenges, which are presented within each of the themes. Hospitals are labelled A-I.

Infrastructure and resources

Participants described that inadequate and poorly maintained buildings were a barrier to effective IPC. Damaged surfaces, including walls and floors, were difficult to keep clean. A head nurse at a hospital in sub-Saharan Africa described this problem: 'We have structural issues in the sense that the pavements are not flat and it’s difficult to clean them and keep them clean' [hospital C]. They went on to describe that a lack of functioning windows and doors further hampered cleaning efforts: 'Even if we are cleaning every day there is always dust, insects, flies, mosquitoes… it’s difficult to manage' .

As well as the physical structures in the building requiring maintenance, the layout and space within the hospitals also presented challenges to IPC. Inadequate bed capacity for the number of patients resulted in overcrowding on the wards; beds were too close together and patients had to occupy other available spaces such as on mattresses in the corridors and on the ward floors. As a consequence of this overcrowding, regular cleaning was problematic. A ward nurse from a hospital in the Middle East said that it was difficult to clean the rooms according to ICRC standards because 'the patients are like sardines laying there' [hospital H]. Many of the hospital buildings also lacked sufficient isolation and cohorting rooms for infectious patients. Consequently, staff worried that outbreaks of HAIs would be more challenging to control.

Overcrowding on the wards was exacerbated when upsurges in conflict led to a sudden influx of patients. At hospital C, where the ICRC run a surgical ward for the treatment of those with weapon wounds, the head nurse described overcrowding as one of many ways that the conflict affected the services provided by the hospital: 'We have mass causalities and high numbers of patients and it becomes more and more difficult to manage hygiene and infection control with a huge number of patients' [hospital C].

A number of sites lacked functional water points in patient care areas, meaning that critical IPC practices such as hand washing and environmental cleaning were more difficult to perform. Where there was no running water at handwashing stations, staff would have to collect water from the nearest source and carry it back to the ward, which was time consuming and not conducive to correct practices. A hospital administrator at a hospital in sub-Saharan Africa discussed the potential solutions for this in the context of cleaning: 'We need to ensure there is water available in the right places. If there's not, we could have trollies to help [the cleaners] carry the water' [hospital B].

Waste management facilities were also lacking across the sites, with many reporting problems with the incinerators. Whilst some incinerators were broken, others were functional but there were no staff that had been trained on how to use them. At one particular hospital, an incinerator with inadequate capacity resulted in waste pilling up in the hospital grounds: ‘It's sharps, infectious waste, normal household waste, everything is one big pile. It's open, uncovered' [hospital H].

A shortage of resources was another barrier to IPC across many hospitals and participants from across all hospital types acknowledged this. This included a scarcity of hospital furniture, as well as medicines and essential supplies for IPC such as PPE and hand hygiene and cleaning equipment. A hospital project manager running a surgical ward for weapon wounded in rural sub-Saharan Africa linked the lack of resources to increased infections: 'We always have the same problem – if they cannot access the right equipment, we see infections' [hospital E]. Many participants explained that the ICRC would step in to provide supplies as a result of shortages, despite this not being part of the Memorandum of Understanding with the hospital management.

'The supportive role [the ICRC] play is in every element of the hospital. So it’s ‘supportive’ officially but we use this word loosely … ICRC are providing all the supplies and medical equipment, even chairs, tables, hand hygiene. We are providing everything as well as the incentives for the staff' [hospital B]

The conflict situation within some of the countries imposed an additional burden on the scarce resources. Strikes and security issues hindered the delivery and collection of essential supplies and resulted in supply chain breakdowns: 'We see the manifestations of instability – strikes, supplies arriving late because of strikes or security issues on the road' [hospital C]. The conflict also resulted in supplies going missing. Some participants reported that things would be stolen from the hospitals and sold for money. At one hospital, the participant said that the money from stolen supplies could be used 'to send to the soldiers' .

Management structures were frequently discussed by participants as having an impact on the success of an IPC programme. It was evident from the interviews that participants valued building a strong relationship with the hospital management. ICRC teams worked in a supportive role to the local hospital and as such, it was important to collaborate with hospital management to implement their respective programmes. This collective approach also worked towards ensuring the sustainability of the work that the ICRC were doing in the hospitals.

‘Our relationship with the hospital management is good. We have regular meetings and discuss together what the plan for the project is.’ [hospital F].

Sometimes, the conflict situation could make it difficult to foster such partnerships. One participant described that hospital management changed from one day to the next, meaning that it was difficult to institute IPC interventions across the hospital:

'The conflict affects everything in the hospital. One day things are red and the next day things are blue … the management is changing every day … [improving IPC] starts to become quite difficult.' [hospital H].

In addition to needing a strong relationship between hospital and ICRC management, participants said that an effective IPC governance structure was also critical to a successful IPC programme. Many participants placed great value on the establishment of an IPC committee or team that met regularly and represented all types of hospital staff. This enabled all the relevant personnel (hospital and ICRC staff) to discuss the IPC programme and set strategic targets based on which areas needed improving. Having an IPC governance structure in place meant that regular training could be implemented, which was also widely recognised as key to a successful IPC programme.

The health workforce

A shortage of staff was a common across the sites. Some participants related this to a lack of funding, and others to the high numbers of patients and subsequent increased workload. A number of hospitals said that staff turnover was high due to the low wages, particularly amongst cleaning staff: 'There is turnover amongst [cleaners] … they come and go – if they find a motivation outside of the hospital that is better than what we offer them they quickly leave' [hospital D]. Some hospitals were sent volunteers when staff numbers were low, but volunteers could be untrained. One participant described that the conflict in the country had a direct impact on the staff numbers: 'There are staff who say they cannot come to work because of war' [hospital E].

Participants across all of the sites said that education levels amongst the health workforce were a challenge to IPC, in particular specific knowledge of IPC theory and practice. Some participants suggested that the conflict situation within the country had an impact on national training programmes.

In terms of capacity building, all participants believed that more in-service training was required for critical IPC practices. Participants indicated that cleaning staff in particular required tailored support because of low literacy levels, agreeing that on-the-job training was the most effective mode of delivery: “ We do a bit of theory but we mostly do practical work about how hygiene should be practiced. We simulate what they should do' [hospital D]. A ward nurse at a rural hospital in the Middle East echoed this. They found that leading by example and demonstrating cleaning practices inspired staff to adopt these methods into their own daily practices.

However, participants acknowledged that training alone was insufficient to improve compliance to IPC practices. Hand hygiene and waste segregation were widely recognised as practices that needed continuous reinforcement. The head nurse at hospital in sub-Saharan Africa attributed this to a lack of motivation amongst staff: 'It’s not a lack of knowledge [about waste segregation] but it’s more related to motivation and a lack of adherence to practices' [hospital F]. Participants commented that a lack of monitoring and follow-up after training resulted in limited changes in behaviour. New skills needed to be reinforced to be integrated into everyday practices. However, this could be challenging due to understaffing, as the head nurse of a surgical ward noted: 'We need to supervise but we are not always present' [hospital C].

At sites where it was taking place, monitoring and supervision was used as a tool to assess progress towards IPC goals and increase motivation among the workforce:

'[The IPC team] monitor which services are better than others and this motivates services to work better. I think this is a good idea to push people to work harder. Monitoring of services is good as then you can know where they are and what needs to be done' [hospital E];

One hospital in particular spoke about the successes of the effective monitoring of services and supervision of staff. At a large hospital in sub-Saharan Africa, the nursing team noticed that health workers across different departments lacked a focal point for IPC information and support. In response to this, the IPC team elected a group of IPC champions (one nurse from each department). The IPC champions met regularly to discuss challenges and come up with solutions which they took back to their departments. They were also responsible for promoting and reinforcing correct practices and following-up new skills that had been taught in training. The head nurse noted:

'Since the implementation of the IPC champions there has been follow up with the cleaners of the hospital and supervision of their activities, working together in reinforcing cleaning … this is something that has started to improve … [Waste segregation] was something that before the implementation of the IPC champions wasn’t implemented in the hospital in all the different departments. Now we're seeing an improvement.' [hospital F].

Many participants identified large numbers of visitors as a challenge to IPC, despite some providing a critical role in caring for their sick relatives. Participants explained that visitors did not always understand the importance of hygiene practices, such as hand washing, which increased the risk of transmission of HAIs. At a hospital in sub-Saharan Africa, the hospital administrator acknowledged that it would be difficult to change such behaviours because it was not feasible to provide hygiene education to all of the patients and visitors that came through the doors.

In addition, large visitor numbers contributed to overcrowding on the wards, which hindered the cleaners' ability to effectively clean the wards.

'Visitors are making it harder to clean and harder to care for patients. We are dependent on caretakers to be there, the patients will not survive without them. The caretakers don't always understand the importance of hygiene' [hospital A].

On top of this, because of the volatility and tensions caused by the conflict, participants felt it was difficult to restrict visitors to the hospital and impose visiting hours: ' The overcrowding is a priority but it is also very hard to work on with the volatile situation here … It provokes aggression which could make the situation worse' [hospital A] .

Direct effect of conflict

Whilst some existing challenges to IPC were exacerbated by the conflict situation in the country, other challenges were a direct result of it. The general functioning of many hospitals was dependent upon the situation around them. Security issues were raised by a number of participants who explained that this often led to staff being evacuated, or even hospital closures.

A major challenge to IPC directly related to the conflict situation was the high rate of wound infection among patients. The majority of participants described how patients coming with weapon wounds often presented late and in many cases would already have infected wounds. One participant working on an ICRC ward for the weapon wounded in sub-Saharan Africa described the impact this had on IPC:

'The majority of our patients are coming late to the facility, I think the average is about 4–5 days [since injury] … They are coming already infected so the risk of transmitting infection to other patients is quite high' [hospital C].

Many participants also believed that these weapon wounds posed challenges to surgical site infection surveillance because it was difficult to assess where the original infection had come from, as a hospital administrator described:

'It’s difficult to assess post-operative infections … weapon wounds are often contaminated since the day they arrived. When there is a post-operative infection related to surgical care it is difficult to know the cause in an objective way' [hospital F].

This qualitative study found that inadequate hospital infrastructure, resource and workforce shortages, education of staff, inadequate in-service IPC training and supervision, and large visitor numbers are barriers to IPC in health facilities in conflict-affected settings, echoing research in other resource-limited contexts [ 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 ]. Our findings also highlight the unique challenges faced by hospitals in countries affected by conflict, in which high patient numbers, supply chain disruptions, high infection rates and attacks on healthcare infrastructures exacerbated existing challenges and imposed an additional burden on hospitals and their IPC programmes.

In our study, as within the wider literature [ 9 , 10 ], many respondents saw the environment around them as unsupportive of IPC. The built environment and availability of resources play a critical role in supporting vital IPC practices, such as hand hygiene and environmental cleaning [ 31 ]. Inadequate buildings, WASH infrastructure and a scarcity of resources limited the opportunity for such practices in our study. The conflict situation in the country had an additional impact on the availability of supplies for IPC. Strikes and insecure roads resulted in supply chain disruptions; a well-documented challenge to health care provision in the context of armed conflict [ 17 , 19 ].

Participants also felt that poor structural design led to overcrowding and an increased risk of HAI transmission. As a result of conflict and mass casualties, already crowded facilities could experience a sudden influx of patients, exceeding maximum capacity. Increased patients and visitors to the hospital made it harder for staff to follow IPC protocols, such as environmental cleaning, and general tensions and the volatile situation made imposing restrictions on visitors challenging. Participants felt that hygiene behaviours of patients and visitors (and sometimes staff), such as a lack of hand washing, also added to the risk of infection transmission. It is also worth noting that although in our study, and in other low- and middle-income settings [ 32 ], visitors and patient caretakers play a vital role in patient care, very little is known empirically about their impact on infection transmission. Overcrowding is acknowledged as a risk factor for increased HAIs [ 4 ] and an exploratory qualitative study in three tertiary hospitals in Bangladesh found that overcrowded wards and an uncontrolled flow of visitors were conducive to the transmission of infection [ 33 ]. Coupled with inadequate isolation capacity in many of the hospitals studied and high infection rates due to the nature of war wounds, participants in our study worried about the safety of the health care environment for patients, visitors and healthcare workers.

Low knowledge and education of staff and a lack of compliance to IPC practices stood out as a major challenge to IPC in our study. Similar barriers to IPC were found in a qualitative study among health workers in Mongolia, where staff had suboptimal knowledge of infection control, attributed to inadequate coverage of IPC in national training programmes [ 13 ].

Poor hand hygiene compliance was another barrier to IPC in our study; a challenge not unique to this setting and one known to play a central role in the transmission of HAIs globally [ 34 ]. Participants in our study felt that training alone was insufficient to improve compliance to critical IPC practices such as hand hygiene among healthcare workers. They emphasised the need for behaviour change interventions and monitoring and follow-up on top of in-service training. This echoes evidence from a review by Naikoba and Hayward [ 35 ], who found that stand-alone, educational interventions for hand hygiene had limited long-term impact on compliance. Instead, the most effective approaches were multifaceted, combining education with written material, reminders and continuous feedback. The implementation of WHO's multimodal improvement strategy [ 36 ] has been found to significantly improve hand hygiene compliance across a number of LMICs, including Mali [ 37 ] and Rwanda [ 38 ], demonstrating feasibility of such interventions in resource-limited settings.

Throughout the interviews, participants frequently referred to cleaning staff when discussing challenges to IPC. Respondents acknowledged their value to the IPC programme but stressed that they needed more training and supervision in order to improve their practice. Cleaners have often been neglected in IPC programmes—data from 56 health facilities across Zanzibar, The Gambia, Bangladesh and India found that less than half provided any form of IPC training for cleaners and that the cleaning workforce had low status and poor work conditions [ 39 ]. In our study, the need for locally adapted training materials that are tailored to cleaning staff with low literacy was evident, which is a priority recognised more broadly for IPC training in low-resource settings [ 12 ], and something that is being piloted through initiatives such as TEACH CLEAN [ 40 ].

In terms of what participants felt worked to improve IPC at their hospitals, value was given to the presence of an IPC committee, an essential first step in setting up an IPC programme [ 10 ]. Regular in-service training, including practical sessions and consistent monitoring and supervision of staff, which are both known to improve professional practice in health care settings [ 31 , 41 ], were also recognised as strategies to improve IPC practices in our study. Of particular interest, with the potential to be transferred across ICRC sites and to other settings, was the implementation of IPC champions to support education and empower staff to make sustainable behavioural changes. The use of IPC champions as trainers and mentors is an approach recommended by WHO in their Core Components for Infection Prevention and Control at the healthcare facility [ 31 ]. Bundled IPC interventions have also seen success in low-resource settings, with potential to be implemented in conflict-affected settings such as those in this study [ 42 , 43 ]. Across fifteen LMICs and 86 intensive care units, an intervention bundle including education, constant performance feedback and outcome and process surveillance improved IPC protocol adherence among staff and the incidence of the HAI under study [ 44 ], demonstrating the potential of low-cost and high-impact multi-component interventions in these settings.

Responses to the current coronavirus pandemic also provide important lessons for IPC programmes in resource limited and conflict-affected settings. One example includes the response to global PPE shortages, a challenge that was common for hospitals in our study before the onset of the pandemic. In such settings where supply chain disruptions and insecurity can result in inadequate PPE supply, the WHO’s guidance on the rational use, decontamination and reprocessing of PPE for covid-19 could be reviewed to create locally tailored solutions to mitigate the impact of PPE shortages [ 42 ].

Whilst participants in this study felt they had implemented approaches that were having a positive impact on IPC, many hospitals still faced the direct effects of conflict. Security incidents, hospital closures, changes in management and a lack of funding hampered progress towards IPC goals. The current global coronavirus pandemic has further highlighted the fragility of conflict and humanitarian settings, where global issues such as inadequate bed capacity and staff and PPE shortages during the pandemic, all identified as challenges to effective IPC in this paper, will be felt most acutely [ 46 , 47 , 48 ]. It emphasises the urgency of this topic and the need for additional research and intervention to strengthen the response for the most vulnerable populations.

An important strength of this study is that it is, to our knowledge, the first to explore qualitatively the barriers and challenges to IPC in hospitals in conflict-affected settings. While it highlights the stark challenges faced in such settings, similar to those identified by Mouallem and colleagues [ 48 ], it also offers realistic approaches to overcome some of these challenges in the context of limited resources and funding. It also presents an agenda for further research and intervention in these settings, particularly in the light of the global coronavirus pandemic. A limitation of this study is the relatively small sample, which limits the generalisability of our findings. A second limitation relates to the lack of data from local hospital staff. All of those who were interviewed were members of ICRC staff, some who had been working at the sites for a limited amount of time, and some who were not nationals to the country. Whilst highly experienced in their field, the data lacked the perspective of individuals who may have had greater knowledge and insight into the specific contexts in which they worked. Finally, relying on online methods for data collection through a messaging app posed a number of challenges. Poor connection resulted in disruption to the natural flow of conversation and the inability to use the video function, which at times made it difficult to build and maintain rapport with participants.

Many of the barriers to effective IPC that were identified in this paper are common across LMIC settings. These include inadequate infrastructure, resource and workforce shortages, low workforce education levels, inadequate in-service IPC training, and large visitor numbers. In conflict-affected settings, there is an additional burden on health facilities and their IPC programmes. Upsurges of conflict and security incidents resulted in supply chain disruptions, high patient numbers, and high infection rates. While the hospitals included in this study faced significant barriers, they also demonstrated how they overcame certain challenges in the face of limited resources and funding. These strategies present opportunities for learning and knowledge exchange across contexts, particularly in the face of the current global coronavirus pandemic. While this study was carried out before the coronavirus pandemic was declared, the findings are increasingly relevant today as they provide evidence of the fragility of IPC programmes in these settings and how more research is required on tailoring IPC programmes so that they can be feasible and sustainable in unstable settings.

Availability of data and materials

The datasets generated and analysed during the current study are not publicly available due to the protection of individual privacy.

Change history

07 january 2022.

A Correction to this paper has been published: https://doi.org/10.1186/s13031-022-00433-5


Healthcare Associated Infections

Infection Prevention and Control

Personal Protective Equipment

World Health Organization

International Committee of the Red Cross

Low- and Middle-Income country

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The authors gratefully acknowledge the co-operation and contribution to the study from the interviewees in the participating hospitals. The wider project within which this qualitative component was undertaken was supported by an Advisory Group and we thank the members for their overall guidance. Senior oversight of the project from ICRC was provided by Eileen Daly and Carole Dromer, and we hereby gratefully acknowledge this.

Funding for this study was provided by the International Committee of the Red Cross (ICRC).

