Dutch guideline for the prevention and control of multidrug-resistant organisms in the hospital setting, 2024 update

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Sussenbach, Veronica Weterings, Erik Bathoorn, Myrte J. Tielemans, and 12 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-6957898/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract The emergence of multidrug-resistant organisms (MDROs) represents a significant challenge for global healthcare systems. The Netherlands maintains one of the lowest antimicrobial resistance rates in the world, attributed to prudent antibiotic use and effective infection prevention and control policies in healthcare settings. This report presents an updated national guideline for the infection prevention and control of MDROs in hospitals, developed by the Dutch Collaborative Partnership for Infection Prevention Guidelines (SRI). Using a multidisciplinary approach and evidence-based frameworks such as AGREE-II and GRADE, the guideline addresses the definition of MDRO, risk assessment and recommendations for MDRO screening, isolation and infection prevention measures, source and contact tracing, discontinuation of isolation measures, and organization of care. It incorporates new evidence, and other aspects such as patient perspectives, sustainability, costs, and organizational factors, providing practical recommendations to mitigate MDRO transmission. This update aims to strengthen national infection control practices and sustain the Dutch low antimicrobial resistance levels. Infectious Diseases Hospital Medicine Health Policy Guidelines infection control cross infection evidence-based practice Microbial Drug Resistance Transmission Introduction Antimicrobial resistance is rising to alarmingly high levels worldwide, leading to increased medical costs, prolonged hospital stays, and higher morbidity and mortality rates ( 1 ). The Netherlands remains one of the countries with the lowest antimicrobial resistance rates in clinical isolates across Europe ( 2 ). For instance, the prevalence of vancomycin-resistant Enterococcus faecium (VRE) in blood cultures is substantially lower in the Netherlands, at 0.5%, compared to the European Union /European Economic Area (EU/EEA) population-weighted mean percentage of 19.8% in 2023 ( 2 ). Similarly, the prevalence of carbapenem-resistant Enterobacterales remains low, with 0.1% for Escherichia coli and 0.4% for Klebsiella pneumoniae versus 0.3% and 13.3% across the EU ( 2 ). Only the prevalence of third-generation cephalosporin-resistant Enterobacterales has increased in recent years in the Netherlands, with resistance in E. coli rising from 6.1–8.0% and in K. pneumoniae from 7.6–10.2% over the past 10 years ( 2 , 3 ). However, it remains below the EU average (2023: 16.2% for E. coli and 34.8% for K. pneumoniae ) ( 2 ). The low prevalence of antimicrobial resistance in the Netherlands is largely attributed to the prudent and restrictive use of antibiotics ( 4 ), and effective infection prevention and control (IPC) policies in healthcare settings. These measures are guided by national guidelines and overseen by the Dutch Health and Youth Care Inspectorate (IGJ). The first Dutch guideline for multidrug-resistant organisms (MDRO) was published in 2005 and updated in 2012 as part of a planned revision ( 5 , 6 ). However, no further revisions have been made since 2012, highlighting the need to update the MDRO guideline. New insights, such as revised MDRO criteria and updated IPC measures, should be incorporated. From 1981 to 2017, the Dutch Working Party on Infection Prevention (Werkgroep Infectie Preventie [WIP]) was responsible for developing national IPC guidelines to reduce nosocomial infections and the transmission of pathogens in healthcare settings ( 7 , 8 ). After the dissolution of the WIP, a new infrastructure was established, and in 2021, the Dutch Ministry of Health, Welfare and Sport (VWS) launched the Dutch Collaborative Partnership for Infection Prevention Guidelines (Samenwerkingsverband Richtlijnen Infectiepreventie [SRI]( 9 )), a new guideline organization dedicated to developing evidence-based IPC guidelines ( 8 ). During the interim period, no revisions were made to the existing WIP guidelines. The SRI has since published its first set of guidelines online, including the guideline for MDRO ( 10 ). The SRI guideline on MDROs outlines IPC measures in specialist medical care settings—primarily hospitals—to prevent the transmission of MDROs, excluding methicillin-resistant Staphylococcus aureus (MRSA) and multidrug-resistant tuberculosis (MDR-TB), as these are addressed in separate SRI guidelines. The guideline is intended for healthcare professionals involved in the care of patients with MDROs and those responsible for developing and implementing local IPC policies. The guideline was developed using the GRADE (Grading of Recommendations Assessment, Development and Evaluation) Evidence-to-Decision Framework, which allows clinical questions to be addressed using evidence from systematic literature reviews, supplemented by expert opinions and additional literature ( 11 , 12 ). In this paper, we describe the methodology, results and recommendations of the MDRO guideline developed by the SRI. Methods The guideline was developed following recommendations from established manuals on guideline development, including the Appraisal of Guidelines for Research and Evaluation II (AGREE-II) ( 11 – 13 ). Guideline development group A multidisciplinary Guideline Development Group (GDG) with a balanced range of expertise was formed. The GDG consisted of representatives from the Dutch Society of Medical Microbiology (NVMM), the Dutch Society of Internal Medicine (NIV), the Dutch Society of Dermatology and Venereology (NVDV), the Dutch Society of Infection Prevention and Control in the healthcare setting (VHIG), the National Institute for Public Health and the Environment (RIVM), the Dutch Association of Elderly Care Physicians and Social Geriatricians (Verenso), the Dutch Nursing Association (V&VN), the Patient Federation Netherlands (PFNL) and the Netherlands Society of Occupational Medicine (NVAB). The GDG held regular meetings with support from a guideline methodologist ( 8 ). Key questions