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Hattie Lowe

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Hattie Lowe, Susannah Woodd, Isabelle L. Lange & Wendy Graham

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WJG, SW and HL conceptualised the study. SJ and JB provided input on data collection tools and procedures. HL, SW and IL collected and analysed the data. HL wrote the first draft of the manuscript and SW, IL, WJG, SJ and JB contributed to editing and finalising the manuscript. All authors read and approved the final manuscript.

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Lowe, H., Woodd, S., Lange, I.L. et al. Challenges and opportunities for infection prevention and control in hospitals in conflict-affected settings: a qualitative study. Confl Health 15 , 94 (2021). https://doi.org/10.1186/s13031-021-00428-8

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Etiology and antimicrobial resistance of secondary bacterial infections in patients hospitalized with COVID-19 in Wuhan, China: a retrospective analysis

  • Jie Li 1   na1 ,
  • Junwei Wang 1   na1 ,
  • Yi Yang 1   na1 ,
  • Peishan Cai 1 ,
  • Jingchao Cao 1 ,
  • Xuefeng Cai 1 &
  • Yu Zhang 1  

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A considerable proportion of patients hospitalized with coronavirus disease 2019 (COVID-19) acquired secondary bacterial infections (SBIs). The etiology and antimicrobial resistance of bacteria were reported and used to provide a theoretical basis for appropriate infection therapy.

This retrospective study reviewed electronic medical records of all the patients hospitalized with COVID-19 in the Wuhan Union Hospital between January 27 and March 17, 2020. According to the inclusion and exclusion criteria, patients who acquired SBIs were enrolled. Demographic, clinical course, etiology, and antimicrobial resistance data of the SBIs were collected. Outcomes were also compared between patients who were classified as severe and critical on admission.

Among 1495 patients hospitalized with COVID-19, 102 (6.8%) patients had acquired SBIs, and almost half of them (49.0%, 50/102) died during hospitalization. Compared with severe patients, critical patients had a higher chance of SBIs. Among the 159 strains of bacteria isolated from the SBIs, 136 strains (85.5%) were Gram-negative bacteria. The top three bacteria of SBIs were A. baumannii (35.8%, 57/159), K. pneumoniae (30.8%, 49/159), and S. maltophilia (6.3%, 10/159). The isolation rates of carbapenem-resistant A. baumannii and K. pneumoniae were 91.2 and 75.5%, respectively. Meticillin resistance was present in 100% of Staphylococcus aureus and Coagulase negative staphylococci , and vancomycin resistance was not found.


SBIs may occur in patients hospitalized with COVID-19 and lead to high mortality. The incidence of SBIs was associated with the severity of illness on admission. Gram-negative bacteria, especially A. baumannii and K. pneumoniae, were the main bacteria, and the resistance rates of the major isolated bacteria were generally high. This was a single-center study; thus, our results should be externally examined when applied in other institutions.


The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which first appeared in 2019, spread to most of the countries around the world, and the corona virus disease 2019 (COVID-19) has progressed into a global pandemic. Globally, as of July 15, 2020, there have been more than 12 million confirmed cases of COVID-19, including over 570 thousand deaths [ 1 ]. According to the previous studies [ 2 , 3 ], secondary bacterial infection (SBI), which occurs at an approximate incidence of 10% ~ 15%, is a dangerous and common complication in patients hospitalized with COVID-19. According to existing reports, 50% of COVID-19 deaths experienced secondary bacterial infections (SBIs); thus, patients with SBIs have a higher risk of mortality [ 3 , 4 ]. SBIs had become the hidden threat lurking behind COVID-19. The effective antimicrobial regimen is still one of the key measures for the successful treatment of COVID-19 [ 5 ].

Due to the lack of controlled clinical trials about the use of empiric antibacterial agents in COVID-19 patients, the current recommendations are based upon extrapolation of data from other viral pneumonia [ 5 ]. A quick guide [ 6 ] has recommended empiric antimicrobial treatment for all possible bacteria in severe COVID-19 patients with SBIs. Also, empiric use of third-generation cephalosporin combined enzyme inhibitor for SBIs has been recommended in severe patients [ 7 ]. Yet, the SBIs caused by COVID-19 tend to differ from other forms of SBIs. During the outbreak, a large number of broad-spectrum antibacterial agents were used, and the vast majority of patients hospitalized with COVID-19 were given empirical antimicrobial treatment before SBIs were confirmed [ 2 , 3 , 8 ]. The broader application of antibacterial agents may further lead to changes in etiology and antimicrobial resistance. The SBIs in patients hospitalized with COVID-19 should be treated according to further microbiological data. Currently, there is no report on the pathogenic spectrum of SBIs. Some cases of bacterial infections have been reported in the research about the clinical characteristics of COVID-19; however, these were no systematic studies on the etiology of SBIs, and the number of positive cultures was small [ 8 , 9 , 10 , 11 , 12 ]. Merely indicating the distribution of bacteria is not enough to guide reasonable empiric use of antibacterial agents.

Consequently, in the present study, we conducted a first large sample size retrospective analysis of SBIs in patients hospitalized with COVID-19. The aim was to obtain the etiology and antimicrobial resistance of SBIs for more accurate antimicrobial use.

Materials and methods

Study population.

This single-center, retrospective study was done at Wuhan Union Hospital, which was a designated hospital to treat patients with COVID-19 in Wuhan, China. A total of 1495 patients were diagnosed as COVID-19 and treated in the West Campus of Wuhan Union Hospital between January 27 and March 17, 2020. According to the severity of illness on admission, 1050 of them were classified as severe (i.e., dyspnea, respiratory frequency ≤ 30/min, blood oxygen saturation ≤ 93%, the partial pressure of arterial oxygen to fraction of inspired oxygen ratio < 300, and/or lung infiltrates > 50% within 24 to 48 h) and 258 patients were critical (i.e., respiratory failure, septic shock, and/or multiple organ dysfunction or failure). Demographic, clinical course, laboratory, and treatment data were collected from electronic medical records.

Study design

SBIs were defined when patients showed clinical characteristics of bacterial infections, and at least one positive etiology of bacteria was acquired from qualified microbiological specimens (qualified sputum, endotracheal aspirate, bronchoalveolar lavage fluid, blood samples, or qualified urine) after SARS-CoV-2 infection [ 3 , 13 ]. We performed a retrospective review of medical records that met the criteria from January 27 to March 17, 2020. Inclusion criteria were: (1) patients diagnosed with COVID-19 according to the Guidance for COVID-19 (7th edition) released by the National Health Commission of China [ 14 ]; (2) met the diagnostic criteria of SBIs. Patients were excluded if: (1) before being infected with SARS-CoV-2, they had other infectious diseases; (2) the medical records were incomplete. Patients enrolled in the study were basically severe or critically ill. Therefore, according to the severity of illness on admission, the enrolled patients were divided into severe group and critical group.

The study was approved by the Ethics Committee of Union Hospital, Tongji Medical College, Huazhong University of Science and Technology (Permission number: [2020]0104).

Pathogen detection and antimicrobial susceptibility

The qualified microbiological specimens of patients with COVID-19 from January 27, 2020 to March 17, 2020 were collected and cultured. Pathogen identification and antimicrobial susceptibility testing were carried out on the Phoenix-100 automatic microbiological system (BD Corporation, USA). In some further antimicrobial susceptibility testing, the international Kirby-Bauer method was also used. All the results were interpreted according to the criteria of the Clinical and Laboratory Standards Institute (CLSI 2019) [ 15 ]. The same strains from one patient were counted only once. The data were analyzed using WHONET 5.6 software (World Health Organization).

Statistical analysis

Continuous and categorical variables were presented as median (IQR) and percentages. We assessed differences between the severe and critical groups using the Mann-Whitney U test for continuous variables and χ 2 test, or Fisher’s exact test for categorical variables. A P -value < 0.05 was regarded as statistically significant. All statistical analyses were performed by IBM SPSS Statistics 26.0.

General information

After excluding 9 patients who had other infectious diseases before being infected with SARS-CoV-2, and 7 in patients with incomplete medical records, a total of 102 patients (6.8%, 102/1495) were included in the study. The mean age was 66.2 ± 11.2 years (30 ~ 93 years; Table  1 ), and 68 patients (66.7%) were males. Compared with the severe group, the critical group was more likely to acquire SBIs (69/258 [26.7%] vs. 33/1050 [3.1%]). Almost half of the patients who acquired SBIs (49.0%, 50/102) died during hospitalization, and the other patients were discharged. Compared with the severe group, the critical group had a significantly increased mortality (45/69 [65.2%] vs. 5/33 [15.2%], P  < 0.0001).

The proportion of SBIs in the lungs, bloodstream, and urinary tract was 86.3% (88/102), 34.3% (35/102), and 7.8% (8/102), respectively. Moreover, 27 (26.5%) patients had lung infections mixed with bloodstream infections; 2 (2.0%) patients had urinary tract infections. There was no secondary infection in other sites.

Etiology of the secondary infection

A total of 159 strains of bacteria were isolated from the cultures in the 102 patients. Among the isolated bacteria, Gram-negative bacteria were the main bacteria, accounting for 85.5%. The top three bacteria of SBIs were Acinetobacter baumannii ( A. baumannii , 35.8%), Klebsiella pneumoniae ( K. pneumoniae , 30.8%), and Stenotrophomonas maltophilia ( S. maltophilia , 6.3%). The distribution and composition ratios of bacteria are shown in Table  2 . Among them, 46 patients had infections with mixed bacteria, mostly A. baumannii mixed with K. pneumoniae (41.3%)(Table  3 ).

Antimicrobial susceptibility

The antimicrobial resistance rate of bacteria isolated from patients with SBIs was generally high. The isolation rates of carbapenem-resistant A. baumannii (CRAB) and carbapenem-resistant K. pneumoniae (CRKP) were 91.7 and 76.6%, respectively. The infection rates of CRAB and CRKP in the critical group were significantly higher than in the severe group ( P  < 0.05). Meticillin resistance was present in 100% of Staphylococcus aureus and Coagulase negative staphylococci , and vancomycin resistance was not found. The isolation rate of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli ( E. coli ) was 75%. The results of antimicrobial susceptibility testing for the major bacteria are shown in Table  4 and Table  5 .

Respiratory failure or multiple organ failure is the direct cause of death in patients with COVID-19, and SBIs have an important role in this process [ 16 ]. Among the 1495 patients with COVID-19, the incidence of SBIs was 6.8%. The incidence of SBIs was lower than the data in previous studies (10% ~ 15%, Wuhan, China), which may be due to the larger sample size in the present study [ 2 , 3 ]. In the mild ill COVID-19 patients, there was no SBI that met the inclusion and exclusion criteria; thus, it was impossible to compare the differences between the mild group and the severe group. The incidence in the critical group was much higher than in the severe group, which was consistent with the higher rate of central catheter placement and invasive mechanical ventilation in critical patients [ 2 ]. Almost half (49.0%) of the patients with SBIs died during hospitalization, which was consistent with the previous study (50%) [ 3 ]. Compared with the severe group, the critical group had significantly increased mortality. Recent studies related to COVID-19 reported that the male gender was a risk factor for disease severity status, and age 65 or older was a risk factor related to death [ 3 , 17 , 18 ]. In our research, no differences in gender and age were found between the severe and critical groups, which suggested that gender and age were not risk factors for death in patients with SBIs. A. baumannii and K. pneumoniae were the main pathogens of SBIs, and the infection rates of A. baumannii , CRAB, K. pneumoniae and CRKP in critical group were significantly higher than in the severe group. As the mortality of CRAB and CRKP has always been high, we believe it is one of the reasons why the mortality rate in the critical group was higher than that in the severe group.

According to the sites of SBIs, lung infections were the main type, which may be related to the decrease of airway defense function after SARS-CoV-2 infection [ 19 ]. Invasive operations such as trachea intubation and ventilator-assisted breathing during hospitalization may also be the causes of SBIs in the lungs. There were 35 patients with bloodstream infections, 27 of which were bloodstream infections mixed with lung infections. We compared the bacteria of mixed infections and found that 21 patients had the same bacteria in the lungs and bloodstream, including K. pneumoniae (66.7%, 14/21) and A. baumannii (33.3%, 7/21). In these 21 patients, lung infections occurred first, followed by bloodstream infections. The antibiogram reportings of K. pneumoniae and A. baumannii isolated from qualified sputum specimens and blood specimens were the same. It is possible that the migration of K. pneumoniae or A. baumannii from the lungs resulted in bloodstream infections in these patients.

A total of 159 strains of bacteria isolated in this study were mainly Gram-negative bacteria. The top three bacteria of secondary lung infections were A. baumannii , K. pneumoniae , and S. maltophilia . The etiological distribution was different from the previously reported bacteria of hospital-acquired pneumonia (HAP) [ 20 , 21 ]. The proportion of A. baumannii and K. pneumoniae was significantly increased, and the proportion of Pseudomonas aeruginosa ( P. aeruginosa ) and Staphylococcus aureus ( S. aureus ) was decreased, which suggested that the initial empirical antimicrobial program of HAP should not be completely copied if SBIs occur in the lungs. The lower proportion of P. aeruginosa and S. aureus suggests that it is not necessary to first choose antimicrobial with antibacterial activity of P. aeruginosa and S. aureus for SBIs in the lungs . The choice of antimicrobial program could be more suitable to treat the infections of A. baumannii and K. pneumoniae. The antimicrobial susceptibility tests showed that most of A. baumannii and K. pneumoniae were multi-drug resistant bacteria. The isolation rates of CRAB and CRKP were 91.7 and 76.6%, respectively. When patients suffer from SBIs, the possibility of infections by drug-resistant strains should be adequately considered. The resistance rate of tigecycline and cefoperazone sulbactam was relatively lower, and the combination could be considered for the initial empirical treatment of SBIs in the lungs. According to reports [ 22 , 23 ], the avibactam compound has a better effect on carbapenem-resistant K. pneumoniae ; yet, there is still no systematic research in patients with COVID-19.

Although the bacteria of secondary bloodstream infections were mainly Gram-negative bacteria, the proportion of Gram-positive bacteria was relatively higher than lung infections. If the bacteria derived from lung infections were excluded from the statistics, Gram-positive bacteria would be the main bacteria for bloodstream infections. In this study, we found that 80.0% (16/20) of patients infected with Gram-positive bacteria were given central venous catheter implantation during hospitalization. Our results revealed that the bloodstream infections of Gram-positive bacteria were associated with central venous catheter implantation. Therefore, we suggest that the management of venous catheters in severe patients should be strengthened to avoid bloodstream infections. According to antimicrobial susceptibility tests, methicillin resistance was found in 100% of Staphylococcus aureus and Coagulase negative staphylococci , and vancomycin resistance was not yet found. This suggests that vancomycin can be used as the empirical choice for Gram-positive bacteria if secondary bloodstream infections occur.

The number of secondary urinary tract infections was relatively small, and E. coli was still the main bacterium. According to antimicrobial susceptibility tests, the isolation rate of ESBL-producing E. coli was 75%. As the initial empirical choice, β-lactams combinations with β-lactamase inhibitors could be recommended, rather than levofloxacin and ceftriaxone.

This study has several limitations. First, this was a single-center study performed in the Wuhan Union Hospital. The etiology and antimicrobial resistance in different medical institutions or different regions may be different. The results should be externally examined when applied in other institutions. Second, during the epidemic, the main focus was dedicated to treating COVID-19 patients; thus, there was no enough time to examine the mechanism of bacterial resistance. Third, our analysis of the treatment effect of SBIs was insufficient, which should be carried out in further research.

SBI is one of the main complications in patients hospitalized with COVID-19 that leads to high mortality. Gram-negative bacteria, especially A. baumannii and K. pneumoniae , are the main bacteria. The antimicrobial resistance rates of the major isolated bacteria are generally high, which indicates that more accurate use of antibacterial agents is necessary for SBIs in patients hospitalized with COVID-19.

Availability of data and materials

The supporting data are available from the corresponding author and laboratory depositories.


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Acinetobacter baumannii

Klebsiella pneumoniae

Escherichia coli

Stenotrophomonas maltophilia

Pseudomonas aeruginosa

Staphylococcus aureus

Carbapenem-resistant A. baumannii

Carbapenem-resistant K. pneumoniae

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We acknowledge the supports from colleagues in Wuhan Union Hospital in the interpretation of the microbiological results.

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Jie Li, Junwei Wang and Yi Yang contributed equally to this work.

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Department of Pharmacy, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China

Jie Li, Junwei Wang, Yi Yang, Peishan Cai, Jingchao Cao, Xuefeng Cai & Yu Zhang

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JL, JW, YY, JC, XC collected, analyzed and interpreted the clinical and laboratory data. JW and YY processed data analysis. JL and JW drafted the manuscript. XC and YZ revised the final manuscript and take responsibility for all data. The author(s) read and approved the final manuscript.

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Li, J., Wang, J., Yang, Y. et al. Etiology and antimicrobial resistance of secondary bacterial infections in patients hospitalized with COVID-19 in Wuhan, China: a retrospective analysis. Antimicrob Resist Infect Control 9 , 153 (2020). https://doi.org/10.1186/s13756-020-00819-1

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Secondary bacterial infections and antimicrobial resistance in COVID-19: comparative evaluation of pre-pandemic and pandemic-era, a retrospective single center study

Mustafa karataş.

1 Faculty of Medicine, Ege University, İzmir, Turkey

Melike Yaşar-Duman

2 Department of Medical Microbiology, Faculty of Medicine, Ege University, İzmir, Turkey

Alper Tünger

Feriha Çilli, Şöhret aydemir, volkan Özenci.

3 Division of Clinical Microbiology, Department of Laboratory Medicine, Karolinska Institutet, Stockholm, Sweden

4 Department of Clinical Microbiology F 72, Karolinska Institutet, Karolinska University Hospital, Huddinge, 141 86 Stockholm, Sweden

Associated Data

Authors can confirm that all relevant data are included in the article and/or its additional information files.

In this study, we aimed to evaluate the epidemiology and antimicrobial resistance (AMR) patterns of bacterial pathogens in COVID-19 patients and to compare the results with control groups from the pre-pandemic and pandemic era.

Microbiological database records of all the COVID-19 diagnosed patients in the Ege University Hospital between March 15, 2020, and June 15, 2020, evaluated retrospectively. Patients who acquired secondary bacterial infections (SBIs) and bacterial co-infections were analyzed. Etiology and AMR data of the bacterial infections were collected. Results were also compared to control groups from pre-pandemic and pandemic era data.

In total, 4859 positive culture results from 3532 patients were analyzed. Fifty-two (3.59%) patients had 78 SBIs and 38 (2.62%) patients had 45 bacterial co-infections among 1447 COVID-19 patients. 22/85 (25.88%) patients died who had bacterial infections. The respiratory culture-positive sample rate was 39.02% among all culture-positive samples in the COVID-19 group. There was a significant decrease in extended-spectrum beta-lactamase (ESBL)-producing  Enterobacterales  (8.94%) compared to samples from the pre-pandemic (20.76%) and pandemic era (20.74%) (p = 0.001 for both comparisons). Interestingly,  Acinetobacter baumannii  was the main pathogen in the respiratory infections of COVID-19 patients (9.76%) and the rate was significantly higher than pre-pandemic (3.49%, p < 0.002) and pandemic era control groups (3.11%, p < 0.001).

Due to the low frequency of SBIs reported during the ongoing pandemic, a more careful and targeted antimicrobial prescription should be taken. While patients with COVID-19 had lower levels of ESBL-producing  Enterobacterales,  the frequency of multidrug-resistant (MDR)  A. baumannii  is higher.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12941-021-00454-7.


Antimicrobial Resistance (AMR) is recognized as a public threat with constantly increasing urgency [ 1 ]. It is estimated that by the year 2050, 10 million deaths and an economic loss of $100 billion would be expected annually due to multidrug-resistant (MDR) (resistant to more than three or more antimicrobial categories) infections [ 2 ]. It is widely accepted that antimicrobial surveillance is crucial for tackling AMR globally [ 3 ]. The current pandemic, a consequence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is associated with high mortality, morbidity, and healthcare-related costs [ 4 ]. Recent data shows that more than 175 million people have so far been infected and 3.7 million of them died [ 5 ]. Secondary bacterial infections (SBIs) result in higher mortality rates in patients with COVID-19 [ 6 ]. As previously reported in recent pandemics [ 7 , 8 ], viral infections can also promote the development of bacterial invasive respiratory infections by impairing the immune response, enhancing the destruction of cells and tissue.

In the pandemic era, deaths and hospitalizations have been reported across all age groups, with a higher frequency in the elderly (> 60 years) patients [ 9 ]. SBIs have previously been reported in patients with COVID-19 [ 6 , 10 , 11 ]. It was recently shown that SBIs were observed in 15% of COVID-19 patients, while the SBIs were associated with 50% of all deaths [ 12 ]. Therefore, it is crucial to consider SBIs in order to improve the outcome of COVID-19. Consequently, patients with COVID-19 are treated with prophylactic broad-spectrum antibiotics in order to prevent and treat possible SBIs [ 13 – 16 ]. Recently, other approaches including phage therapeutics have been suggested as possible non-antibiotic treatment options [ 17 ].

Hygiene procedures such as hand hygiene, usage of disinfectants, personal protective equipment (PPE) are significantly changed due to the COVID-19 pandemic [ 18 ].

In environments where personnel and personal protective equipment (PPE) are insufficient, hygienic conditions may deteriorate, as well as increased use of PPE in interventions may prevent the increase of SBIs and the spread of common resistant bacterial strains. A previous study from Italy has suggested that lack of PPE, and lack of healthcare professionals associated with increased risk of spreading the carbapenem-resistant Klebsiella pneumoniae in the intensive care units (ICUs) [ 19 ].

It is important to evaluate the etiology and resistance patterns of SBIs as well as to compare the data with other patients before and during the pandemic. There is scarce data on SBI etiology and antimicrobial susceptibility data [ 10 , 16 ]. However, hitherto published studies have not analyzed the changes in AMR in patients with COVID-19 and controls. In addition, there is no published data from developing countries on SBIs where high AMR is prevalent. The data is crucial for establishing effective antibiotic therapy as well as avoiding unnecessary treatment [ 20 ].

In this study, we aimed to evaluate the etiologies of SBIs and co-infections and AMR profiles of the bacterial pathogens causing these infections in patients with COVID-19. Also, our secondary aim was to reveal the differences in the AMR between patients with COVID-19 and other patients from the pre-pandemic and pandemic era.

Study design

This study was performed at Ege University Hospital, Izmir, with a total of 2426 patient beds. The study covers the data between December 15, 2019, and June 15, 2020, which can be considered as the preceding three months, and the first three months of the COVID-19 pandemic in Turkey.

Study population

Covid-19 group.

During the pandemic peak for SARS-CoV-2, real-time reverse transcription PCR (RT-PCR) assay positive and negative patients with symptoms consistent with COVID-19 were included. The RT-PCR assay negative patients had radiological imaging findings meeting the Ministry of Health's probable case [ 21 ] criteria for COVID-19 and therefore were included in the COVID-19 patient group (Additional file 2 ). SBIs are defined as infections occurring two days or more after patients were admitted to the hospital. Infections occurring not more than two days of hospitalization were defined as co-infections.

Control group

This study included two control groups, i.e., one pre-pandemic era group with clinical microbiology culture results registered between December 15, 2019–March 15, 2020, and one pandemic era group with microbiology culture results registered between March 15, 2020–June 15, 2020, with no clinical and/or laboratory diagnosis of COVID-19 (Fig.  1 ).

An external file that holds a picture, illustration, etc.
Object name is 12941_2021_454_Fig1_HTML.jpg

Flow chart of the study population.* A total of 1447 COVID-19 patients were studied and 85 had bacterial infections

Laboratory methods

Bacterial culture.

The investigation of bacterial pathogens in clinical samples was conducted with standard procedures as requested by the attending physician and was evaluated by microbiologists (Additional file 1 ). Identification and antimicrobial susceptibility testing of the isolates were performed using MALDI-TOF MS (Matrix-Assisted Laser Desorption/Ionization-Time of Flight Mass Spectrometry) (BioMérieux, France) and VITEK 2 (BioMérieux, France) automated systems, respectively. For viridans group streptococci, Haemophilus spp., Corynebacterium striatum , Streptococcus pneumoniae, and Stenotrophomonas maltophilia , the international Kirby Bauer disk diffusion method was used. All the susceptibility results were evaluated in accordance with the EUCAST criteria [ 22 ]. When imipenem or meropenem resistance was detected in Enterobacterales strains with the automated system, the result was confirmed by gradient test (BioMérieux, France). Antibiotic MIC values were confirmed by gradient test when isolates were determined resistant to vancomycin, teicoplanin, linezolid, tigecycline with VITEK 2 automated system. The VITEK 2 cefoxitin screen test was used to detect MRSA strains. Only one isolate per patient was studied.


For PCR tests, DirectDetect™ SARS-CoV-2 Detection Kit (Coyote Bioscience Co, China) and Bio-Speedy SARS-COV2 (2019-nCoV) qPCR Detection Kit (Bioeksen R&D Technologies Ltd, Turkey) was used and according to the manufacturers’ recommendations. The PCR tests were performed with Qiagen Rotorgene Q-5 Plex-HRM Thermal Cycler (Qiagen, Belgium).

Data collection

Blood, respiratory tract, urinary tract, and other samples such as gastrointestinal tract, tissue, normally sterile fluids cultures sent from patients were evaluated and susceptibility test results were collected from the microbiology laboratory database.

Statistical analysis

Statistical analyses were performed using Microsoft Excel 2016 and IBM SPSS Statistics Version 18.0 (IBM Corp, Armonk, NY). Cross tables were created for categorical variables and chi-square analysis was performed. Categorical variables were shown as numbers and %, numerical variables as median (min., max.). A. baumannii changes between different groups were analyzed with two-tailed Fisher's exact test. Other comparisons (e.g., etiological changes, multidrug-resistant bacteria changes) were done with two-tailed Pearson's chi-squared test. A p value < 0.05 was considered statistically significant.

Ethical approval

This study has been approved by the Ege University Medical Research Ethics Committee (20–9T/75) and Turkish Ministry of Health.

In total, 4859 culture-positive samples from 3532 patients were studied. The samples were collected between December 15, 2019, and June 15, 2020. The pre-pandemic era control group consists of 3034 samples from 2143 patients and the pandemic era control group included 1702 samples from 1304 patients. 1447 COVID-19 diagnosed patients’ data were evaluated separately, and 85 of them had 123 bacterial infections.

Of the 2143 patients in the pre-pandemic group, 1057 (49.32%) were female, 1086 (50.68%) were male, and the median age of these patients was 52 (0–99 years). Of the 1304 patients in the pandemic group, 630 (48.31%) were female, 674 (51.69%) were male, and the median age of these patients was 55 (0–100 years). 85 patients evaluated as COVID-19 patients, 45 (52.94%) were female and 40 (47.06%) were male and the median age of the patients was 61 (9 months-99 years). The mortality rate was 25.88% in COVID-19 patients who had been diagnosed with bacterial infections and 64 (38–96 years) was the median age among deaths.

Pre-pandemic control group

During the three months before the pandemic (December 15, 2019–March 15, 2020), microbiological data from 2143 patients were evaluated, and 3034 culture-positive samples were detected. Strains were mostly isolated from urine (1472, 48.52%), respiratory tract samples (e.g., sputum, bronchoalveolar lavage) (540, 17.32%), and blood samples (442, 14.57%). Other isolated samples came from different tissue samples such as wound swabs and sterile body fluids (455, 14.9%), stool (96, 3.1%), cerebrospinal fluid (29, 0.9%). The most common strains were Escherichia coli (766, 23.55%), K. pneumoniae (324, 11.56%), and Pseudomonas aeruginosa (254, 8.37%) (Fig.  2 .). Extended-spectrum beta-lactamase ESBL-producing Enterobacterales were the most common (630, 20.76%) MDR bacteria among the strains isolated from these samples.

An external file that holds a picture, illustration, etc.
Object name is 12941_2021_454_Fig2_HTML.jpg

Etiology of the bacterial infections RTI: Respiratory Tract Infections UTI: Urinary Tract Infections BSI: Bloodstream Infections Other: Bacterial gastroenteritis, tissue infections, and infections in sterile body fluid

Pandemic era control group

Microbiological data from 1304 patients were evaluated and 1702 culture-positive samples were included in the pandemic era control group. Strains were obtained from urine (796, 46.77%), blood (276, 16.22%), lower respiratory tract samples (261, 15.33%), and others (e.g., feces, tissue, and sterile fluid). The most common isolated strains were E. coli (447, 26.26%), K. pneumoniae (197, 11.57%), and P. aeruginosa (136, 7.99%) (Table ​ (Table1). 1 ). ESBL-producing Enterobacterales were the most common (353, 20.74%) type of MDR strain, followed by carbapenem-resistant Enterobacterales (CRE) (62, 3.64%).

Bacterial strains detected in patients with COVID-19 and controls

# N = numbers, * p < 0.05, *** p = 0.001

COVID-19 patients

The existence of bacterial infections in 1447 COVID-19 patients (both inpatient and outpatient) were evaluated. In total, 52/1447 (3.59%) patients had SBIs and 38/1447 (2.62%) had bacterial co-infections. Bacterial isolates were detected in 123 clinical samples. A secondary bacterial infection developed in five patients with bacterial co-infection during their follow-up. 28 (32.94%) patients had multiple bacterial, and 57 (67.05%) patients had mono-bacterial infections. The most common MDR organisms were ESBL-producing Enterobacterales (11, 8.94%) (Fig.  3 ).

An external file that holds a picture, illustration, etc.
Object name is 12941_2021_454_Fig3_HTML.jpg

The most common multidrug-resistant isolates . ESBL: Extended-spectrum beta-lactamase CRE: Carbapenem-resistant Enterobacterales VRE: Vancomycin-resistant Enterococcus MRSA: Methicillin-resistant Staphylococcus aureus

In total, 78/123 (63.41%) bacterial strains were obtained two days after hospitalization of the patients and described as hospital-acquired infections while 45/123 (36.59%) were community-acquired infections. The most common bacteria was A. baumannii (10, 9.76%) among all respiratory tract samples (Table ​ (Table2 2 ).

Strains isolated from COVID-19 patients

UTI Urinary Tract Infections, RTI Respiratory Tract Infections, BSI Bloodstream Infections, Other Feces, tissue, and sterile fluid

a Four Stenotrophomonas maltophilia , three Enterobacter cloacae , three Proteus mirabilis , three Streptococcus agalactiae , two Streptococcus pneumoniae, two Staphylococcus haemolyticus , one Staphylococcus epidermidis, one Corynebacterium spp, one Corynebacterium pseudodiphtheriticum, one Corynebacterium propinquum, one Campylobacter coli, one Acinetobacter junii, one Elizabethkingia meningoseptica, one Haemophilus influenzae non-type B, one Morganella morganii, one Pseudomonas stutzeri, one Pseudomonas putida, one Salmonella enterica subsp. enterica, one Streptococcus pyogenes. All the strains and bacterial profiles of patients were shown in Additional file 3

Viral respiratory infections have been associated with an increased risk of bacterial infections. During the 2009 H1N1 outbreak, within 72 h of intensive care unit (ICU) admission, 30.3% of cases had bacterial co-infection [ 23 ]. Pandemics and seasonal flu data suggest that bacterial infections can worsen viral diseases and causes severe outcomes. Patients receiving invasive mechanical ventilation in other SARS and MERS epidemics developed secondary infections and had higher mortality [ 24 ] .

In the present study, 2.62% of patients with COVID-19 had bacterial co-infections whereas 3.59% of them had secondary bacterial infections. In total, 22/85 (25.88%) COVID-19 patients with bacterial infections died. Recent studies from Turkey showed that the overall mortality rate in patients with COVID-19 is 4.5% [ 25 , 26 ]. Therefore, it is reasonable to suggest that bacterial infections are related to higher mortality rates in patients with COVID-19. UTI was the most common infection type (45.5%) and followed by RTI (39.02%) which was significantly higher than the two control groups. Previous studies analysing SBIs in patients with COVID-19 are contradictory. He et al . showed that 50% of the patients with COVID-19 had a SBI or carried bacterial pathogens [ 27 ]. However, in a recent meta-analysis, it was reported that the SBI rate in COVID-19 patients was between 4.7 and 19.5% and was associated with an increased risk of severe course or fatal outcomes [ 28 , 29 ]. The underlying reason for low bacterial infection rates in the present study is not known. It might be related to several factors including the severity of the disease in patients included prior antimicrobial therapy or stringent local hygiene protocols applied during the pandemic era [ 30 ]. The observation of 3.59% of SBI suggests that empiric antibiotic treatment may not be necessary for all COVID-19 patients, since proven bacterial infections are relatively rare.

The most common pathogens in the COVID-19 study group were E. coli (22, 17.89%), K. pneumonieae (15, 12.2%), A. baumannii (12, 9.76%), and S. aureus (11, 8.94%). Detection of E. coli (22, 17.89%) was significantly lower in patients with COVID-19, compared to the pandemic era control group (447, 26.26%) (p = 0.04). In contrast, detection of A. baumannii in patients with COVID-19 was higher than in the two control groups.

In lower respiratory tract infections, the most detected pathogens were Gram-negative bacteria (32, 66.66%), following by Gram-positive bacteria (16, 33.33%). In Gram-negative bacteria, the most common isolated strains were A. baumannii (10/32, 31.25%), followed by P. aeruginosa (5/32, 15.63%) . Among Gram-positive bacteria, S. aureus (7/16, 43.75%) was the most common isolated strain. Although the distribution of Gram-negative and Gram-positive bacteria were similar, a higher A. baumannii occurrence as observed in our COVID-19 study group and needs further evaluation with comprehensive clinical data. A recent study from China showed that the most common bacterial pathogens isolated from respiratory tract samples were Gram-negative bacteria (26, 65%), following by Gram-positive bacteria (14, 34.99%). In that study, the most common bacterial pathogens encompassed K. pneumoniae (n = 11), E. faecium (n = 9), followed by A. baumannii (n = 8) [ 6 ]. The underlying reason for discrepant results between the present study and the previous report might be associated with differences in colonisation of bacteria types between centers, patients’ clinical profile as well as administration of prophylactic antibiotics.

ESBL-producing Enterobacterales were significantly lower in COVID-19 compared to pre-pandemic (p = 0.001) and pandemic era control group (p = 0.002). In a recent study which is reported from Egypt, Gram-negative isolates were mostly ESBL- or carbapenemase-producers which differs from our study [ 31 ]. The distinction may be due to the difference in the drug resistance profile between countries and/or local hygiene measures taken for patients with COVID-19. MDR A. baumannii was the most common bacteria (9.76%) in respiratory tract samples (39.02%) from COVID-19 patients, and this rate was significantly higher than that in the pre-pandemic (3.49%) (p = 0.002) and pandemic (3.11%) (p = 0.001) era control groups. In another study from New Jersey, when COVID-19 cases surge, increased carbapenem-resistant A. baumannii (CRAB) counts were reported. CRABs were mostly observed among COVID-19 patients admitted to ICUs and receiving ventilation therapy [ 32 ]. In both cases, the increase in intervention needed for COVID-19 patients may have led to a deterioration in hygiene conditions and an increase in the spread of MDR A. baumannii.

The present study has some limitations. First, not all COVID-19 patients were confirmed by PCR to be SARS-CoV-2 positive, and the comprehensive clinical data and disease severity of these patients were not studied. Secondly, a limited number of patients were available in our single-center study. However, we followed the official guidelines for the diagnosis of COVID-19, and it is highly unlikely that the patients with typical COVID-19 radiological findings had other infections. The lack of clinical severity data might be important, but the study focuses on the description of the prevalence of microorganisms and AST results in patients with COVID-19 in general. In addition, the sample size covers a period of 3 months in the pandemic era. The study has the following strengths: First, unlike other studies, we compared both the prevalence of bacterial infections and antimicrobial resistance patterns in patients with COVID-19 and control groups. Also, this study is the first comparative study presented from Turkey which is a developing country with a general high MDR bacteria profile.

In conclusion, the present study shows that SBIs and bacterial coinfections were low in COVID-19 patients; but when present, it causes severe outcomes and is related to mortality. With these results, the administration of empirical broad spectrum antimicrobials to COVID-19 patients should be evaluated more carefully as the excessive use of antimicrobials could lead to a surge of antimicrobial resistance [ 33 ]. Also, while it was observed that COVID-19 patients had a lower risk of infected with ESBL-producing Enterobacterales ; a significant increase in the MDR A. baumannii rates and increase of respiratory tract samples was observed and needs further evaluation. The present study will have an impact on diagnosis, possible treatments, and evaluating the existing sanitation measures in the hospitals. Further studies with larger sample size and detailed clinical data are warranted.

Authors' contributions

ŞA and VÖ presented the main conceptual ideas. ŞA, VÖ, MYD, MK designed the study. MK, MYD performed the analyses, wrote the first draft, and revised with FÇ, AT, ŞA, VÖ. ŞA and VÖ supervised the findings of this work. All authors read and approved the final manuscript.