During the preparatory phase, the GDG consulted relevant stakeholders to gather input on the challenges faced in the care of patients with MDROs. Additional feedback was collected from stakeholders during an invitational conference. Recommendations from the previous guideline ( 5 , 6 ) were also reviewed to identify areas for potential revisions. Based on these inputs, the GDG prioritized the challenges and formulated draft key questions, which were subsequently finalized. Evidence review and grading The clinical questions focused on the effectiveness of various IPC aspects. Comprehensive searches were conducted in Embase, Ovid/Medline, and Cinahl to identify relevant studies published in English. These databases were searched up to date as stated in each review protocol (see Additional files). Studies were selected based on their design, study population, and interventions. For each clinical question, the data were summarized and evaluated using the GRADE methodology, which categorizes the quality of evidence as high, moderate, low, or very low ( 8 , 11 , 12 , 14 , 15 ). If the GDG determined that the evidence was insufficient in a particular area, further research to address identified knowledge gaps could be recommended. Guideline recommendations When formulating guideline recommendations, the GDG used conclusions from the systematic literature review to answer the clinical questions. However, these conclusions were not always directly applicable as practical recommendations. Therefore, the evidence-to-decision framework required the GDG to consider other aspects, such as patient perspectives, sustainability, preferences, costs, and organizational aspects ( 8 , 12 ). These considerations, often based on expert opinion or literature not included in the systematic literature review, were explicitly and systematically documented, presenting arguments both in favour and against various IPC measures ( 11 , 12 ). Recommendations were thus based on a combination of the scientific conclusions from the systematic literature review (if applicable) and additional considerations. The quality of evidence and the weight of the additional considerations influenced the strength of each recommendation. Results The key questions and recommendations were structured into six distinct modules. Module I: Definition of multidrug-resistant organisms (MDRO) Various definitions of MDRO exist in the international literature. In 2012, an international group of experts proposed interim standard definitions for “multidrug-resistant”, “extensively drug-resistant”, and “pan drug-resistant” bacteria to enhance global uniformity ( 16 ). These definitions have been criticized for being overly broad and for assigning equal weight to all antimicrobial classes. In 2017, the World Health Organization (WHO) published a list of resistant bacteria that should be prioritized for the development of new antibiotics ( 17 ). Although widely used to guide IPC measures globally, this WHO list was not initially intended for that purpose. Recently, an update of the list was published, but again, primarily focused on research and development ( 18 ). Since 2005, a context-specific definition for MDRO has been developed, tailored to the Dutch healthcare system. This approach built on the aforementioned international publications and focused on more pragmatic criteria. According to this definition, MDROs are characterized by three core criteria: ( a ) the microorganism causes disease, ( b ) it has acquired antimicrobial resistance that hampers (empirical) therapy, and ( c ) it has the potential to spread if transmission-based precautions are not implemented ( 5 ). To further establish consensus, in 2021, the Dutch Society of Medical Microbiology (NVMM) consulted its members to define which microorganisms should be classified as MDROs based on these criteria. Potential MDROs were assessed by medical microbiologists, with microorganisms primarily transmitted outside healthcare settings (e.g., Streptococcus pneumoniae , Salmonella spp., and Neisseria gonorrhoeae ) excluded. Consensus that a microorganism met all three criteria provided a solid rationale for the GDG to designate it as an MDRO. The GDG based its recommendations largely on the previous national guideline ( 6 ), expert opinion, and consensus, while also considering additional factors such as the clinical impact of limited treatment options on patient outcomes, the organism's transmissibility, and the effectiveness of IPC measures. These factors informed decisions regarding the classification of MDROs and the implementation of screening, isolation, and other IPC interventions. Evidence and rationale for the recommendations Based on the abovementioned considerations, a list of microorganisms classified as MDRO has been compiled and presented in Table 1 . One new pathogen, Candida auris , is added to the updated MDRO list ( 6 ). Given the high prevalence of antifungal resistance ( 19 – 23 ), the rapid resistance development ( 24 , 25 ), and the lack of consensus on antifungal susceptibility testing and clinical breakpoints ( 26 ), C. auris is classified as an MDRO in all cases, regardless of susceptibility test results. Conversely, some microorganisms previously classified as MDROs are no longer considered as such. For example, Enterobacterales resistant to aminoglycosides and fluoroquinolones are no longer defined as MDROs, as these organisms do not significantly hinder treatment with standard therapies. Table 1 An overview of microorganisms defined as MDRO. Microorganism Resistance (mechanism) 1 Enterobacterales ESBL Enterobacterales Carbapenem 2 or carbapenemase Enterobacterales group II 3 Aminoglycosides 4 + fluoroquinolones 5 + sulfamethoxazole/trimethoprim Acinetobacter baumannii-calcoaceticus complex 6 Aminoglycosides 4 + ciprofloxacin or levofloxacin Acinetobacter baumannii-calcoaceticus complex 6 Carbapenemase 7 Pseudomonas aeruginosa ≥ 3 of the following: ● Tobramycin or amikacin ● Carbapenem 8 or carbapenemase ● Piperacillin ● Ceftazidime ● Fluoroquinolones Enterococcus faecium Vancomycin or vanA gene or vanB gene + penicillin-group Candida auris 9 Regardless of resistance 10 Note : In specific settings, such as neonatology or haematology, local policies may define MDRO differently, often due to specific antimicrobial prophylaxis. During outbreaks of resistant pathogens not yet classified as MDROs, additional infection prevention measures may be necessary. ESBL = extended-spectrum beta-lactamase. 