Open access funding provided by Karolinska Institute. The author(s) received no specific funding for this work.

Availability of data and materials


This study has been approved by the Ege University Medical Research Ethics Committee (20 – 9T / 75) and Turkish Ministry of Health. Informed consent was waived by the Ethics Committee because of the retrospective nature of the study. The analysis was done with totally anonymous data.

Not applicable.

This study was waived by the Ethics Committee because of the retrospective nature of the study. The analysis was done with totally anonymous data.

The authors have no conflicts of interest to declare.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Şöhret Aydemir and Volkan Özenci contributed equally to this work

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Health Care-Associated Infection Prevention Outcomes: Evaluating the Link Between Infection Prevention Practices in Healthcare Facilities and their Health Care-Associated Infection Rates

Chidinma Veronica Njoku Follow

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Degree name.

Master of Health Administration (MHA)

Health Care Administration and Policy

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Neeraj Bhandari

Second Committee Member

Josue Epane

Third Committee Member

Fourth committee member.

Catherine Dingley

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Healthcare-associated infections (HAI) are a pressing problem affecting vulnerable individuals who come to the hospital to receive care for one condition only to find that they have contracted another during their stay. Studies point to the importance of training and educating staff in order to implement and comply with recommended infection control and prevention control and prevention practices as lack of training and knowledge about infection control and prevention has been perceived to bring about a limited ability for direct care staff to adhere to recommended processes and activities. Although there are prior studies on the effects of assessments, infection control practices, and audits on the reduction of healthcare associated infections, there is little research tying facility structure, resources, and practices with HAI rates of facilities.

The purpose of this research is to discover if there is an association between infection control practices of healthcare facilities, their reported HAI rates and outbreaks of notifiable disease. Datasets for analysis will include: National Healthcare Safety Network (NHSN) data, Infection control assessments result from Nevada facilities, health care facility outbreak data (length of outbreak, etiologic agent, the month of outbreak, etc.), nursing home compare data, and hospital compare data as it related to the study. Once the link is better understood, this information can be utilized in assessing and developing more effective infection prevention measures for healthcare facilities.

The Donabedian framework was used to examine and evaluate the structure, process, and outcome of infection control practices. In this study, structure elements and process elements are shown to influence outcome.

Healthcare Associated Infection; Healthcare Policies; Infection Control practice; Infection prevention; Infection rate; Nosocomial infection

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University of Nevada, Las Vegas

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Njoku, Chidinma Veronica, "Health Care-Associated Infection Prevention Outcomes: Evaluating the Link Between Infection Prevention Practices in Healthcare Facilities and their Health Care-Associated Infection Rates" (2019). UNLV Theses, Dissertations, Professional Papers, and Capstones . 3831. http://dx.doi.org/10.34917/18608740

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A proposal for a comprehensive approach to infections across the surgical pathway

  • Massimo Sartelli   ORCID: orcid.org/0000-0003-3202-7542 1 ,
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Despite evidence supporting the effectiveness of best practices in infection prevention and management, many healthcare workers fail to implement them and evidence-based practices tend to be underused in routine practice. Prevention and management of infections across the surgical pathway should always focus on collaboration among all healthcare workers sharing knowledge of best practices. To clarify key issues in the prevention and management of infections across the surgical pathway, a multidisciplinary task force of experts convened in Ancona, Italy, on May 31, 2019, for a national meeting. This document represents the executive summary of the final statements approved by the expert panel.

Prevention and management of infections across the surgical pathway should always focus on collaboration among all healthcare professionals with shared knowledge and widespread diffusion of best practices.

Leading international organizations, such as the World Health Organization (WHO), acknowledge that collaborative practice is essential for achieving a concerted approach to providing care that is appropriate to meet the needs of patients, thus optimizing individual health outcomes and overall service delivery of healthcare [ 1 ].

To clarify key issues in the prevention and management of infections across the surgical pathway, a multidisciplinary task force of national experts convened in Ancona, Italy, on May 31, 2019, for a national meeting. The multifaceted nature of these infections has led to a multidisciplinary collaboration involving epidemiologists and infection control specialists, infectious disease specialists, hospital pharmacists, microbiologists, intensivists, general and emergency surgeons, and nurses. During the meeting, the panelists presented the statements developed for each of the main questions regarding the prevention and management of infections in surgery. An agreement on the statements was reached by the Delphi method. Statements were approved with an agreement of ≥ 80%. After the meeting, the expert panel met via email to prepare and revise the consensus paper resulting from the meeting. The manuscript was successively reviewed by all members and ultimately revised as the present manuscript. This document represents the executive summary of the final statements approved by the expert panel.

Healthcare-associated infections and patient safety

Improving patient safety in hospitals worldwide presently requires a systematic approach to preventing healthcare-associated infections (HAIs) and antimicrobial resistance (AMR). The two go together. HAIs are infections that occur while receiving healthcare. Patients with medical devices (central lines, urinary catheters, ventilators) or who undergo surgical procedures are at risk of acquiring HAIs.

The occurrence of HAIs continues to escalate at an alarming rate. These infections result in significant patient illnesses and deaths, prolong the duration of hospital stay, and necessitate additional diagnostic and therapeutic interventions, which generate supplementary costs to those already sustained due to the patient’s underlying disease. However, the phenomenon is not yet sufficiently perceived among both healthcare workers (HCWs) and patients, thus resulting in a low level of intervention request and relative inadequate responses [ 2 ]. Although HAIs are the most frequent adverse events in healthcare, their true global burden remains unknown because of the difficulty in gathering reliable data: most countries lack surveillance systems for HAIs, and those do have them struggle with the complexity and the lack of uniformity of criteria [ 3 ].

HAIs are considered adverse events, and as many are preventable, they are considered an indicator of the quality of patient care and a patient safety issue. In 2018, a systematic review and meta-analysis of studies between 2005 and 2016 evaluated the results of multifaceted interventions to reduce catheter-associated urinary tract infections (CAUTIs), central line-associated bloodstream infections (CLABSIs), surgical site infections (SSIs), ventilator-associated pneumonia, and hospital-acquired pneumonia not associated with mechanical ventilation in acute care or long-term care settings [ 4 ]. Of the 5226 articles identified, 144 studies were included in the final analysis. Published evidence suggested a sustained potential for the significant reduction of HAI rates in the range of 35–55% associated with multifaceted interventions irrespective of a country’s income level.

Question 1. How can you implement global guidelines for the prevention of surgical site infections (SSIs)?

Statement 1.1. Recent global guidelines for the prevention of SSIs can support healthcare workers to develop or strengthen infection prevention and control programs, with a focus on surgical safety, as well as AMR action plans. All healthcare workers should adopt these evidence-based recommendations in their clinical practice.

Statement 1.2. A safer surgical care requires a range of precautions aimed at reducing the risk of SSIs before, during and after surgery.

Statement 1.3. To support local implementation of guidelines for the prevention of SSIs, 5 steps of a multimodal strategy, including system change, training and education, evaluation and feedback, communications for awareness raising and institutional safety climate and culture are suggested.

Improving behavior in infection prevention and control (IPC) practices remains a challenge. Despite progress in preventive knowledge, SSIs remain the most common HAI among surgical patients and one of the most frequent adverse events in hospitals. They represent a major clinical problem in terms of morbidity, mortality, length of hospital stay, and overall direct and not direct costs worldwide. It is obviously important to improve patient safety by reducing the occurrence of SSIs. Preventing SSIs is a global priority, also because bacteria are becoming increasingly resistant to antibiotics, making SSI prevention even more important nowadays. On the other hand, SSI prevention is complex and requires the integration of a range of measures before, during, and after surgery.

Both WHO [ 5 , 6 ] and the Centers for Disease Control and Prevention (CDC) [ 7 ] have published guidelines for the prevention of SSIs. The 2016 WHO Global guidelines for the prevention of SSI [ 5 , 6 ] are evidence-based including systematic reviews presenting additional information in support of actions to improve practice. The first-ever global guidelines for the prevention of SSIs were published on November 3, 2016, then were updated in some parts and published in a new edition in December 2018. The guidelines include 13 recommendations for the preoperative period and 16 for preventing infections during and after surgery. They range from simple precautions such as ensuring that patients bathe or shower before surgery, appropriate way for surgical teams to clean their hands, guidance on when to use prophylactic antibiotics, which disinfectants to use before incision, and which sutures to use.

The proposed recommendations are classified as follows:

“Strong”: Expert panel was confident that benefits outweighed risks, considered to be adaptable for implementation in most (if not all) situations, and patients should receive intervention as a course of action.

“Conditional”: Expert panel considered that benefits of intervention probably outweighed the risks; a more structured decision-making process should be undertaken, based on stakeholder consultation and involvement of patients and healthcare professionals.

In 2018, WHO published a document about the implementation approaches for these evidence-based recommendations [ 8 ]. The purpose of this document is to present a range of tested approaches to achieve successful SSI prevention implementation at the facility level, including in the context of a broader surgical safety climate, using an evidence- and team-based approach and a multimodal strategy for achieving sustainable change based on system change, training and education, evaluation and feedback, communications for awareness raising, and institutional safety climate and culture. The manual is aimed at all those concerned with the prevention of SSIs. A multidisciplinary team is necessary to successfully implement preventive measures. This should include at least IPC and associated staff, such as those working in epidemiology, decontamination/sterilization, quality improvement and patient safety, hospital administration, and the surgical teams (including surgeons, anesthesiologists, and perioperative nurses).

Question 2. Why do you have to survey HAIs?

Statement 2.1. Surveillance of HAIs improves the quality of care because it reduces the risk of infection. It should be supported by all healthcare workers.

IPC program should be in place to prevent HAIs in all hospitals worldwide, and one of the main cornerstones is the presence of a formal system to monitor IPC and ensure that appropriate actions are taken to minimize infection rates [ 9 ]. HAI surveillance is a challenging task also because it requires particular expertise after obtaining epidemiological data to assess the quality of the information produced and to interpret its meaning and root cause in order to tailor intervention and prevention measures.

Program surveying SSIs have been implemented throughout the world and are associated with a reduction in SSI rates. Data on non-prosthetic surgery from the Italian SSI surveillance program for the period 2009 to 2011 [ 10 ] demonstrated that implementation of a national surveillance program was helpful in reducing SSI rates and should be prioritized in all healthcare systems. A 17% decrease in SSI related to ten selected procedures was reported between 2008 and 2013 in the USA following improvement programs [ 11 ]. In African hospitals, a 60% SSI risk reduction was observed following the implementation of a WHO multimodal strategy in the context of the WHO Surgical Unit-based Safety Program (SUSP) including SSI surveillance [ 12 ]. Surveillance also allows hospitals and clinicians to measure the effectiveness of strategies that are implemented to decrease infection rates. Infection rate data should be used in a positive way to improve the quality and safety of healthcare.

HAI surveillance is conventionally conducted by two methods. Passive surveillance (self-reporting of suspected HAIs by the treating physicians) is a very poor and inefficient method to track HAIs as there is a risk of bias and underreporting. Active surveillance, on the other hand, is the systematic collection of data by a designated unbiased surveillance team. This is the method recommended by the main surveillance networks. Following the data extraction, analysis of the collected information should be done. Feedback and reports after the analysis should be disseminated by infection control committees, keeping the confidentiality of individuals. The importance of surveillance systems for HAI control has been accepted globally, and some countries have established national surveillance systems with the aim to prevent HAIs.

Question 3. How can you implement the prevention of HAIs?

Statement 3.1. It is necessary to set up a solid and branched surveillance network gathering alert signals, verifying their severity and initiating the organizational response via “warnings”.

Statement 3.2. The collection and analysis of monitoring data serve to identify vulnerabilities in the system. This is the basis for organizational improvement, risk reduction, and damage control.

HAIs affect around 5–15% of all hospital patients worldwide. Despite the availability of standard procedures and evidence-based guidelines aiming at reducing the impact of HAIs, the implementation of those into routine practice appears as the biggest challenge [ 13 ].

HAI surveillance and timely feedback of results are strongly recommended by WHO as part of the core components of effective IPC programs [ 14 ]. Every healthcare facility should be committed to provide quality and safe care. Surveillance is not to be undertaken in isolation, but as integrated into a comprehensive and multimodal IPC strategy. Conducting high-quality IPC and surveillance is crucial to assess the safety level of the surgical workflow, detect criticalities, and diffuse warnings to trigger the response capability of healthcare organizations. Feedback on IPC achievements should be constantly monitored and timely disseminated throughout the levels of the organization by the hospital IPC [ 15 ]. Surveillance of HAIs is a fundamental aspect of the IPC program, in particular, when SSIs are identified as a target for improvement.

Particularly in surgical care, SSI surveillance provides feedback to surgical teams on the HAI risks patients are exposed to. Cooperation of surgical teams in surveillance efforts is crucial to make visible to them the effect on patients’ care, if they have confidence in the methods being used. Thus, it is important for surgeons to comprehend the opportunities of the surveillance process for surgical care improvements [ 15 ]. In this regard, the support of human factors and ergonomics paired with implementation science is crucial to embed the knowledge gained through an epidemiological into the daily routine of HCWs [ 16 ].

Question 4. How can you prevent and manage Clostridioides difficile infection (CDI)?

Statement 4.1. Key points for CDI prevention are:

Antimicrobial stewardship.

Contact precautions.

Hand washing (soap, not alcohol).

Avoid unnecessary gastric acid suppressants.

Statement 4.2. Key points for CDI treatment are:

Stop unnecessary antibiotics.

Metronidazole (mild episodes).

Oral/intracolonic vancomycin.

Oral fidaxomicin.

IV bezlotoxumab (recurrent episodes).

Fecal microbiota transplantation.

Prompt surgery when indicated.

In the last two decades, CDI has become a major global public health problem, with a dramatic increase in the incidence and severity of episodes. CDI may be a particular concern in surgical patients, as surgery may predispose patients to CDI and surgery itself could be necessary to treat severe cases of CDI [ 17 ].

Risk factors for CDI may be divided into three general categories [ 17 ]:

Host factors (immune status, co-morbidities)

Exposure to C. difficile spores (hospitalizations, community sources, long-term care facilities)

Factors that disrupt normal colonic microbiome (antibiotics, other medications, surgery)

The main risk factors are antibiotic exposure, age more than 65 years, comorbidity or underlying conditions, inflammatory bowel diseases, immunodeficiency (including human immunodeficiency virus infection), malnutrition, and low serum albumin level. Antibiotics play a central role in the pathogenesis of CDI, presumably by disrupting the normal gut flora, thereby providing a perfect setting for C. difficile to proliferate and produce toxins. Although nearly all antibiotics have been associated with CDI, clindamycin, third-generation cephalosporins, penicillins, and fluoroquinolones have usually been considered at greatest risk [ 16 ].

A prompt and precise diagnosis is an important aspect of effective management of CDI. Early identification of CDI allows the establishment of an early treatment and can improve outcomes. Rapid isolation of infected patients is fundamental to limit C. difficile transmission. This is particularly important in reducing environmental contamination as spores can survive for months in the environment, despite regular use of environmental cleaning agents. Patients with CDI should be maintained in contact (enteric) precautions until the resolution of diarrhea (passage of formed stool for at least 48 h). Patients with known or suspected CDI should ideally be placed in a private room with en suite hand washing and toilet facilities. If a private room is not available, as often occurs, known CDI patients may be cohort, nursed in the same area, though the theoretical risk of transfection with different strains exists. Hand hygiene with soap and water and the use of contact precautions along with a good cleaning and disinfection of the environment and patient equipment should be used by all HCWs contacting any patient with known or suspected CDI. Alcohol-based hand sanitizers are highly effective against non-spore-forming organisms, but they may not kill C. difficile spores or remove C. difficile from the hands. The most effective way to remove them from the hands is through handwashing with soap and water.

In cases of suspected severe CDI, antibiotic agents should be discontinued, if possible [ 18 ]. A meta-analysis addressing factors associated with prolonged symptoms and severe disease due to C. difficile showed that continued use of antibiotics for infections other than CDI is significantly associated with an increased risk of CDI recurrence [ 18 ]. If continued antibiotic therapy is required for the treatment of the primary infection, antimicrobial therapy with agents that are less frequently implicated with antibiotic-associated CDI should be used; these include parenteral aminoglycosides, sulfonamides, macrolides, vancomycin, or tetracycline/tigecycline.

Although there is a clinical association between proton pump inhibitor (PPI) use and CDI [ 19 ], no randomized controlled trial (RCT) studies have studied the relationship between discontinuing or avoiding PPI use and the risk of CDI. Thus, a strong recommendation to discontinue PPIs in patients at high risk for CDI regardless of the need for PPIs will require further evidence. However, stewardship activities to discontinue unneeded PPIs are strongly warranted.

Regarding treatment, antibiotic therapy is the first choice for CDI treatment and molecule choice should be based according to the severity of the disease. When antibiotic therapy is indicated for symptomatic cases with a positive stool C. difficile test, options include metronidazole, oral or intraluminal vancomycin, and oral fidaxomicin [ 20 , 21 , 22 , 23 , 24 ]. Metronidazole should be limited to the treatment of an initial episode of mild-moderate CDI. Vancomycin orally 125 mg four times daily for 10 days is considered superior to metronidazole in severe CDI [ 25 , 26 , 27 ]. Doses of up to 500 mg have been used in patients with severe or fulminant, as defined as hypotension or shock, ileus, or megacolon, CDI [ 28 ], although there is little evidence for this in the literature. Fidaxomicin orally 200 mg twice daily for 10 days may be a valid alternative to vancomycin in patients with CDI [ 29 , 30 ]. Fidaxomicin may be useful for treating patients who are considered at high risk for recurrence (elderly patients with multiple comorbidities who are receiving concomitant antibiotics).

Fecal microbiota transplantation (FMT) is an effective option for patients with multiple CDI recurrences who have failed appropriate antibiotic treatments [ 31 ]. FMT involves infusing intestinal microorganisms (in a suspension of healthy donor stool) into the intestine of patients to restore the intestinal microbiota. The rationale of FMT is that disruption of the normal balance of colonic flora allows C. difficile strains to grow and produce CDI. By reintroducing normal flora via donor feces, the imbalance may be corrected and normal bowel function re-established [ 31 ].

Coadjuvant treatment with monoclonal antibodies (bezlotoxumab) may prevent recurrences of CDI, particularly in patients with CDI due to the 027 epidemic strain, in immunocompromised patients and in patients with severe CDI. Bezlotoxumab (MK-6072), approved in 2016 by Food and Drug Administration (FDA), is a human monoclonal antibody which reduces recurrent CDI by blocking the binding of C. difficile toxin B to host cells, thus limiting epithelial damage and facilitating recovery of the microbiome [ 32 ].

Patients with severe CDI who progress to systemic toxicity should undergo early surgical consultation and should be evaluated for potential surgical intervention. Resection of the entire colon should be considered to treat patients with fulminant colitis. However, diverting loop ileostomy with colonic lavage is a useful alternative to resection of the entire colon.

Question 5. How can you prevent central-venous catheter-related infections?

Statement 5.1. The most effective means to reduce to the minimum possible central-venous catheter-related infections are represented by a «bundles» management, based on the guidelines, implemented with training and motivational meetings aimed at increasing compliance of healthcare workers (better if organized in a dedicated team) and applied by checklist.

In order to guarantee a correct management of central venous catheter-related infections, a correct diagnostic framework is essential, to be obtained by a standardized execution of blood cultures from a peripheral vein and central venous catheter (CVC), in order to be able to implement a correct interpretation of the results and take timely decisions on a possible removal/conservative strategy towards the catheter.

About half of nosocomial bloodstream infections occur in intensive care units (ICUs), and the majority of them are associated with an intravascular device. Central venous catheter-related bloodstream infections (CRBSIs) are an important cause of HAIs. CVCs are integral to modern clinical practices and are inserted in critically ill patients for the administration of fluids, blood products, medication, and nutritional solutions and for hemodynamic monitoring. They are the main source of bacteremia in hospitalized patients and therefore should be used only if necessary.

Risk factors for CRBSIs include patient-, catheter-, and operator-related factors. Several factors have been proposed to participate in the pathogenesis of CRBSI. Hospitalized patients with neutropenia are at higher risk. However, other host risk factors also include immune deficiencies in general, chronic illness, and malnutrition. The diagnosis of CRBSI is often suspected clinically in a patient using a CVC who presents with fever or chills, unexplained hypotension, and no other localizing sign. Diagnosis of CRBSI requires establishing the presence of bloodstream infection and demonstrating that the infection is related to the catheter. However, blood cultures should not be drawn solely from the catheter port as these are frequently colonized with skin contaminants, thereby increasing the likelihood of a false-positive blood culture. Indeed, according to IDSA guidelines [ 33 ], a definitive diagnosis of CRBSI requires a culture of the same organism from both the catheter tip and at least one percutaneous blood culture. Alternatively, the culture of the same organism from at least two blood samples (one from a catheter hub and the other from a peripheral vein or second lumen) meeting criteria for quantitative blood cultures or differential time to positivity. Most laboratories do not perform quantitative blood cultures, but many laboratories are able to determine the differential time to positivity. Quantitative blood cultures demonstrating a colony count from the catheter hub sample ≥ 3-fold higher than the colony count from the peripheral vein sample (or a second lumen) supports a diagnosis of CRBSI. Differential time to positivity refers to growth detected from the catheter hub sample at least 2 h before growth detected from the peripheral vein sample. The CVC and arterial catheter, if present, should be cultured and removed as soon as possible if the patient has unexplained sepsis or erythema overlying the catheter insertion site or purulence at the catheter insertion site in immunocompromised patients.

Antibiotic therapy for catheter-related infection is often initiated empirically. The initial choice of antibiotics will depend on the severity of the patient’s clinical disease, the risk factors for infection, and the likely pathogens associated with the specific intravascular device. Resistance to antibiotic therapy due to biofilm formation also has an important role in the management of bacteremia. In fact, the nature of the biofilm structure makes microorganisms difficult to eradicate and confer an inherent resistance to antibiotics.

CRBSIs can be reduced by a range of interventions including closed infusion systems, aseptic technique during insertion and management of the central venous line, early removal of central venous lines, and appropriate site selection. Different measures have been implemented to reduce the risk for CRBSI, including the use of maximal barrier, precautions during catheter insertion, effective cutaneous anti-sepsis, and preventive strategies based on inhibiting microorganisms originating from the skin or catheter hub from adhering to the catheter [ 34 ]. The simultaneous application of multiple recommended best practices to manage CVCs has been associated with significant declines in the rates of CRBSI. Bundles can be defined as the systematic implementation of a set of evidence-based practices, usually three to five, that when performed properly and collectively can improve patient outcomes. Research on CRBSI prevention demonstrated the effectiveness of bundles, which reduce the incidence of CRBSI by up to 80% [ 35 , 36 , 37 ], reaching a rate of 0 in some cases [ 38 ]. Education and training of healthcare workers and adherence to standardized protocols for insertion and maintenance of intravascular catheters significantly reduced the incidence of catheter-related infections and represent the most important preventive measures.

The global burden of antimicrobial resistance

AMR has emerged as one of the principal public health problems of the twenty-first century. This has resulted in a public health crisis of international concern. Combating resistance has become a top priority for global policymakers and public health authorities. New mechanisms of resistance continue to emerge and spread globally, challenging our ability to manage common infections. Antibacterial and antifungal use in animal and agricultural industries aggravates selective pressure on microbes. A One Health approach is required urgently. Addressing the rising threat of AMR requires a holistic and multisectoral approach—referred to as One Health—because antimicrobials used to treat various infectious diseases in animals may be the same or similar to those used for humans. Resistant bacteria arising in humans, animals, or the environment may spread from one to another and from one country to another. AMR does not recognize geographic or human-animal borders [ 39 ].

The worldwide impact of AMR is significant, in terms of economic and patient outcomes, because of untreatable infections or those necessitating antibiotic agents of last resort leading to increased length of hospital stay, morbidity, death, and treatment cost. Raising awareness of AMR and promoting behavioral change through public communication programs that target different audiences in human health, animal health, and agricultural practice, as well as consumers, are critical to tackling this issue.

HCWs play a central role in preventing the emergence and spread of resistance. An effective and cost-effective strategy to reduce AMR should involve a multifaceted approach aimed at optimizing antibiotic use, strengthening surveillance and IPC, and improving patient and clinician education regarding the appropriate use of antibiotic agents.

Although the phenomenon of AMR can be attributed to many factors, there is a well-established relationship between antimicrobial prescribing practices and the emergence of antimicrobial-resistant pathogens. However, after they have emerged, resistant pathogens may be transmitted from one individual to another. Every infection prevented is one that needs no treatment. Prevention of infection can be cost-effective and implemented in all settings and sectors, even where resources are limited. A range of factors such as diagnostic uncertainty, fear of clinical failure, time pressure, or organizational contexts can complicate both antibiotic prescribing decisions and preventing measures. Because of cognitive dissonance (recognizing that action is necessary but not implementing it), however, changing behavior is extremely challenging, and awareness of AMR is still low.

Every hospital worldwide should utilize the existing resources to create an effective multidisciplinary team for combating AMR. The best strategies for combating AMR are not definitively established and are likely to vary based on local culture, policy, and routine clinical practice despite several guidelines on the topic.

The Italian situation

In a study published in January 2019 in The Lancet Infectious Diseases, the European Center for Disease Prevention and Control (ECDC) assessed the weight of infections due to multiresistant bacteria in invasive isolates in Europe [ 40 ].

Elaborating the 2015 data contained in the European Antimicrobial Resistance Surveillance Network (EARS-Net) and crossing them with a conversion factor, the authors arrived at the first estimate of the impact of antibiotic resistance on the European population. The authors estimate that infections caused by multiresistant bacteria can cause at least 33,000 deaths each year in Europe (equal to the sum of deaths caused by influenza, AIDS, and tuberculosis) and almost 880.000 cases of disability. Italy and Greece have the most infections from multiresistant bacteria. Although we consider that the Italian population is of a medium-high age, it is noteworthy that about a third of deaths due to antibiotic-resistant bacterial infections in Europe have been in Italy. Not surprisingly, in December 2017, the ECDC published a report on the Italian situation and activities for the prevention and control of antibiotic resistance [ 41 ]. The report summarizes visits and meetings that ECDC experts had in Italy from January 9 to 13, 2017, to discuss and specifically assess the situation in the country regarding antibiotic-resistance prevention and control in our country. Observations of this visit by the ECDC confirm that the antibiotic resistance situation in Italian hospitals will represent a serious threat to public health for the country in the near future.

ECDC experts noted the following:

Little sense of urgency about the current AMR situation from most stakeholders and a tendency by many stakeholders to avoid taking charge of the problem

Lack of institutional support at the national, regional, and local level

Lack of professional leadership at each level

Lack of accountability at each level

Lack of coordination of the activities between and within levels

According to a report by the Organization for Economic Co-operation and Development (OECD) [ 42 ], in Italy, the proportion of antibiotic-resistant infections have grown from 17% in 2005 to 30% in 2015 and will reach 32% in 2030, if antibiotic consumption will continue to follow the same trends. The proportion of antibiotic resistance in Italy is substantially higher than that in the 17% average resistance of OECD countries in 2015.

On November 2, 2017, the Ministry of Health published the national anti-microbial resistance plan (PNCAR) 2017–2020 [ 43 ], which identified strategies and actions to be implemented at different levels: national, regional, and local. The PNCAR is developed according to a One Health approach. The actions set out in the plan, at the level of central, regional, and local institutions, pursue specific objectives:

Improve awareness and education of health professionals, citizens, and stakeholders

Monitor the phenomenon of antibiotic resistance and the use of antibiotics

Improve IPC

Optimize the use of antimicrobials in the field of human and animal health

Increase and support research and innovation.

Appropriate management of infections across the surgical pathway

Antibiotics can be life-saving when treating bacterial infections but are often used inappropriately. Although most clinicians are aware of the problem of AMR, most underestimate this problem in their own hospital. Clinicians should always optimize antimicrobial management to maximize the clinical outcome of the patients and minimize the emergence of AMR. The necessity of formalized systematic approaches to the optimization of antibiotic therapy in the setting of surgical units worldwide, both for elective and emergency admissions, has become increasingly urgent.

Below, we report 11 strategies for a correct antibiotic therapy.

Communication and education.

Updating local epidemiological data stratifying them for specific settings.

Start and choice treatment always using a severity driven approach.

Drafting local algorithms / bundles.

Avoid redundant prescriptions.

Not being impulsive in starting antimicrobial therapy.

Being parsimonious with combination regimens.

Strict collaboration with microbiology laboratory in daily life.

Being aware about PK/PD issues.

Shortening therapy.

Creating a multidisciplinary team for specific setting, syndromes, etc.

Hospital-based programs dedicated to improving antibiotic use, commonly referred to as Antimicrobial stewardship programs (ASPs), can both optimize the treatment of infections and minimize adverse events associated with antibiotic use and AMR [ 44 , 45 ]. Every hospital worldwide should utilize the existing resources to create an effective multidisciplinary team. The preferred means of improving antibiotic stewardship should involve a comprehensive program that incorporates collaboration between various specialties within a healthcare institution including infectious disease specialists, hospital pharmacists, clinical pharmacologists, administrators, epidemiologists, IPC specialists, microbiologists, surgeons, anesthesiologists, intensivists, and underutilized but pivotal stewardship team members, the surgical, anesthetic, and intensive care nurses in our hospitals.

Antimicrobial stewardship policies should be based on both international and national antibiotic guidelines and tailored to local microbiology and resistance patterns. Facility-specific treatment recommendations, based on the guidelines and local formulary options promoted by the antimicrobial stewardship team, can guide clinicians in antibiotic selection and duration of the therapy for the most common indications. Standardizing a shared protocol of antibiotic prophylaxis should represent the first step of any ASP. Since physicians are primarily responsible for the decision to use antibiotics, educating them and changing the attitudes and knowledge that underlie their prescribing behavior are crucial for improving antibiotic prescription. Education is fundamental to every ASP; however, due to cognitive dissonance (recognizing that action is necessary but not implementing it), changing the prescribing behavior is extremely challenging [ 46 ]. Efforts to improve educational programs are thus required, and this should preferably be complemented by active interventions such as prospective audits and feedback to clinicians to stimulate further change [ 47 ]. It is also crucial to incorporate fundamental ASP and IPC principles in under- and post-graduate training at medical faculties to equip young doctors and other healthcare professionals with the required confidence, skills, and expertise in the field of antibiotic management.

Question 6. The clinical microbiology laboratory: which is its role in the control of infections with multidrug-resistant bacteria?

Statement 6.1. The implementation of microbiological diagnostic activities improves the diagnostic capacity towards infections caused by multidrug-resistant organisms (MDROs).

Statement 6.2. The three main challenges of a modern microbiology laboratory are: to maintain high-quality services, to consolidate laboratory medical care into large hospital systems and, as a consequence of consolidation to reach a full automation possibly in all the analytical steps of the diagnosis.

ASPs and prescribing physicians depend on the information and guidance from the clinical microbiology laboratory, thus making the laboratory vital to patient care and the success of ASPs. The three most relevant challenges of a modern microbiology laboratory are the following.

Maintaining high-quality and cost-effective services

ASPs aid physicians in providing optimal antimicrobial therapy to their patients, prescribing the right antimicrobial regimen to the right patient for the right period of time, and avoiding the unnecessary use of antimicrobial. Ultimately, ASPs aim to improve patient outcomes while limiting adverse drug events and reducing AMR. The clinical microbiology laboratory plays a critical role in the success of the antimicrobial stewardship efforts by providing essential information for accurately diagnosing and treating patients with infectious diseases [ 48 ].

Clinical microbiology laboratories (CMLs) conduct surveillance on the local AMR trends among microbial pathogens. The collection, organization, and communication of resistance data culminates could be summarized in the preparation of the antibiogram. Antibiograms provide critical information to ASPs and to prescribing physicians on local institution susceptibility patterns. CMLs provide patient-specific information by identifying the microbial pathogens and performing the antimicrobial susceptibility testing. This information is necessary so that empiric antimicrobial therapy can be shortened and substituted by a pathogen-driven approach. Over the past decade, there have been several advances in rapid microbiological diagnostic testing. Compared to standard techniques that require 48–72 h for final results, these methods can greatly reduce the time to pathogen identification by providing final organism identification within hours from the sample collection or, less efficiently, from the availability of an isolated bacterial colony by culture-based methods.

Consolidation of laboratory medical care into large hospital systems: consolidated hospital network systems open the possibility to merger microbiology diagnostic activities into larger laboratories

Many new innovative microbiological diagnostic approaches have been made available during the last 10 years with a major impact on patient care and public health surveillance [ 49 ]. In parallel, to enhance the cost-effectiveness of the CMLs, European laboratory professionals have streamlined their organization leading to the amalgamation of diagnostic activities and thus restructuring of their professional relationships with clinicians and public health specialists. Through this consolidation process, an operational model has emerged that combines large centralized CMLs performing a large panel and number of tests within a high-throughput analytical platform connected to several distal laboratories dealing locally with urgent analyses at the near point of care testing. The centralization of diagnostic services so that encompassing a large geographical region has given rise to the concept of regional-scale “microbiology laboratories network” or, in another word to “geographically spread laboratories.” Although the volume-driven cost savings associated with such laboratory networks seem self-evident, the consequences for the quality of patient care and infectious disease surveillance and control remain a challenge even if the fast-changing landscape of CMLs in Europe may give a range of opportunities to contribute to improving the quality of patient care but also the early detection and enhanced surveillance of public health threats caused by infectious diseases.

Full automation is currently being required to meet the needs of a changing healthcare system based on consolidated geographically spread microbiology laboratories

During the last decade, most CMLs have encountered many management and financial difficulties, mainly resulting from the gradual and continuous increase in sample volume with limited budgets and personnel shortages. Thus, laboratories have been forced to optimize their workflow to raise their productivity: this improvement must be accompanied by at least a maintained analytical quality, but possibly by an improved clinical value of the generated data. Automation was introduced many years ago in several diagnostic disciplines such as chemistry, clinical pathology, and hematology to increase laboratory productivity and quality. The automation process was by far more complicated in molecular biology and bacteriology settings: this was due to several reasons, including the complexity and variability of sample types, the many different analytical processes, and the insufficient volume of samples. However, the introduction of automation was considered to be also applicable in microbiology in more recent years thanks to the technological improvements currently available. Recently, these new technologies have triggered the development of automated solutions specifically designed for microbiology. In particular, the automation process has been applied to all the pre-analytical steps and to the evaluation of the results by using sophisticated artificial intelligence algorithms. The complete clinical laboratory automation is currently the main organizational challenge for microbiologists [ 50 ].

Question 7. How can you manage the patient with infection/colonization of multidrug-resistant organisms (MDROs)?

Statement 7.1. The application of contact isolation precautions is always recommended for patients known or highly suspected for MDROs.

MDROs including methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus (VRE), extended-spectrum β-lactamase (ESBL) producers, and Klebsiella pneumoniae -producing carbapenemase (KPC) pose significant public health challenges. The prevention and control of MDROs are a global priority.

Traditionally, hospitals have been considered the main reservoir of MDROs. Around 20–40% of nosocomial infections can be mainly attributed to cross-infection via the hands of healthcare personnel. Less frequently, patients can become colonized with nosocomial pathogens by direct contact with contaminated patient care equipment or contaminated surfaces in the healthcare environment [ 51 ].

Current strategies to address MDROs consist of the three following strategies [ 52 ]:

Developing new antimicrobial agents

Increasing antimicrobial stewardship efforts

Interrupting MDROs cross-transmission

Bacteria tend to inhabit specific sites on either in the human body or in the hospital environment which serve as reservoirs for transmission. The reservoirs of resistant organisms include niches in the human microbiome. The microbiota of the skin, respiratory epithelium, and the gastrointestinal tract are altered within a few days in the hospital. Patients’ flora can be deranged by antibiotics, chemotherapy, or acquisition of nosocomial organisms. Patients who are colonized with resistant bacteria serve inadvertently as potential reservoirs for transmission. Colonization pressure, or the proportion of patients in a given unit who are colonized with resistant bacteria, is an independent risk factor for transmission. Surveillance cultures for carbapenem-resistant Enterobacteriaceae (CRE) have been advocated in a number of reports and recommendations as part of an overall strategy to combat it. Active screening for CRE using rectal surveillance cultures has been shown to be highly effective, when part of a comprehensive infection control program, in halting the spread of CRE in healthcare facilities [ 53 ].

Isolation or cohorting of colonized/infected patients is a cornerstone of IPC. Its purpose is to prevent the transmission of microorganisms from infected or colonized patients to other patients, hospital visitors, and HCWs, who may subsequently transmit them to other patients or become infected or colonized themselves. Isolating a patient with highly resistant bacteria is beneficial in stopping the patient-to-patient spread. Isolation measures should be an integral part of any IPC program; however, they are often not applied consistently and rigorously, because they are expensive, time-consuming, and often uncomfortable for patients.