1 Resistance is determined based on clinical breakpoints (see https://www.eucast.org/ ). 2 For Proteus spp., Providencia spp., Serratia marcescens and Morganella morganii imipenem is not considered. 3 Includes Citrobacter freundii, Enterobacter spp., Klebsiella aerogenes, Hafnia alvei, Morganella morganii, Providencia spp., Serratia marcescens , and other Enterobacterales typically carrying chromosomal AmpC. 4 Resistance to gentamicin or tobramycin or amikacin; for S. marcescens tobramycin and amikacin are not considered ( 76 , 77 ). 5 Resistance to ciprofloxacin, norfloxacin, or levofloxacin. 6 Includes Acinetobacter calcoaceticus, A. baumannii, A. pittii , and A. nosocomialis. 7 The bla OXA−51 gene is not considered a carbapenemase gene, as it is an intrinsic chromosomal resistance gene. If the laboratory cannot detect relevant carbapenemase genes or carbapenemase production, resistance to imipenem and/or meropenem should be determined based on clinical breakpoints. 8 Excluding ertapenem. 9 See WHO fungal priority pathogens list . 10 Susceptibility testing is always indicated Plasmid-mediated AmpC beta-lactamase-producing Enterobacterales Plasmid-mediated AmpC beta-lactamase-producing Enterobacterales were not classified as MDRO in the previous national guideline ( 6 ), primarily due to the absence of reported outbreaks in the Netherlands and the low prevalence of plasmid-mediated AmpC beta-lactamase Enterobacterales. Additionally, differentiating between chromosomal and plasmid-mediated AmpC beta-lactamase production was challenging with the laboratory methods available at the time ( 27 ). However, advancements in diagnostic techniques since the 2012 guideline have prompted a reassessment of whether plasmid-mediated AmpC beta-lactamase-producing Enterobacterales meet the criteria for MDRO classification. While plasmid-mediated AmpC beta-lactamase-producing Enterobacterales meet the first two core criteria (disease causation and obstruction of standard therapy), it was unclear if they also met the third criterion (transmissibility). A systematic literature review was conducted to explore the following question in addressing this issue: Are outbreaks caused by E. coli, K. pneumoniae, Klebsiella oxytoca, or Proteus mirabilis with a plasmid-encoded AmpC beta-lactamase (without extended-spectrum beta-lactamase or carbapenemase) observed in healthcare facilities, if only basic IPC measures are implemented? See Additional file 1 for the corresponding Population, Intervention, Comparison, and Outcomes (PICO) question, summary of the literature, results, and evidence tables. Three studies were included in the literature analysis ( 28 – 30 ). The GDG concluded that available data from these studies did not justify classifying Enterobacterales with a plasmid-encoded AmpC gene as MDRO requiring additional IPC measures. The literature suggests that the spread of these bacteria in specialized medical care settings has been minimal. Furthermore, a surveillance study in the Netherlands reported a decrease in the carriage of these microorganisms among hospitalized patients from 2013 to 2016, even without additional IPC measures ( 31 ). Consequently, the GDG concludes that plasmid-mediated AmpC beta-lactamase-producing Enterobacterales do not currently meet the criteria for classification as MDRO. However, given the dynamic nature of hospital-associated bacteria and the unpredictable evolution of microbial trends, there remains a possibility that successful Enterobacterales strains with plasmid-encoded AmpC genes could emerge. Therefore, ongoing surveillance in hospitals is essential to detect any potential rise of such strains. Recommendation 1 Consider the following microorganism as MDRO: [ Table 1 ] Recommendation 2 Do not classify Enterobacterales with a plasmid-mediated AmpC gene as MDRO. Monitor in hospital settings for increases based on phenotype to detect nosocomial transmission of Enterobacterales with a plasmid-mediated AmpC gene, and implement outbreak management measures to control outbreaks. Module II: Risk assessment for screening of MDRO and recommendations for MDRO selection per risk For the past 20 years, Dutch hospitals have implemented a risk-based screening policy for asymptomatic MDRO carriage upon admission ( 6 ). This policy (search and destroy/control) targeted known MDRO carriers, patients who had been hospitalized in another Dutch healthcare setting with an outbreak within the past two months during an ongoing outbreak, and patients who had been hospitalized in a foreign healthcare setting within the past two months, as they were all considered at higher risk for MDRO carriage. These patients were screened upon admission and (pre-emptively) isolated while awaiting culture results to reduce patient-to-patient transmission. Since 2015, it has also been recommended to additionally screen individuals residing in refugee centers, although this recommendation was based on limited evidence ( 32 ). Patients treated in foreign healthcare settings were screened for Gram-negative MDRO, while the recommendation to screen individuals from refugee centers did not specify which MDRO to screen for. The previous national MDRO guideline ( 6 ), international guidelines, and relevant scientific articles were reviewed to evaluate whether the current risk groups still have an increased risk of MDRO carriage. This review also aimed to determine whether potential new risk groups, such as travelers without healthcare-related contacts, should be added, taking into account the (low) background prevalence of MDROs in the Netherlands. Evidence and rationale for the recommendations Foreign healthcare setting Several recent studies have examined the risk of MDRO carriage associated with recent admissions to foreign healthcare settings, all of which support the inclusion of hospitalization abroad as a risk factor. See Additional file 2 for an overview of studies from primarily low-endemic MDRO countries that report the prevalence of MDRO carriage among patients treated in foreign hospitals or otherwise provide data on this risk factor. Based on this data, the GDG recommends maintaining the current risk assessment, which includes recent admission to a healthcare facility abroad for Gram-negative MDRO. However, the GDG also recommends screening for VRE for this group, given the currently low prevalence of VRE in the Dutch population ( 33 ) and the occasionally high carriage rates within this risk group ( Additional file 2 ). Additionally, screening for C. auris is recommended as C. auris is an emerging pathogen causing outbreaks of invasive healthcare-related infections worldwide, including in Europe ( 21 , 22 ). Refugee shelters In recent years, several studies have investigated the prevalence of MDRO among asylum seekers and refugees. See Additional file 2 for an overview of studies reporting MDRO prevalence among individuals residing in refugee centres. Compared to the background prevalence in the Netherlands, a higher prevalence of MDRO was observed in individuals living in or recently staying at refugee centres. For this reason, the GDG recommends screening individuals who have resided in a refugee centre within the past two months for at least ESBL-producing Enterobacterales and carbapenemase-producing or carbapenem-resistant Enterobacterales (CPE/CRE). The GDG does not recommend screening this group for multidrug-resistant P. aeruginosa , resistant A. baumannii-calcoaceticus complex, or C. auris due to a lack of evidence. Patients recently traveling abroad (without healthcare contact) Traveling abroad is often cited as a risk factor for MDRO carriage. A recent systematic review of 22 studies concluded that the risk of acquiring an MDRO depends on the travel destination and the use of antibiotics during the trip. The highest rates of MDRO carriage were observed after travel to South Asia (median 71%), followed by North Africa (median 41%), with ESBL-producing E. coli being the most found. Although CPE was found in only a few cases, the culture methods used were not always aimed at detecting it ( 34 ). A study by Wuerz, which included 15 studies, also showed an increased prevalence of ESBL-producing Enterobacterales among travellers, particularly if fluoroquinolones were used during the trip ( 35 ). The duration of MDRO carriage acquired during travel is generally short, ranging from a median of 30 days ( 36 ) to 1–2 months ( 37 ), although this can vary depending on the clone. Based on this data, the GDG concludes that patients who have recently travelled to Asia (including Turkey) and/or Africa have an increased risk of carrying ESBL-producing Enterobacterales and possibly CPE or CRE. The GDG advises healthcare facilities to be vigilant for possible ESBL-producing Enterobacterales and CPE/CRE carriage in travellers from these regions and leaves it to the local healthcare facility, whether to include this group in the risk assessment. Risk assessment in the outpatient setting The risk assessment is indicated upon or shortly before admission to a healthcare facility, not during outpatient clinic visits ( 38 ). However, in some outpatient settings, invasive procedures are performed. Additionally, there are outpatient departments that can be considered clinical departments based on the patient population or type of care provided (such as dialysis and oncology day centres). In these cases, the risk of MDRO transmission may be higher or have a larger impact, making a risk assessment necessary. The GDG considers it the responsibility of the healthcare facility to determine which outpatient departments are classified as “clinical” depending on the invasiveness of the procedures performed or the characteristics of the patient population. Recommendation 3 Conduct following risk assessment upon or shortly before admission to a healthcare facility, as well as during visits to outpatient clinics that the healthcare facility designates as clinical departments: 1. Determine if the patient is a known carrier of an MDRO and implement appropriate infection control measures 2. Screen for carriage of all MDROs listed in Recommendation 1 in patients who meet the following criteria: ● Patients who stayed in a healthcare facility abroad for more than 24 hours within the last two months ● Patients who stayed in a healthcare facility abroad for less than 24 hours within the last two months and underwent an invasive procedure ● Patients who stayed in a healthcare facility abroad between two and twelve months ago and underwent an invasive procedure 3. Screen for MDRO carriage in patients transferred from another Dutch healthcare facility with an ongoing MDRO outbreak. Screen for the specific MDRO causing the outbreak. 4. Screen for extended-spectrum beta-lactamase-producing Enterobacterales (ESBL-E) and carbapenemase-producing or carbapenem-resistant Enterobacterales (CPE/CRE) in patients who have resided in a refugee center within the past two months. Module III: Isolation and infection prevention measures While standard precautions apply to all patient interactions (regardless of their MDRO status), the GDG considers them insufficient to prevent MDRO transmission; therefore, additional organism-specific measures are recommended. While substantial evidence supports these additional measures to prevent MDRO transmission, many studies assessed bundled strategies. These strategies typically combine interventions such as specific personal protective equipment (PPE), single-room or isolation settings, and environmental disinfection. This bundling complicates assessment of the effectiveness of individual interventions. Furthermore, many studies are conducted during outbreaks, often lacking control groups and are prone to performance bias. To provide recommendations on which IPC measures should be taken to prevent MDRO transmission, specified by each MDRO, the GDG considered most recommendations from the previous national MDRO guideline ( 6 ), along with international guidelines and expert opinions. A systematic review of the literature was conducted to assess the scientific evidence supporting the need for terminal disinfection of patient rooms when a patient is infected with or colonized by ESBL-producing E. coli . Another systematic review was performed to determine if