Facilities should have written policies and procedures that identify patients with MDROs and should require that contact precautions are implemented in all practice settings. Communication is a vital component for successful implementation of contact precautions and must occur at all points in the perioperative process.

Question 8. Antimicrobial stewardship: Is a multidisciplinary approach necessary?

Statement 8.1. The three basic requirements of an Antimicrobial Stewardship program are:

The existence of a multidisciplinary antimicrobial stewardship team.

A microbiological report on a fixed basis on the bacterial resistance of the hospital at least annually, if possible stratified by departments or at least for some key departments (e.g. Intensive Care Units).

A report on fixed consumption of antibiotics in the hospital.

Statement 8.2. A multidisciplinary antimicrobial stewardship team should be coordinated by an infectious disease specialist, or by another specialist with documented infectious skills.

Every hospital worldwide should utilize the existing resources to create an effective multidisciplinary team for combating AMR. The best strategies for combating AMR are not definitively established and are likely to vary based on local culture, policy, organization, and routine clinical practice despite several guidelines on the topic [ 44 ].

We propose that the best means of improving programs to contain AMR should involve collaboration among various specialties within a healthcare institution. They should focus on collaboration between all healthcare professionals to shared knowledge and widespread diffusion of practice. The involvement of HCWs may raise their awareness of AMR [ 44 ]. It is essential for any team to have at least one member who is an infectious disease specialist. Pharmacists with advanced training or long-standing clinical experience in infectious diseases are also key actors for the design and implementation of the stewardship program interventions monitoring consumption data of antibiotics. In any healthcare setting, a significant amount of energy should be spent on IPC. Infection control specialists and hospital epidemiologists should be always included in these programs to coordinate efforts on monitoring and preventing HAIs. Microbiologists should actively guide the proper use of tests and the flow of laboratory results. Being involved in providing surveillance data on AMR, they should provide periodic reports on AMR data allowing the multidisciplinary team to determine the ongoing burden of AMR in the hospital. Moreover, timely and accurate reporting of microbiology susceptibility test results allows the selection of more appropriate targeted therapy and may help reduce broad-spectrum antimicrobial use. Surgeons with adequate knowledge in surgical infections and surgical anatomy when involved may audit both antibiotic prescriptions and prevention practices, provide feedback to the prescribers and integrate best practices of antimicrobial use among surgeons, and act as champions among colleagues implementing change within their own sphere of influence. Infections are the main factors contributing to mortality in ICUs. Intensivists have a critical role in treating multidrug-resistant organisms in ICUs in critically ill patients. They have a crucial role in prescribing antimicrobial agents for the most challenging patients and are at the forefront of successful antibiotic prescribing policies. Emergency departments (EDs) represent a particularly important setting for addressing inappropriate antimicrobial prescribing practices, given the frequent use of antibiotics in this setting that sits at the interface of the community and the hospital. Therefore, also ED practitioners should be involved. Without adequate support from hospital management, these programs will be inadequate or inconsistent since the programs do not generate revenue. Engagement of hospital management has been confirmed as a key factor for both developing and sustaining. Finally, an essential participant who has been often unrecognized and underutilized is the “staff nurse” as nurses perform numerous functions that are integral to success.

Question 9. Why and how do you have to monitor antibiotics consumption in the hospitals?

Statement 9.1. It is important to monitor antibiotics consumption. The data of the consumption data of antibiotics should be expressed in specific reports in defined daily doses.

Pharmacy’s contribution to ASPs has significantly evolved over the course of the twenty-first century. Although microbiologists and infection specialist physicians have been conventionally responsible for providing advice on clinical management of infected patients, many pharmacists in clinical practice have now established roles complementing the expertise in multidisciplinary antimicrobial stewardship teams.

Pharmacists’ responsibilities for antimicrobial stewardship include promoting the optimal use of antimicrobial agents. Typical interventions include patient-specific recommendations on therapy; the implementation of policies, education, therapeutic drug monitoring, and participation in antimicrobial stewardship ward rounds [ 54 , 55 ].

Antibiotics are prescribed in up to a third of hospital inpatients, often inappropriately [ 56 ], and more than two thirds of critically ill patients are on antibiotics at any given time during their hospital admission [ 57 ]. Antibiotic use is one of the most important parameters for assessing the impact that an ASP has on a hospital and its patient population, although microbiological resistance and clinical outcomes are also important measures. Antimicrobial measures looking at consumption are the most commonly used measures and are focused on defined daily dose (DDD), usually standardized per 1000 patient-days.

DDD is a metric that was developed in the 1970s and has been further refined and promoted by the WHO Collaborating Centre for Drug Statistics Methodology. DDD is described as “the assumed average maintenance dose per day for a drug used for its main indication in adults” [ 58 ]. In simple terms, a DDD is the amount of drug that a typical patient might receive on any day for therapeutic purposes. An important advantage of using DDDs is the relative ease of hospital systems to report consumption using DDDs: most pharmacy departments have a mechanism to calculate overall prescription, dispensing, or consumption of a quantity of antimicrobials, allowing DDDs/1000 patient-days to be relatively easy to calculate if bed utilization is also available. Additionally, institution-wide consumption can be benchmarked against similar institutions. The landmark guidelines on antimicrobial stewardship by the Infectious Diseases Society of America and Society for Healthcare Epidemiology of America advocated for DDDs/1000 patient-days as a universal metric for hospital-based ASPs [ 59 ].

Question 10. What is the role for the nurse in preventing HAIs?

Statement 10.1. The nurse is an integral part of the multidisciplinary team for the prevention of infections across the surgical pathway.

Statement 10.2. It is important to implement educational and training interventions concerning the prevention of SSIs by following a modality appropriate to the level of education of the patient/caregiver.

The role of the professional nurse in preventing HAIs is significant. The nurse is a member of the healthcare team who leads the rest of the team in practicing prevention strategies to protect the patient from infection [ 60 ]. Some of the most basic strategies resulting in positive patient outcomes include the following:

The practice and promotion of hand hygiene

Consistent use of aseptic technique

Cleaning and disinfection practices

Use of standard precautions

Patient assessment and additional precautions

Patient education

Use of safety devices

Removal of unnecessary invasive devices

Use of bundle strategies for infection prevention

Fit for duty

Nurses play a pivotal role in preventing hospital-acquired infections (HAIs), not only by ensuring that all aspects of their nursing practice are evidence-based, but also through patient education. One of the most important roles nurses have today is patient education. This was once reserved for the physician, but no longer. Today nurses assume more and more responsibility for educating patients and helping them to become responsible for their own health status. Patients need to take a proactive role in their own healthcare. This means they need to comprehend their health status and work to stabilize and prevent or minimize complications such as HAIs. Demographic variables, such as formal education level, reading ability, and barriers to participation in education, must be considered to maximize the effectiveness of self-management education outcomes. Hospital nurses can best educate patients by understanding that discharge planning begins with admission. Nurses have to ensure patients are effectively educated throughout their hospitalization so that they are prepared to care for themselves and participate in the care pathway.

Question 11. Which are the principles of antibiotic prophylaxis?

Statement 11.1. Prolonging antibiotic prophylaxis after surgery is generally not associated with better clinical results.

Statement 11.2. There is no universally recognized intervention for improving the appropriateness of antibiotic prophylaxis in surgery. These interventions must be tailored to the type of surgeon and team to which they are addressed.

Preoperative antibiotic prophylaxis (PAP) has been demonstrated in multiple randomized controlled trials and meta-analyses to reduce the risk of SSIs across different types of surgical procedures [ 61 ].

Given the evidence, systemic PAP is considered to be a key component of perioperative infection prevention bundles [ 62 ]. Although compliance with appropriate timing and spectrum of PAP has improved as a result of quality improvement initiatives, there remain significant deficiencies in compliance with other aspects of PAP such as duration of postoperative antibiotics [ 63 , 64 ]. Given that approximately 15% of all antibiotics in hospitals are prescribed for surgical prophylaxis [ 65 , 66 ], perioperative antibiotic prescribing patterns can be a major driver of some emerging infections (such as C. difficile ) [ 67 , 68 ] and selection of antibiotic resistance, increasing healthcare costs.

Although appropriate PAP plays a pivotal role in reducing the rate of SSIs [ 69 ], other factors that impact SSI rates should not be ignored. PAP should never substitute for good medical practices, such as those of IPC. Perioperative SSI prevention strategies should include attention to basic IPC strategies, surgical technique, hospital and operating room environments, instrument sterilization processes, and perioperative optimization of patient risk factors [ 70 ].

The key elements of appropriate surgical antimicrobial prophylaxis prescribing include the correct antimicrobial indication, drug dose, route, the timing of administration, and duration.

Joint guidelines for PAP in surgery were revised and updated in 2013 by the American Society of Health-System Pharmacists, Infectious Diseases Society of America, Surgical Infection Society, and Society for Healthcare Epidemiology of America [ 68 ]. These guidelines focus on the effective and safe use of AP. Therapeutic serum and tissue concentrations of antimicrobial agents should be present during the period of potential contamination. Additional antibiotic doses may need to be administered intraoperatively for prolonged procedures or for agents with short half-lives. In order to be safe, PAP should have no or few adverse effects and should have the narrowest spectrum of activity necessary to prevent postoperative infections.

There is no evidence that prolonging PAP after surgery can reduce the risk of SSIs. A single preoperative dose is adequate for the majority of procedures. Post-procedural doses of intravenous antibiotics (up to 24 h) may be only required in defined circumstances, such as some cardiac and vascular surgeries.

Below, seven practices for a correct surgical antibiotic prophylaxis are illustrated [ 71 ]:

Antibiotics alone are unable to prevent SSIs. Strategies to prevent SSIs should always include attention to the following:

IPC strategies including correct and compliant hand hygiene practices

Meticulous surgical techniques and minimization of tissue trauma

Hospital and operating room environments

Instrument sterilization processes

Perioperative optimization of patient risk factors

Perioperative temperature, fluid, and oxygenation management

Targeted glycemic control

Appropriate management of surgical wounds

Antibiotic prophylaxis should be administered for operative procedures that have a high rate of postoperative SSI, or when foreign materials are implanted.

Antibiotics given as prophylaxis should be effective against the aerobic and anaerobic pathogens most likely to contaminate the surgical site, i.e., Gram-positive skin commensals or normal flora colonizing the incised mucosae.

Antibiotic prophylaxis should be administered within 120 min prior to the incision. However, administration of the first dose of antibiotics beginning within 30–60 min before the surgical incision is recommended for most antibiotics (e.g., cefazolin), to ensure adequate serum and tissue concentrations during the period of potential contamination. Obese patients ≥ 120 kg require higher doses of antibiotics.

A single dose is generally sufficient. Additional antibiotic doses should be administered intraoperatively for procedures > 2–4 h (typically where duration exceeds two half-lives of the antibiotic) or with associated significant blood loss (> 1.5 L).

There is no evidence to support the use of postoperative antibiotic prophylaxis.

Each institution is encouraged to develop guidelines for the proper surgical prophylaxis.

Knox and Edye [ 63 ] demonstrated that an educational ASP was ineffective in changing surgical prophylactic antibiotic prescribing in an Australian hospital. Although that study was disappointing as far as showing improved behaviors, others have shown that ASPs may have a significant impact on optimizing antibiotic use in surgical prophylaxis practices [ 72 , 73 ]. Van Kasteren et al. [ 73 ] in a prospective multisite study of elective procedures in 13 Dutch hospitals evaluated the quality of prophylaxis auditing before and after an intervention consisting of performance feedback and implementation of national clinical practice guidelines. Antimicrobial use decreased from 121 to 79 DDD/100 procedures, and costs reduced by 25% per procedure. After the intervention, antibiotic choice was inappropriate in only 37.5% of the cases instead of 93.5% expected cases in the absence of any intervention. Prolonged prophylaxis was observed in 31.4% instead of 46.8% expected cases and inappropriate timing in 39.4% instead of the expected 51.8%. Time series analysis showed that all improvements were statistically significant ( P < 0.01). The overall SSI rates before and after the intervention were 5.4% (95% CI 4.3–6.5) and 4.6% (95% CI 3.6–5.4), respectively [ 73 ]. Huh et al. [ 72 ] performed an interrupted time-series study of an ASP relating to surgical prophylaxis in a tertiary care hospital. The ASP consisted of monitoring of performance indicators and implementation of a computerized decision support system. The program was effective in improving multiple measures including the total use of antibiotics, the use of third-generation cephalosporins and aminoglycosides, trends in proportions of resistant bacterial strains such as meropenem-resistant Pseudomonas aeruginosa , and length of stay. Saied et al. [ 12 ] implemented ASPs in 5 tertiary, acute-care surgical hospitals. The ASPs consisted of education aimed at surgeons and anesthesiologists, audit and feedback, and selection of surgeon champions. The efficacy of the intervention on timing and duration of antibiotic prophylaxis varied across hospitals when measured pre- and post-ASP implementation. Local factors such as available resources and stakeholder engagement likely play a role in the conflicting results of ASPs addressing surgical prophylaxis across different settings, as seen in these studies.

Question 12. Which are the principles of antibiotic therapy?

Statement 12.1. It is important to know the local epidemiological context to define therapeutic protocols / guidelines for surgical infections treatment.

Statement 12.2. It is important to frame clinical conditions, in particular to differentiate between critical and non-critical patients.

Statement 12.3. It is important to pursue as much as possible targeted therapy or in any case a de-escalation in order to preserve some molecules: e.g.: carbapenems.

Statement 12.4. It is important to assess properly the duration of therapy based on source control.

Statement 12.5. In the setting of uncomplicated intra-abdominal infections including uncomplicated acute cholecystitis and acute appendicitis post-operative antimicrobial therapy is not necessary.

Statement 12.6. In patients with complicated intra-abdominal infections, when patients are not severely ill and when source control is complete, a short course (3-5 days) of post-operative therapy is suggested.

Statement 12.7. In patients with ongoing or persistent intra-abdominal infections, the decision to continue, revise, or stop antimicrobial therapy should be made on the basis of clinician judgment and laboratory information.

Empirical antibiotic therapy should be based on local epidemiology, individual patient risk factors for difficult-to-treat pathogens, clinical severity of infection, and infection source. Initial antibiotic therapy for surgical infections is empirical in nature because microbiological data (culture and susceptibility results) may require > 24/48 h before they are available for a more detailed analysis. However, the results direct expansion of antimicrobial regimen if it is too narrow and perform a de-escalation if it is too broad [ 74 , 75 ], particularly in critically ill patients where de-escalation strategy is one of the cornerstones of ASPs [ 76 ]. The principles of empiric antibiotic treatment should be defined according to the most frequently isolated microbes, always taking into consideration the local trend of antibiotic resistance. In this era of prevalent drug-resistant microorganisms, the threat of resistance is a source of major concern that cannot be ignored [ 76 ].

In the past 20 years, the incidence of intra-abdominal infections (IAIs) caused by MDROs has risen dramatically [ 76 ]. Quinolone resistance, prevalence of ESBL-producing bacteria, prevalence and mechanisms of carbapenem resistance in the local environment, and the place of recent traveling should be always taken into account when antibiotic therapy is administered empirically. Generally, the most important factors in predicting the presence of resistant pathogens are acquisition in a healthcare setting (particularly if the patient becomes infected in the ICU or has been hospitalized for more than 1 week), corticosteroid use, organ transplantation, baseline pulmonary or hepatic disease, and previous antimicrobial therapy [ 76 , 77 ].

Previous antibiotic therapy is one of the most important risk factors for resistant pathogens [ 78 ]. Inappropriate therapy in critically ill patients may have a strong negative impact on the outcome. An ineffective or inadequate antimicrobial regimen is one of the variables more strongly associated with unfavorable outcomes in critically ill patients. Broad empiric antibiotic therapy should be started as soon as possible in patients with organ dysfunction (sepsis) and septic shock [ 79 , 80 , 81 , 82 , 83 ]. International guidelines for the management of sepsis and septic shock (the Surviving Sepsis Campaign) recommend intravenously administered antibiotics as soon as possible and in any case within the first hour of onset of sepsis and the use of broad-spectrum agents with adequate penetration of the presumed site of infection [ 84 ].

The results of microbiological testing may have great importance for the choice of therapeutic strategy of every patient, in particular, in the adaptation of targeted antibiotic treatment. They provide an opportunity to expand the antibiotic regimen if the initial choice was too narrow but also allow de-escalation of antibiotic therapy if the empirical regimen was too broad. Antibiotic de-escalation has been associated with lower mortality rates in ICU patients and is now considered a key practice for antimicrobial stewardship purposes [ 75 ]. The duration of antibiotic therapy has been studied appropriately in the setting of intra-abdominal infections (IAIs).

In the event of uncomplicated IAIs, the infection involves a single organ and does not extend to the peritoneum. When the source of infection is treated effectively by surgical excision, postoperative antibiotic therapy is not necessary, as demonstrated in managing uncomplicated acute appendicitis or cholecystitis [ 85 , 86 , 87 ].

In 2015, an important prospective study on the appropriate duration of antibiotic therapy in patients with complicated IAIs was published [ 88 ]. The study randomized 518 patients with complicated IAIs and adequate source control to receive antibiotics until 2 days after the resolution of fever, leukocytosis, and ileus, with a maximum of 10 days of therapy (control group), or to receive a fixed course of antibiotics (experimental group) for 4 ± 1 calendar days. In patients with complicated IAIs who had undergone an adequate source control procedure, the outcomes after fixed-duration antibiotic therapy (approximately 4 days) were similar to those after a long course of antibiotics (approximately 8 days) that extended until after the resolution of physiological abnormalities. In this study, most patients were not severely ill.

The high mortality associated with abdominal sepsis requires clinicians to maintain a high index of clinical suspicion of treatment failure and the early diagnosis of ongoing infections. These patients should always be monitored carefully including the potential use of inflammatory response markers.

Below, we report 13 practices in an appropriate antibiotic therapy across the surgical pathway [ 71 ]:

The source of infection should always be identified and controlled as soon as possible.

Antibiotic empiric therapy should be initiated after a treatable surgical infection has been recognized, since microbiological data (culture and susceptibility results) may not be available for up to 48–72 h to guide targeted therapy.

In critically ill patients, empiric broad-spectrum therapy to cover all likely pathogens should be initiated as soon as possible after a surgical infection has been recognized . Empiric antimicrobial therapy should be narrowed once culture and susceptibility results are available and/or adequate clinical improvement is noted.

Empirical therapy should be chosen on the basis of local epidemiology, individual patient risk factors for MDR bacteria and Candida spp., clinical severity, and infection source.