additional IPC measures are necessary in the outpatient setting. Evidence and rationale for the recommendations Isolation and infection prevention measures in the inpatient setting Table 2 provides an overview of the isolation and additional IPC measures for each MDRO in the inpatient setting, while Additional file 3 details the evidence and rationale behind these recommendations. Table 2 an overview of the isolation and infection prevention measures described for each multidrug-resistant microorganism. Microorganism Resistance Patient room Personal protective equipment Terminal cleaning and disinfection after discharge, transfer, or death Gown Surgical mask Gloves Enterobacterales ESBL Single patient room with dedicated sanitary facilities Exception : A multiple-occupancy room is permitted if no single patient room is available, provided there is a 1.5-meter space around the bed and dedicated sanitary facilities. Yes No Yes Yes Enterobacterales Carbapenem or carbapenemase Single patient room with dedicated sanitary facilities Yes No Yes Yes Enterobacterales group II Aminoglycosides + fluoroquinolones + sulfamethoxazole/trimethoprim Single patient room with dedicated sanitary facilities Yes No Yes Yes Acinetobacter baumannii-calcoaceticus complex Aminoglycoside + ciprofloxacin or levofloxacin Negative-pressure isolation room Yes Yes Yes Yes Acinetobacter baumannii-calcoaceticus complex Carbapenemase Negative-pressure isolation room Yes Yes Yes Yes Pseudomonas aeruginosa ≥ 3 of the following: ● Tobramycin or amikacin ● Carbapenem or carbapenemase ● Piperacillin ● Ceftazidime ● Fluoroquinolones Single patient room with dedicated sanitary facilities Yes No Yes Yes Enterococcus faecium Vancomycin or vanA gene or vanB gene + penicillin-group Single patient room with dedicated sanitary facilities Yes No Yes Yes Candida auris Regardless of resistance Negative-pressure isolation room Yes Yes Yes Yes High risk for MDRO carriage, regardless of type (e.g. a recent admission to a foreign healthcare facility) Single patient room with dedicated sanitary facilities Yes No Yes Yes (if culture results are not yet available) In summary, alongside standard precautions such as hand hygiene according to the WHO's 5 Moments ( 39 ), healthcare workers are advised to wear gowns and gloves when in direct contact with patients or their immediate environment in all cases of MDRO. This practice reduces the risk of contaminating hands and clothing, which could otherwise contribute to the transmission of MDRO. For the A. baumannii-calcoaceticus complex and C. auris , the use of a surgical mask is recommended during patient care. In the case of A. baumannii-calcoaceticus complex, this is recommended due to insufficient evidence to revise the recommendation from the previous national MDRO guideline ( 5 , 6 ). For C. auris , a surgical mask is recommended because much remains unknown about the transmission routes of this emerging microorganism. A. baumannii-calcoaceticus complex and C. auris are the only microorganisms for which an isolation room with an anteroom and specific air management (e.g., ventilation control) is recommended. A. baumannii-calcoaceticus complex can potentially spread via airborne transmission ( 40 , 41 ). For C. auris , although the exact transmission route is not yet fully understood and airborne transmission is unlikely, current literature indicates that it can spread easily and cause outbreaks in healthcare settings ( 22 ). The presence of an anteroom may improve adherence to infection control measures. For all other MDRO, the GDG advises using a single patient room with dedicated sanitary facilities. An exception is made for ESBL-producing Enterobacterales, for which isolation in a multiple-occupancy room may be permitted under certain conditions. This exception is supported by a recent cluster-randomized study that found no difference in ESBL-producing Enterobacterales infection risk between single and multiple-occupancy rooms ( 42 ). However, the GDG still prefers single rooms for ESBL-producing Enterobacterales to reduce contamination risk and improve adherence to infection control measures. If a single room is unavailable, contact isolation in a multiple-occupancy room may be allowed, provided a 1.5-meter clearance around the bed and dedicated sanitary facilities. Finally, terminal disinfection of a patient room following the discharge, transfer, or death of a patient with an MDRO infection or carriage is a widely accepted routine practice in Dutch hospitals. However, the necessity for terminal disinfection specifically for ESBL-producing E. coli is sometimes debated. In response to this debate, a systematic review of the literature was conducted to address the following question: Is terminal disinfection of a patient room necessary after the discharge, transfer, or death of a patient infected with or carrying ESBL-producing Escherichia coli? See Additional file 4 for the PICO criteria and the result of the search. Unfortunately, no studies meeting the PICO criteria were identified. Consequently, the GDG concluded that scientific evidence to support the de-implementation of terminal disinfection for ESBL-producing E. coli is currently lacking. Therefore, the recommendation remains unchanged from the previous national guideline: terminal disinfection (following cleaning) of the room is always recommended after the discharge, transfer, or death of a patient with any MDRO. [ Table 2 ] Recommendation 4 In the inpatient setting, when caring for or treating a patient with an MDRO (or a suspected MDRO) involving direct patient contact and/or contact with the patient’s immediate environment, apply isolation and additional infection prevention measures as outlined in Table 2 . Recommendation 5 Following the discharge, transfer, or death of a patient with an MDRO, including ESBL-producing Escherichia coli , perform terminal cleaning and disinfection of the patient room and the sanitary facility. This recommendation applies to single- and multi-occupancy patient rooms. Isolation and infection prevention measures in the outpatient setting It is unknown whether MDRO transmission occurs during outpatient visits. To address this research question, a systematic review of the literature was conducted. The GDG focused the literature search on evaluating the need for additional IPC measures specifically for VRE, CPE/CRE, and carbapenemase-producing or carbapenem-resistant Acinetobacter baumannii-calcoaceticus complex (CP/CRAB). This selection was based on the potential risk of spread within healthcare facilities and the challenges of treating infections with limited antibiotic options. The review aimed to answer the following question: Are there outbreaks in outpatient clinics caused by vancomycin-resistant Enterococcus faecium, carbapenemase-producing or carbapenem-resistant Enterobacterales, or carbapenemase-producing or carbapenem-resistant Acinetobacter baumannii-calcoaceticus complex in the absence of additional measures beyond standard precautions ? See Additional file 5 for the PICO question, a summary of the literature and evidence tables. The literature search yielded three outbreak studies ( 43 – 45 ) involving VRE and CPE/CRE in outpatient settings. Additionally, one observational study ( 46 ) described the risk of environmental contamination with VRE during outpatient visits. These outbreak studies indicate that CPE transmission can occur in outpatient clinics and have, in rare cases, initiated outbreaks in healthcare settings. Two studies describe extensive VRE contamination in dialysis units, which can lead to outbreaks. No studies were found regarding outbreaks of CP/CRAB in outpatient settings. Despite the above findings, the GDG concluded that there is insufficient scientific evidence to support the routine implementation of additional IPC measures in outpatient clinics, as the transmission risk is generally lower than inpatients clinics. The GDG considered that contact and care moments in outpatient clinics are typically shorter and less intensive than inpatient settings. However, in situations where the outpatient clinic functions similarly to an inpatient unit - based on the type of care and/or patient population (e.g., dialysis and oncology day centers) - the GDG identified a higher risk and impact of transmission of VRE, CPE/CRE, and CP/CRAB. Therefore, additional IPC measures for these MDROs are indicated in such settings. Recommendation 6 For patients with (suspected) vancomycin-resistant Enterococcus faecium (VRE), carbapenemase-producing or carbapenem-resistant Enterobacterales (CPE/CRE), or carbapenemase-producing, carbapenem-resistant Acinetobacter baumannii-calcoaceticus complex (CP/CRAB) in outpatient setting, additional infection prevention measures should be implemented if there is a high risk of transmission due to the nature of the care provided or if transmission would significantly impact the patient population. Module IV: Source and contact tracing Source and contact tracing are generally considered essential components of IPC policies. They provide insights into the potential spread of an MDRO, enabling early detection and helping prevent further transmission between patients. However, conducting these investigations requires additional resources, including materials, tools, and personnel, which leads to increased costs. Therefore, it is important to determine when and how source and contact tracing should be implemented in cases of unexpected carriage or infection with an MDRO. In developing considerations and recommendations, the GDG primarily focused on inpatient care. To provide recommendations for conducting source and contact tracing, the GDG reviewed the previous national MDRO guideline ( 6 ), and supplemented it with expert opinion. Consideration was also given to the (low) background prevalence of MDRO in the Netherlands. Evidence and rationale for the recommendations In cases of an unexpected MDRO detection, the source and contact investigation follow the "ring principle". This method starts by screening those with the highest risk of exposure, typically the patient’s roommates or immediate contacts. If another positive case is identified, the screening circle is widened to include patients at moderate or lower risk of exposure. The scope of screening is determined by infection control professionals, such as medical microbiologists or infection control practitioners ( 47 ). Decisions regarding whether to implement additional isolation and IPC measures for close contacts while awaiting culture results are also made by these specialists as additional infection control measures may not always be necessary. Contact tracing and screening among healthcare workers is generally unnecessary, because MDRO carriage in staff rarely leads to transmission when standard precautionary measures are properly followed ( 48 ). Exception policy for ESBL-producing Escherichia coli in non-outbreak situations In the previous national MDRO guideline, an exception was made for ESBL-producing bacteria, stating that contact tracing was not required for an unexpected ESBL case in non-outbreak situations, provided adequate surveillance was in place within the healthcare facility to detect any increase in cases ( 6 ). The rationale at the time was that approximately 4% of the Dutch population carried ESBL-producing bacteria, making it challenging to identify nosocomial transmission, particularly because accurate typing methods were not yet widely available. Although the prevalence of ESBL carriage in the Netherlands has remained stable at around 5% ( 49 ), the GDG has revised its recommendation on source and contact tracing. The previous policy remains valid for cases of unprotected contact with ESBL-producing E. coli , where contact tracing can be omitted if adequate surveillance is in place. However, for other ESBL-producing Enterobacterales, source and contact tracing is now recommended. This revision is due to the global dissemination of ESBL genes among virulent non- E. coli Enterobacterales lineages, which have increasingly spread within healthcare settings. In recent years, several outbreaks involving ESBL-producing non- E. coli Enterobacterales have been reported in Dutch hospitals ( 50 ). These non- E. coli ESBL-producing Enterobacterales pose a higher transmission risk than E. coli ( 42 ), and carriers also face an increased risk of infection ( 51 ). As a result, source and contact tracing is recommended for all cases of unprotected contact. Recommendation 