Specimens for microbiological evaluation from the site of infection are always recommended for patients with hospital-acquired or with community-acquired infections at risk for resistant pathogens (e.g., previous antimicrobial therapy, prior infection or colonization with a multidrug-resistant, extensively drug-resistant, and pan-drug-resistant pathogens) and in critically ill patients. Blood cultures should be performed before the administration of antibiotics in critically ill patients.

Antibiotics dose should be optimized to ensure that pharmacokinetic-pharmacodynamic (PK-PD) targets are achieved. This involves prescribing of an adequate dose, according to the most appropriate and right method and schedule to maximize the probability of target attainment.

The appropriateness and need for antimicrobial treatment should be reassessed daily.

Once source control is established, short courses of antibiotic therapy are as effective as longer courses regardless of signs of inflammation.

Intra-abdominal infection: 4 days are as effective as 8 days in moderately ill patients.

Bloodstream infection: 5–7 days are as effective as 7–21 days for most patients.

Ventilator-associated pneumonia: 8 days are as effective as 15 days.

Failure of antibiotic therapy in patients having continued evidence of active infection may require a re-operation for a second source control intervention.

Biomarkers such as procalcitonin (PCT) may be useful to guide duration and/or cessation of antibiotic therapy in critically ill patients.

Clinicians with advanced training and clinical experience in surgical infections should be included in the care of patients with severe infections.

IPC measures, combined with ASPs, should be implemented in surgical departments. These interventions and programs require regular, systematic monitoring to assess compliance and efficacy.

Monitoring of antibiotic consumption should be implemented and feedback provided to all ASP team members regularly (e.g., every 3–6 months) along with resistance surveillance data and outcome measures.

Question 13. How can you manage invasive candidiasis in surgical patients?

Statement 13.1. It is important the knowledge of the risk of developing invasive candidiasis, improve microbiological diagnostics and optimize treatment .

Invasive candidiasis (IC) has a significant impact on morbidity, mortality, length of hospital stay, and healthcare costs in critically ill patients [ 89 ]. The overall mortality for these patients is high. Candidemia increases mortality rates in the range of 20–49% [ 90 ], and the attributable mortality has been calculated to be around 15% [ 91 ]. The severity of illness (APACHE II score > 10, ventilator use for > 48 h), antibiotics, central venous lines, total parenteral nutrition, burns, and immunosuppression are the most common risk factors [ 92 ].

The risk factors for IC are so numerous that most patients could be considered as exhibiting risk factors for IC. But, the use of excessive antifungal agents would be associated with substantially increased overall healthcare costs and might lead to the emergence of resistance. Unfortunately, early diagnosis of IC remains a challenge, and criteria for starting empirical antifungal therapy in ICU patients are poorly defined. To both ensure appropriate and timely antifungal therapy and to avoid unnecessary use of antifungal agents, some authors have developed clinical prediction rules to identify patients at high risk of candidiasis and for whom initiation of empirical antifungal therapy could be justified. However, there are many concerns about these rules: high specificity but low sensitivity. In 2006, a Spanish group, using the database of the Estudio de Prevalencia de CANdidiasis project, identified four predictors of proven invasive Candida infection. Based on these predictors, a score named “Candida score” (CS) was built. In 2009, the same group demonstrated a significant linear association between increasing values of the CS and the rate of invasive Candida infections [ 93 ]. The factors to predict IC were surgery, multifocal colonization, total parenteral nutrition, and severe sepsis. To each risk factor, 1 point was given, and for clinical sepsis, a score of 2 was given. The cutoff value of 2.5 had sensitivity of 81% and specificity of 74% [ 93 ]. Although blood cultures are still considered the gold standard for diagnosis, it has been shown that they are negative in up to 50% of cases [ 94 ]. Thus, non-culture diagnostic techniques based on serological biomarkers detecting fungal cell components and/or antibodies directed against these components have been investigated. All these diagnostic tests may diagnose IC earlier than clinical or culture-based measures.

Among the biomarkers, mannan antigen and antigen-antibody complex showed higher sensitivity and specificity when combined together [ 95 ]. In a meta-analysis of 14 studies, 7 of which were performed in non-neutropenic critically ill patients; the sensitivity and specificity of mannan and anti-mannan IgG were 58% and 93%, and 59% and 83%, respectively. Values for the combined assay were 83 and 86%, with the best performances for C. albicans , C. glabrata , and C. tropicalis infection [ 95 ]. The 1,3-beta- d -glucan (BG) is a fungal cell wall antigen that can be detected in the blood of patients with a sensitivity of 56–93% and a specificity of 71–100% for IC [ 96 ]. Thanks to its high negative predictive value, BG is potentially useful for the therapy decision-making process and discontinuing of empirical antifungal therapy. An integrated strategy with BG and CS helped to withhold or discontinue treatment, saving health costs without increasing mortality in 198 severely ill patients admitted to ICU with sepsis and a CS > 3 [ 97 ]. Once the diagnosis is made, early systemic treatment is warranted. The armamentarium of drugs for the treatment of candidiasis currently comprises 3 major drug classes: the polyenes, azoles, and echinocandins.

The majority of patients with candidemia have indwelling CVCs when the diagnostic blood culture is obtained [ 98 ], but differentiating between CVC- and non-CVC-related candidemia is not always straightforward. C. parapsilosis is particularly frequent as a cause of CVC infection. There is compelling evidence that CVC removal is associated with higher rates of treatment success and lower mortality rates as compared with CVC retention [ 98 ]. Despite contradictory data from a post hoc analysis of 2 clinical trials [ 98 ], it is generally accepted that indwelling CVCs should be removed as early as possible in all patients with candidemia [ 99 ]. CVCs should be urgently removed in patients with septic shock. For clinically stable patients for whom immediate CVC removal presents significant difficulties, for example, due to limited vascular access, establishing a diagnosis of CVC infection may be of importance.

Question 14. Which are the principles of antibiotic therapy in critically ill patients?

Statement 14.1. In critically ill patients, antibiotic therapy should be prescribed using a severity and risk stratification driven approach.

Statement 14.2. It is important to support the need for better identification of patients at risk of MDROs infection, more accurate diagnostic tools enabling a rule-in/rule-out approach for bacterial sepsis, the use of adequate dosing and administration schemes to ensure the attainment of pharmacokinetics/pharmacodynamics targets, concomitant source control when appropriate, and a systematic reappraisal of initial therapy in an attempt to minimize collateral damage on commensal ecosystems through de-escalation and treatment-shortening whenever conceivable.

The rapid global spread of multiresistant bacteria and loss of antibiotic effectiveness increases the risk of initial inappropriate antibiotic therapy (IAT) and poses a serious threat to patient safety especially in critically ill patients. A systematic review and meta-analysis of published studies to summarize the effect of appropriate antibiotic therapy or IAT against Gram-negative bacterial infections in the hospital setting was published in 2014 [ 100 ]. Using a large set of studies, the authors found that IAT is associated with a number of serious consequences, including an increased risk of hospital mortality.

Infections caused by drug-resistant, Gram-negative organisms represent a considerable financial burden to healthcare systems due to the increased costs associated with the resources required to manage the infection, particularly longer hospital stays. However, given the impact of early and broad-spectrum empirical therapy and the emphasis on this in international guidelines, there is a low threshold for initiating antibiotics in many patients with suspected infection. This has led to the widespread use of antibiotics in critically ill patients, which is often unnecessary or inappropriate [ 101 ].

The massive consumption of antibiotics in the ICU is responsible for substantial ecological side effects that promote the dissemination of MDROs. Strikingly, up to half of ICU patients receiving empirical antibiotic therapy have no definitively confirmed infection, while de-escalation and shortened treatment duration are insufficiently considered in those with documented sepsis.

Published data notably support [ 102 ] the following:

The need for better identification of patients at risk of MDROs infection

More accurate diagnostic tools enabling a rule-in/rule-out approach for bacterial sepsis

An individualized reasoning for the selection of single-drug or combination empirical regimen

The use of adequate dosing and administration schemes to ensure the attainment of PK-PD targets

Concomitant source control when appropriate

A systematic reappraisal of initial therapy in an attempt to minimize collateral damage on commensal ecosystems through de-escalation and treatment shortening whenever conceivable

Several trials found PCT-guided antibiotic stewardship to reduce antibiotic exposure and associated side effects among patients with respiratory infection and sepsis [ 103 ]. Decisions regarding antibiotic use in an individual patient are complex and should be based on the pre-test probability for bacterial infection, the severity of presentation, and the results of the PCT. In the context of a low pre-test probability for bacterial infections and a low-risk patient, a low PCT level helps to rule out bacterial infection and empiric antibiotic therapy can be avoided. In the context of a high pre-test probability for bacterial infections and/or a high-risk patient with sepsis, monitoring of PCT over time helps to track the resolution of infection and decisions regarding the early stop of antibiotic treatment. Although these concepts have been successful in several respiratory infection and sepsis trials, some studies failed to show an added benefit of PCT due to factors such as low protocol adherence and relying on single rather than repeat PCT measurements.

In this era of AMR, another interesting strategy is a therapeutic approach based on patient risk stratification. Especially for Gram-negative MDRO infections, an approach based on the patient risk stratification could improve outcomes and avoid antibiotic misuse.

This approach could help physicians to avoid antibiotic overuse as well as to start promptly with the most appropriate antibiotic regimen. Several risk factors for Gram-negative MDRO infections have been identified. These include prior infection or colonization with Gram-negative MDROs, antibiotic therapy in the past 90 days, poor functional status performance, hospitalization for more than 2 days in the past 90 days, occurrence five or more days after admission to an acute hospital, receiving hemodialysis, and immunosuppression [ 104 ]. Moreover, prior receipt of carbapenems, broad-spectrum cephalosporins, and fluoroquinolones has been associated specifically with MDR Pseudomonas aeruginosa [ 105 ].

Recently, the high mortality and mortality associated with multidrug-resistant Gram-negative bacteria along with limited treatment options have led to a resurgence in the use of the nephrotoxic drug colistin. Fortunately, several new antibiotic agents with activity against Gram-negative MDROs, including ceftazidime/avibactam and ceftolozane/tazobactam, have become available. Further studies are needed to elucidate their place in therapy and their impact on real-world outcomes such as length of stay and mortality, especially for ICU patients; however, these are the few resources we have and should not be wasted unnecessarily.

Question 15. Who is the surgeon champion?

Statement 15.1. To be a champion in preventing and managing infections in surgery means to create a culture of collaboration in which infection prevention, antimicrobial stewardship and correct surgical approach are of high importance.

There is sometimes a false impression that HAIs are adequately controlled. However, with multidrug-resistant bacteria increasing, such as MRSA, VRE, carbapenem-resistant Enterobacteriaceae (CRE), such infections are more than ever a public health threat. It is well known that HAIs tend to show higher resistance rates to antibiotics than community-acquired infections.

Patients in hospitals are often exposed to multiple risk factors for the acquisition of multidrug-resistant bacteria. Acute care facilities are important sites for the development of AMR. The intensity of care together with populations highly susceptible to infection creates an environment that facilitates both the emergence and transmission of resistant organisms.

Surgeons with satisfactory knowledge in surgical infections involved in both IPC team and in the ASPs may integrate the best practice among surgeons. Although the surgeon’s impact on the incidence of SSIs has not yet been examined in a comprehensive manner, some reports have reported that the incidence of SSIs varies widely between hospitals and between surgeons [ 106 , 107 ], suggesting that working practices play a critical role in the prevention of these infections and that more may be done to improve infection control in routine surgical practice.

Very few studies have focused on the relationship between ASPs and surgeons. In 2015, Çakmakçi [ 108 ] suggested that the engagement of surgeons in ASPs might be crucial to their success. However, in 2013, Duane et al. [ 109 ] showed poor compliance with surgical services with ASP recommendations. A retrospective study by Sartelli et al. [ 110 ] showed that implementation of an education-based ASP achieved a significant improvement in all antimicrobial agent prescriptions and a reduction in antimicrobial drug consumption. In a surgical unit performing mainly elective major abdominal surgery and emergency surgery, both a local protocol of surgical prophylaxis and a set of guidelines for the management of intra-abdominal infections (IAIs) and control of antimicrobial agent use were introduced. Comparing the pre-intervention and post-intervention periods, the mean total monthly antimicrobial use decreased by 18.8%, from 1074.9 defined DDDs per 1000 patient-days to 873.0 DDDs per 1000 patient-days after the intervention. The model was based on the concept of the “surgeon champion.” The “champion” was a surgeon who on a day-to-day basis worked within the surgical unit, promoting and maintaining a culture in which IPC appropriate use of antibiotics was of high importance. Identifying a local opinion leader to serve as a champion may be important because the “surgeon champion” may integrate the best clinical practices and drive the colleagues in changing behaviors. We believe that the concept of the “surgeon champion” can be a crucial way to improve IPC across the surgical pathway.

Question 16. Which are the principles of source control?

Statement 16.1. The timing and adequacy of source control are important in the management of surgical infections; late and/or incomplete procedures may have severely adverse consequences on outcome especially in critically ill patients.

Source control encompasses all measures undertaken to eliminate the source of infection, reduce the bacterial inoculum, and correct or control anatomic derangements to restore normal physiologic function [ 111 , 112 ].

As a general principle, every verified source of infection should be controlled as soon as possible. The level of urgency of treatment is determined by the affected organs, the relative speed at which clinical symptoms progress and worsen, and the underlying physiological stability of the patient. Non-operative interventional procedures include percutaneous drainages of abscesses. Ultrasound- and CT-guided percutaneous drainage of abdominal and extraperitoneal abscesses in selected patients are safe and effective. The principal cause for failure of percutaneous drainage is misdiagnosis of the magnitude, extent, complexity, and location of the abscess [ 113 ].

Surgery is the most important therapeutic measure to control surgical infections. In the setting of intra-abdominal infections, the primary objectives of surgical intervention include determining the cause of peritonitis, draining fluid collections, and controlling the origin of the abdominal sepsis. In patients with intra-abdominal infections, surgical source control entails resection or suture of a diseased or perforated viscus (e.g., diverticular perforation, gastro-duodenal perforation), removal of the infected organ (e.g., appendix, gallbladder), debridement of necrotic tissue, resection of ischemic bowel, and repair/resection of traumatic perforations with primary anastomosis or exteriorization of the bowel.

In certain circumstances, infection not completely controlled may trigger an excessive immune response and local infection may progressively evolve into sepsis, septic shock, and organ failure. Such patients can benefit from immediate and aggressive surgical re-operations with subsequent re-laparotomy strategies, to curb the spread of organ dysfunctions caused by ongoing peritonitis. Surgical strategies following an initial emergency laparotomy include subsequent “re-laparotomy on demand” (when required by the patient’s clinical condition) as well as planned re-laparotomy in the 36–48h postoperative period [ 114 ].

On-demand laparotomy should be performed only when absolutely necessary and only for those patients who would clearly benefit from additional surgery. Planned re-laparotomies, on the other hand, are performed every 36–48 h for purposes of inspection, drainage, and peritoneal lavage of the abdominal cavity. The concept of a planned re-laparotomy for severe peritonitis has been debated for over 30 years. Re-operations are performed every 48 h for reassessing the peritoneal inflammatory process until the abdomen is free of ongoing peritonitis; then the abdomen is closed. The advantages of the planned re-laparotomy approach are optimization of resource utilization and reduction of the potential risk for gastrointestinal fistulas and delayed hernias. The results of a clinical trial published in 2007 by Van Ruler et al. [ 115 ] investigating the differences between on-demand and planned re-laparotomy strategies in patients with severe peritonitis found few advantages for the planned re-laparotomy strategy; however, the study mentioned that this latter group exhibited a reduced need for additional re-laparotomies, decreased patient dependency on subsequent healthcare services, and decreased overall medical costs.

An open abdomen (OA) procedure is the best way of implementing re-laparotomies. Open abdomen (OA) procedure is defined as intentionally leaving the fascial edges of the abdomen unapproximated (laparostomy). The abdominal contents are exposed and protected with a temporary coverage. The OA technique, when used appropriately, may be useful in the management of surgical patients with severe abdominal sepsis [ 116 ]. However, the role of the OA in the management of severe peritonitis is still being debated. The role of the OA in the management of severe peritonitis has been a controversial issue [ 116 ]. Although guidelines suggest not to routinely utilize the open abdomen approach for patients with severe intra-peritoneal contamination undergoing emergency laparotomy for intra-abdominal sepsis, OA has now been accepted as a strategy in treating physiologically deranged patients with acute peritonitis.

Question 17. What is the role of the biomarkers in surgery?

Statement 17.1. C-reactive protein (CRP) and procalcitonin (PCT) can help clinicians to diagnose surgical infections.

Statement 17.2. PCT can help clinicians in early discontinuation of antibiotics in critically ill patients and in patients undergoing intervention for acute peritonitis.

Although more than a hundred biomarkers have been studied, only a limited number of them became routinely available in clinical practice. CRP and PCT are the more frequently studied and used biomarkers.

Serum CRP is an acute-phase protein synthesized exclusively in the liver. Its secretion is initiated 4 to 6 h after an inflammatory insult (effect mediated by cytokines namely interleukin-6), and its concentration doubles every 8 h with a peak at 36–50 h [ 117 ]. The sole determinant of CRP plasmatic levels is its synthesis rate, which is proportional to the intensity of the inflammatory insult. Its production and elimination are not influenced by renal replacement therapy or immunosuppression (both systemic steroids and neutropenia). It has a sensitivity of 68–92% and a specificity of 40–67% as a marker of bacterial infection. Its low specificity and inability to differentiate bacterial infections from non-infectious causes of inflammation make CRP of limited diagnostic value [ 118 ]. The available assays for CRP measurement are reliable, stable, reproducible, rapid, inexpensive, and present an acceptable limit of detection (0.3–5 mg/L). CRP has been analyzed in multiple clinical contexts, but only a small number of studies have focused on its use for optimizing antibiotic therapy [ 119 ]. In primary care, CRP improves the assessment of the severity of infection and extent of inflammation [ 120 ] and performs better in predicting the diagnosis of pneumonia than any individual or combination of clinical signs and symptoms. A Cochrane review [ 121 ] demonstrated reduced antibiotic prescription with CRP testing, which led to its incorporation in the National Institute for Health and Care Excellence (NICE) guidelines for the diagnosis of pneumonia. CRP has been reported to be useful in the diagnosis of appendicitis; however, it lacks specificity. Multiple studies have examined the sensitivity of CRP level alone for the diagnosis of appendicitis in patients selected to undergo appendectomy. Gurleyik et al. noted a CRP sensitivity of 96.6% in 87 of 90 patients with a histologically proven disease [ 122 ]. Similarly, Shakhatreh found a CRP sensitivity of 95.5% in 85 of 89 patients with histologically proven appendicitis [ 123 ]. Asfar et al. reported a CRP sensitivity of 93.6% in 78 patients undergoing appendectomy [ 124 ].

PCT is a precursor protein of calcitonin that can be produced ubiquitously throughout the body. It is released 3–4 h after an inflammatory stimulus with a plasmatic peak within 6–24 h and a half-life ranging from 22 to 35 h. Its plasmatic levels are markedly influenced by renal function, different techniques of renal replacement therapy, and neutropenia. It showed a sensitivity of 77% and a specificity of 79% for early diagnosis of sepsis in critically ill patients [ 117 , 118 ]. PCT is the most widely studied biomarker for antibiotic stewardship. It has been tested as an aid to the initiation and/or discontinuation of antibiotics, both in children and adults presenting with distinct sources of infection and in different scenarios. Multiple trials have investigated the benefits of using serum PCT levels to guide whether and for how long antibiotic therapy is used—a process referred to as a PCT-guided antibiotic stewardship—in patients with infection in the ICU [ 125 , 126 , 127 , 128 , 129 , 130 , 131 , 132 , 133 , 134 , 135 ]. Several studies have demonstrated the benefits of using serum PCT levels to guide antibiotic therapy in patients undergoing intervention for acute peritonitis [ 136 , 137 ].

Question 18. Who are the patients at high risk for surgical site infections?

Statement 18.1. A number of risk factors are known to increase the incidence of SSIs, they can be effective at three different levels: patient, operative (surgical procedure-related) and institutional level (hospital related).

Statement 18.2. Although multiple strategies exist for identifying surgical patients at high risk for SSIs, no one strategy is superior for all patients and further efforts are necessary to determine if risk stratification in combination with risk modification can reduce SSIs in this patients’ population.

SSIs are a significant healthcare quality issue, resulting in increased morbidity, disability, length of stay, mortality, resource utilization, and costs. Identification of high-risk patients may improve preoperative counseling, inform resource utilization, and allow modifications in perioperative management to optimize outcomes.

Many risk factors are beyond practitioner control, but optimizing perioperative conditions can certainly help decrease infection risk [ 138 ]. High-risk surgical patients may be identified on the basis of individual risk factors or combinations of factors. In particular, statistical models and risk calculators may be useful in predicting infectious risks, both in general and for SSIs. These models differ in the number of variables: inclusion of preoperative, intraoperative, or postoperative variables; ease of calculation; and specificity for particular procedures. Furthermore, the models differ in their accuracy in stratifying risk.

Although multiple strategies exist for identifying surgical patients at high risk for SSIs, no strategy is superior for all patients, and further efforts are necessary to determine if the risk stratification in combination with risk modification can reduce SSIs in this patient population [ 138 ].

Early evaluation of perioperative SSI risk factors and patient risk stratification could be of great value in the development of predictive risk models [ 139 ]. Predictive risk models could, in turn, assist surgeons and their patients in the clinical decision-making process (e.g., counseling patients on the appropriateness and risks of surgery). In addition, risk models could be used to develop targeted perioperative prevention strategies and diagnostic care process models and improve risk adjustment for risk modeling used in the public reporting of SSI as a quality metric [ 139 ].

However, a study reviewing SSIs in patients undergoing colorectal resections (C-SSIs), identified from an institutional ACS-NSQIP dataset (2006 to 2014), showed that published risk prediction models do not accurately predict C-SSI in their own independent institutional dataset [ 140 ]. Application of externally developed prediction models to any individual practice must be validated or modified to account for the institution and case-mix specific factors. This questions the validity of using externally or nationally developed models for “expected” outcomes and interhospital comparisons.

Question 19. How can you care post-operative wounds to prevent surgical site infections?

Statement 19.1. Advanced dressing of any type should not be used for primarily closed surgical wounds for the purpose of preventing SSI.

Statement 19.2. The surgical wound dressing can be removed for a minimum of 48 hours after surgery unless leakage occurs. There is no evidence that extending medication time implies a reduction in SSIs.

Appropriate surgical wound and incision management in the postoperative time period is imperative to prevent SSIs. The term “surgical wound” used in this document refers to a wound created when an incision is made with a scalpel or other sharp cutting device and then closed in the operating room by suture, staple, adhesive tape, or glue and resulting in a close approximation of the skin edges [ 141 ]. It is traditional to cover such wounds with a dressing, which acts as a physical barrier to protect the wound from contamination from the external environment until it becomes impermeable to microorganisms.

To assess the effects of wound dressings compared with no wound dressings, and the effects of alternative wound dressings, in preventing SSIs in surgical wound healing by primary intention, a Cochrane review was published in 2016 [ 142 ]. The authors concluded that it is uncertain whether covering surgical wound healing by primary intention with wound dressings reduces the risk of SSI, or whether any particular wound dressing is more effective than others in reducing the risk of SSI, improving scarring, reducing pain, improving acceptability to patients, or is easier to remove. Most studies in this review were small and at a high or unclear risk of bias. Based on the current evidence, decision-makers may wish to base decisions about how to dress a wound following surgery on dressing costs as well as patient preference.

The WHO Global Guidelines for the Prevention of SSIs [ 5 , 6 ] suggest not using any type of advanced dressing over a standard dressing on primarily closed surgical wounds for the purpose of preventing SSI. Low-quality evidence from ten RCTs shows that advanced dressings applied on primarily closed incisional wounds do not significantly reduce SSI rates compared to standard wound dressings. Postoperative care bundles recommend that surgical dressings be kept undisturbed for a minimum of 48 h after surgery unless leakage occurs [ 143 , 144 ].

Question 20. How can we engage surgeons in appropriate infection prevention and management?

Statement 20.1. Active education techniques, such as academic detailing, consensus building sessions and educational workshops, should be implemented in each hospital worldwide according to its own resources.

Statement 20.2. Surgeons with satisfactory knowledge in surgical infections should be involved in the infection control team and recognized as “champions” by the hospital's administration.

Surgeons should be involved in guideline development, and their implementation should translate practice recommendations into a protocol or pathway that specifies and coordinates responsibilities and timing for particular actions among a multidisciplinary team. Although both the WHO [ 5 , 6 ] and CDC [ 7 ] have recently published guidelines for the prevention of SSIs, knowledge and awareness of IPC measures among surgeons are often inadequate and a great gap exists between the best evidence and clinical practice with regards to SSI prevention.

Education is crucial in improving HCW behaviors towards HAIs. Effective prevention and management of HAIs is a process requiring a fundamental understanding of the evolving relationship between inappropriate prevention and management and the prevalence of HAIs and the emergence of AMR. However, because medical professionals have already established their knowledge, attitudes, and behaviors, it is difficult to change their deeply established views and behaviors. Increasing knowledge may influence their perceptions and motivate them to change behavior. Education and training represent an important component for the accurate implementation of recommendations. Education of all health professionals in preventing HAIs should begin at the undergraduate level and be consolidated with further training throughout the postgraduate years. Hospitals are responsible for educating clinical staff about IPC programs. Active education techniques, such as academic detailing, consensus building sessions and educational workshops, should be implemented in each hospital worldwide according to its own resources. Efforts to improve educational programs are required, and it is necessary that every hospital worldwide develops appropriate educational programs to drive HCWs towards correct behaviors in the prevention and management of HAIs. The purpose of training and educating healthcare professionals should be to ensure both individual understanding and a team approach with shared knowledge, skills, and attitudes towards the prevention and management of HAIs.

Peer-to-peer role modeling and champions on an interpersonal level have been shown to positively influence the implementation of infection control practices. Many practitioners use educational materials or didactic continuing medical education sessions to keep up to date. However, these strategies might not be very effective in changing practice, unless education is interactive and continuous and includes discussion of evidence, local consensus, feedback on performance (by peers), and making personal and group learning plans. Identifying a local opinion leader to serve as a champion may be important because the “champion” may integrate best clinical practices and drive the colleagues in changing behaviors, working on a day-to-day basis, and promoting a culture in which IPC is of high importance. Surgeons with satisfactory knowledge in surgical infections may provide feedback to the prescribers, integrate the best practices among surgeons and implement changes within their own sphere of influence interacting directly with the IPC team.

Raising awareness of IPC to stakeholders is another crucial factor in changing behaviors. Probably, clinicians are more likely to comply with the guidelines when they have been involved in developing the recommendations. One way to engage health professionals in guideline development and implementation is to translate practice recommendations into a protocol or pathway that specifies and coordinates responsibilities and timing for particular actions among a multidisciplinary team.


Leading international organizations, such as the WHO, acknowledge that collaborative practice is essential for achieving a concerted approach to providing care [ 1 ]. Prevention and management of infections across the surgical pathway should always focus on the collaboration between all healthcare professionals with shared knowledge and widespread diffusion of best practice. In the Appendix, the statements approved with an agreement ≥ 80% are reported.

Availability of data and materials

Not applicable.


  • Antimicrobial resistance

Antimicrobial stewardship program

Catheter-associated urinary tract infection

Centers for Disease Control and Prevention

Clostridioides difficile infection

Central line-associated bloodstream infection

Clinical microbiology laboratory

Central venous catheter-related bloodstream infection

C-reactive protein

Candida score

Central venous catheter

Defined daily dose

European Center for Disease Prevention and Control

Fecal microbiota transplantation

Healthcare-associated infection

Healthcare worker

Inappropriate antibiotic therapy

Invasive candidiasis

Intensive care unit

Infection prevention and control

Multidrug-resistant organism

Perioperative antibiotic prophylaxis


Proton pump inhibitor

Surgical site infection

World Health Organization

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Massimo Sartelli, Guido Cesare Gesuelli, Walter Siquini & Cristian Tranà

Infectious Diseases Unit, Bolzano Central Hospital, Bolzano, Italy

Leonardo Pagani & Raffaella Binazzi

Ministry of Health, Rome, Italy

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General, Emergency and Trauma Surgery Department, Bufalini Hospital, Cesena, Italy

Luca Ansaloni

Emergency Surgery Unit, New Santa Chiara Hospital, University of Pisa, Pisa, Italy

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Infectious Diseases Unit, Fermo Hospital, ASUR Marche, Marche, Italy

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Infectious Diseases Department, Trieste University Hospital, Trieste, Italy

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Carla Rebagliati

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Division of Emergency Surgery, Fondazione Policlinico Universitario A. Gemelli IRCCS, Università Cattolica del Sacro Cuore, Rome, Italy

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Statement 2.1 . Surveillance of HAIs improves the quality of care because it reduces the risk of infection. It should be supported by all healthcare workers.

Statement 4.1. Key points forCDI prevention are:

Question 8. Antimicrobial stewardship. Is a multidisciplinary approach necessary?

Statement 13.1. It is important the knowledge of the risk of developing invasive candidiasis, improve microbiological diagnostics and optimize treatment.

Statement 15.1. To be a champion in preventing and managing infections in surgery means to create a culture of collaboration in which infection prevention, antimicrobial stewardship and correctsurgical approach are of high importance.

Statement 20.2. Surgeons with satisfactory knowledge in surgical infections should be involved in the infection control team and recognized as “champions” by the hospital’s administration.

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Sartelli, M., Pagani, L., Iannazzo, S. et al. A proposal for a comprehensive approach to infections across the surgical pathway. World J Emerg Surg 15 , 13 (2020). https://doi.org/10.1186/s13017-020-00295-3

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Improving Guidelines for Nursing Home-Associated Viral Respiratory Infections

Amy Vogelsmeier, Ph.D., R.N., FAAN.

Associate Professor

Sinclair School of Nursing

University of Missouri–Colombia

Amy Vogelsmeier, Ph.D., R.N., FAAN

“AHRQ as a funding agency has provided an important opportunity for us to positively influence nursing home care, which is critical given the negative impact of COVID-19.”

The COVID-19 pandemic called nationwide attention to the vulnerability of nursing home residents to viral respiratory healthcare-associated infections (HAIs). Myriad factors, including patient-to-staff ratio and shared living spaces, increase residents’ exposure to infection outbreaks.

Amy Vogelsmeier, Ph.D., .R.N., FAAN, an associate professor at Sinclair School of Nursing, University of Missouri—Columbia, has more than 30 years of experience as a registered nurse in acute and long-term care settings. When COVID-19 hit, Dr. Vogelsmeier was working on a demonstration project that employed advanced practice registered nurses in 16 Missouri nursing homes to reduce avoidable resident hospitalizations. She realized the way nursing homes responded to COVID-19 could influence the health outcomes of residents.

In 2021, Dr. Vogelsmeier received an AHRQ grant to understand nursing homes’ response to COVID-19 and how that response influenced resident outcomes. “An opportunity to minimize respiratory infections and the negative outcomes, not just from the illness itself but all of the constraints put on nursing homes, specific to COVID, is what drove this study,” she noted. Under this 4-year grant, Dr. Vogelsmeier and her co-principal investigator, Lori Popejoy, Ph.D., R.N., FAAN, are conducting research in 24 Missouri nursing homes to develop knowledge and recommendations to improve U.S. nursing homes’ ability to respond to high-risk respiratory and HAI outbreaks. Their goal is to identify best practices and combine them with existing guidelines to reduce risk of patient harm.  “We’re learning how nursing homes used the guidelines imposed on them to understand what worked and what didn’t for COVID-related care.”

Dr. Vogelsmeier says the next step will be to implement the updated and combined best practices and existing evidence-based guidelines in nursing homes. “One example might be to assure nursing homes are part of emergency planning at the community or county level. The few nursing homes in our study that were part of community-level planning noted that it helped them prepare and access resources; unfortunately, community engagement did not commonly occur.”

“Many times, when you look at large-scale outcomes, you miss the nuances of the story and that’s where these 24 nursing homes provide an in-depth understanding of what really happened. This funding mechanism allows us to do that.” This project will end August 31, 2025.

Principal Investigator: Amy Vogelsmeier, Ph.D., R.N., FAAN Institution: Sinclair School of Nursing, University of Missouri–Colombia Grantee Since: 2021 Type of Grant: Health Services Research Project

Related AHRQ Resources

  • AHRQ Nursing Home COVID-19 Action Network .
  • AHRQ’s Safety Program for Nursing Homes: On-Time Preventable Hospital and Emergency Department Visits .
  • AHRQ’s Safety Program for Nursing Homes: On-Time Prevention .
  • Center to Advance Palliative Care (CAPC) COVID-19 Response Resources Hub .
  • Nursing Home Antimicrobial Stewardship Modules .
  • Protecting the Most Vulnerable Through Partnership: Helping Nursing Homes Respond to the COVID-19 Crisis .
  • Staffing During the COVID-19 Pandemic: A Guide for Nursing Home Leaders .

Consistent with its mission, AHRQ provides a broad range of extramural research grants and contracts, research training, conference grants, and intramural research activities. AHRQ is committed to fostering the next generation of health services researchers who can focus on some of the most important challenges facing our Nation's health care system.

To learn more about AHRQ's Research Education and Training Programs, please visit https://www.ahrq.gov/training .

Return to AHRQ Grantee Profiles

Internet Citation: Improving Guidelines for Nursing Home-Associated Viral Respiratory Infections. Content last reviewed December 2023. Agency for Healthcare Research and Quality, Rockville, MD. https://www.ahrq.gov/funding/grantee-profiles/grtprofile-vogelmeier.html

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Business Wire

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Implementing nasal decolonization prior to major surgery to reduce HAIs is recommended by leading medical bodies, including the World Health Organization, 6 the Society for Healthcare Epidemiology of America (SHEA), 7 and NICE. 8 The nose is the major reservoir of pathogens and the majority of surgical site infections (SSIs) and bloodstream infections have been traced back to bacteria in the patient’s nose. 9 A patient with a surgical site infection (SSI) will, on average, spend 7 to 11 days longer in the hospital, significantly increasing costs and lengthening patients' recovery. 10

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1 Stone PW. Economic burden of healthcare-associated infections: an American perspective. Expert Rev Pharmacoecon Outcomes Res. 2009 Oct;9(5):417-22. doi: 10.1586/erp.09.53. PMID: 19817525; PMCID: PMC2827870.

2 Poovelikunnel T, Gethin G, Humphreys H. Mupirocin resistance: clinical implications and potential alternatives for the eradication of MRSA. J Antimicrob Chemother . 2015;70(10):2681-2692. doi:10.1093/jac/dkv169

3 Hansen D, Patzke PI, Werfel U, Benner D, Brauksiepe A, Popp W. Success of MRSA eradication in hospital routine: depends on compliance. Infection. 2007 Jun;35(4):260-4. doi: 10.1007/s15010-007-6273-y. Epub 2007 Jul 23. PMID: 17646910.

4 Bryce E, Wong T, Forrester L, Masri B, Jeske D, Barr K, Errico S, Roscoe D. Nasal photodisinfection and chlorhexidine wipes decrease surgical site infections: a historical control study and propensity analysis. J Hosp Infect. 2014 Oct;88(2):89-95. doi: 10.1016/j.jhin.2014.06.017. Epub 2014 Aug 1. Erratum in: J Hosp Infect. 2015 Sep;91(1):93. PMID: 25171975.

5 Moskven E, Banaszek D, Sayre E, Gara A, Bryce E, Wong T, Ailon T, Charest-Morin R, Dea N., Dvorak M, Fisher C, Kwon B, Paquette S, Street J. Effectiveness of prophylactic intranasal photodynamic disinfection therapy and chlorhexidine gluconate body wipes for surgical site infection prophylaxis in adult spine surgery. Can J Surg. 2023 Nov;66(6), E550–E560. https://doi.org/10.1503/cjs.016922

6 World Health Organization. Global Guidelines for the Prevention of Surgical Site Infection. World Health Organization; 2016. Available at: https://www.who.int/publications/i/item/9789241550475 . Accessed December 12, 2023.

7 Calderwood MS, Anderson DJ, Bratzler DW, et al. Strategies to prevent surgical site infections in acute-care hospitals: 2022 Update. Infect Control Hosp Epidemiol. 2023;44(5):695-720. doi:10.1017/ice.2023.67

8 National Institute for Health and Care Excellence (NICE). NICE Surgical Site Infections: Prevention and Treatment. NICE; 2019. Available at: https://www.nice.org.uk/guidance/ng125 . Accessed December 12, 2023.

9 von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med. 2001 Jan 4;344(1):11-6. doi: 10.1056/NEJM200101043440102. PMID: 11136954.

10 Seidelman JL, Mantyh CR, Anderson DJ. Surgical Site Infection Prevention: A Review. JAMA. 2023;329(3):244–252. doi:10.1001/jama.2022.24075

Vane Percy & Roberts Amanda Bernard +44 (0)1737821890 [email protected]


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