7 Conduct source and contact tracing using the ring principle, targeting at least close contacts, when a patient who has been cared for without infection control measures is unexpectedly identified with an MDRO. For unexpected cases of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli , source and contact tracing can be omitted if adequate surveillance is implemented. It is not necessary to extend source and contact tracing to healthcare workers. Consult with an expert (e.g., medical microbiologist, or infection control practitioner) to determine whether additional isolation and infection prevention measures should be implemented for close contacts of the patient while awaiting the results of MDRO screening. If source and contact tracing indicate that transmission has occurred, initiate an investigation for a potential outbreak. Module V: Discontinuation of isolation and infection prevention measures Although infection prevention and isolation measures are essential to prevent MDRO transmission, they can reduce patient satisfaction, lower the quality of care provided, and increase healthcare workers' workload ( 52 – 54 ). Therefore, it is important to discontinue these measures once a patient is no longer an MDRO carrier. However, clear criteria for ending isolation remain lacking, and the previous guideline ( 6 ) did not specify the requirements needed to confirm MDRO clearance. Evidence and rationale for the recommendations The absence of clear criteria to determine when a patient is no longer an MDRO carrier raises important questions for clinical practice. To address these, a systematic review of the literature was conducted. The review aimed to answer the following question: When can a patient with a previously detected MDRO be considered MDRO-free (i.e., after what duration and/or under what conditions)? Details of the PICO framework, a summary of the literature, and evidence tables, can be found in Additional file 6 . A systematic search was performed to provide evidence-based answers to the clinical question. The literature search led to the inclusion of 15 studies ( 55 – 69 ). The GDG noted significant variation in the reported duration of MDRO carriage across these studies. This variability can be partly explained by differences in diagnostic methods for detecting MDRO, variations in the number and locations of cultures collected, and the intrinsic characteristics of the microorganisms. Although spontaneous loss of an MDRO often occurs within a few months, some individuals may carry MDRO for several years. Because the duration of carriage is unpredictable at the individual level, follow-up cultures are necessary to confirm MDRO clearance. Moreover, insights into the course of MDRO carriage have motivated recommendations regarding the optimal timing of follow-up cultures. The literature shows that multiple cultures are needed to confirm the end of MDRO carriage reliably. Studies suggest using 1 to 3 negative cultures to define loss of carriage of ESBL-producing Enterobacterales and CPE/CRE. For VRE, 2 to 5 negative cultures are suggested. Misclassifying an MDRO carrier as MDRO-negative can increase the risk of an outbreak due to the premature discontinuation of isolation and IPC measures. The likelihood that a patient is correctly identified as MDRO-negative depends partly on the duration of carriage and the number of negative cultures obtained. Given the very low level of evidence regarding the optimal timing and number of cultures, the GDG based its recommendations on insights from the literature and expert opinion. These recommendations take into account the risk of MDRO transmission within healthcare facilities and the potential for these organisms to cause infections that are difficult to treat with antibiotics. For sampling sites, the GDG refers to the Dutch national guideline Laboratory Detection of Multidrug-Resistant Organisms ( 70 ), which generally includes rectal swabs or feces and, if applicable, clinical sites. C. auris is currently not included in the laboratory detection guideline. Pending a revision of this guideline, the GDG recommends following the guidance of Meijer et al. ( 71 ): obtaining throat, nasal, and (peri-)anal swabs, along with additional swabs from the axilla, groin, and any other previously identified positive sites. For patients known to be MDRO carriers who are likely to require readmission or future care, follow-up cultures are advised to confirm the clearance of MDRO carriage. Patients should be informed about the importance of these follow-up cultures and the process for obtaining them. The GDG recommends follow-up cultures starting three months after the last positive culture to determine the loss of carriage of ESBL-producing Enterobacterales. The study with the largest number of patients ( 55 ) showed that after three months, 25% of the carriers have spontaneously lost the MDRO. The GDG considers the impact of incorrectly declaring loss of carriage for this MDRO type minimal. Therefore, the GDG advises confirming the end of carriage with two negative cultures taken on separate days, in line with common practice in studies and reflecting current practice in Dutch healthcare facilities. If the patient has received antibiotics to which the ESBL-producing Enterobacterales is susceptible, the first culture should be obtained at least 48 hours after the antibiotics have been discontinued. For CPE/CRE, similar to ESBL-producing Enterobacterales, 25% of patients spontaneously lost the MDRO after three months, as reported in the previously mentioned study ( 55 ). However, Oren et al. ( 72 ) reported that 45% of patients who initially tested negative for CPE/CRE had subsequent positive cultures. Due to the significant impact of the spread of CPE/CRE and based on the GDG’s experience that individuals who test negative in the first year may remain carriers in subsequent follow-up cultures, the GDG advises that a CPE/CRE carrier should be considered MDRO-positive during the first year after the last positive culture, even if negative cultures are obtained. After one year, the likelihood of decolonization increases, and the end of carriage can be confirmed with two negative cultures, similar to the approach for ESBL-producing Enterobacterales. To minimize the risk of incorrectly declaring a patient MDRO-free, the GDG recommends that follow-up cultures (one set) be taken during the year following the end of carriage if the patient is admitted to a healthcare facility. If antibiotics to which CPE/CRE are susceptible have been administered, the first culture should be obtained at least 48 hours after the antibiotics have been discontinued. Long-term carriage for VRE is common, and the risk of VRE transmission in healthcare settings is high. The GDG recommends managing VRE carriers in a manner similar to CPE/CRE, considering them positive during the first year after the last positive culture, even if negative cultures are obtained. False-negative culture results are more common for VRE compared than for antimicrobial-resistant Enterobacterales. Current evidence suggests that the end of VRE carriage can be reliably confirmed (≥ 95%) with five negative cultures, provided selective broth enrichment is used ( 73 ). Sensitivity increases to 99.3% when molecular diagnostics and a selective broth enrichment step are used together ( 74 ). If both a selective broth enrichment and polymerase chain reaction (PCR) are performed, the GDG advises establishing the end of carriage with three negative cultures. Additionally, the GDG recommends taking follow-up cultures (one set) during the first year after the end of carriage when the patient is admitted to a healthcare facility. If antibiotics susceptible to VRE have been given, the first culture should be taken at least 48 hours after discontinuation of antibiotic therapy. Other MDRO For multidrug-resistant group II Enterobacterales, multidrug-resistant Pseudomonas aeruginosa , resistant Acinetobacter baumannii-calcoaceticus complex and C. auris , the GDG is not aware of adequate studies on timing and number of cultures required to determine the end of carriage. However, since there is a need for recommendations for these MDRO, the same reasoning was applied as for ESBL-producing Enterobacterales, CPE/CRE, and VRE. For multidrug-resistant group II Enterobacterales, the expected duration of carriage and the associated impact are considered like those for ESBL-producing Enterobacterales. Therefore, the GDG makes the same recommendation as for ESBL-producing Enterobacterales. For multidrug-resistant Pseudomonas aeruginosa , resistant Acinetobacter baumannii-calcoaceticus complex , and C. auris , GDG considers the risks and the sensitivity of detection methods to be comparable to CPE/CRE. Thus, the recommendations for the timing and number of cultures are the same as those for CPE/CRE. Recommendation 8 When expecting readmission or future care, take follow-up cultures to demonstrate the end of MDRO carrier status based on the MDRO schedule outlined below. Cultures should only be collected if the patient has not received antimicrobials that suppress the growth of the relevant MDRO during and up to 48 hours prior to the culture collection. ESBL-producing Enterobacterales (ESBL-E) and multidrug-resistant (MDR) group II Enterobacterales - Confirm the end of ESBL-E and MDR group II Enterobacterales carriage with two negative culture sets, collected on separate days, starting at least three months after the last positive culture. Carbapenemase-producing or carbapenem-resistant Enterobacterales (CPE/CRE) - Confirm the end of CPE/CRE carriage with two negative culture sets, collected on separate days, starting one year after the last positive culture. - Take follow-up cultures (one culture set) if a patient is admitted to a healthcare institution in the first year after termination of carrier status to check for recurrences. Vancomycin-resistant Enterococcus faecium (VRE) - Confirm the end of VRE carriage with five negative culture sets, collected on different days, starting one year after the last positive culture. Three negative culture sets are sufficient if both a selective broth enrichment and PCR are used for detection. - Take follow-up cultures (one culture set) if a person is admitted to a healthcare institution in the first year after the end of carriage to check for recurrences. Multidrug-resistant P. aeruginosa and resistant Acinetobacter baumannii-calcoaceticus complex - Confirm the end of multidrug- resistant P. aeruginosa and resistant A. baumannii-calcoaceticus complex carriage with two negative culture sets, collected on separate days, starting one year after the last positive culture. - Take follow-up cultures (one culture set) if a person is admitted to a healthcare institution in the first year after the end of carriage to check for recurrences. Candida auris - Confirm the end of Candida auris carriage with two negative culture sets collected on separate days, starting one year after the last positive culture. - Take follow-up cultures (one culture set) if a person is admitted to a healthcare institution in the first year after the end of carriage status to check for recurrences. Module VI: Organization of care The Netherlands is recognized for having a significantly lower MDRO prevalence compared to many other countries ( 1 , 2 ). In order to preserve this low prevalence, there are essential organizational requirements for managing patients with a suspected or confirmed MDRO infection or carrier status. Healthcare facilities must ensure safe care by implementing transparent IPC policies and clearly communicating MDRO status to care providers and patients. Patient MDRO status should be shared with care providers and explained to patients. Outbreaks require a coordinated response by an outbreak management team, including isolation, contact tracing, and reporting to public health authorities. In addition to managing outbreaks, institutional MDRO policies should carefully balance IPC with the individual care needs, behaviour, and well-being of patients. Special consideration is required for the impact of prolonged isolation or restrictions, ensuring patient well-being is preserved while safeguarding public health. To support epidemiology and regional/national outbreak management, outbreaks must be reported in accordance with the Public Health Act. Healthcare institutions must notify the Health and Youth Care Inspectorate of incidents as specified in the Healthcare Quality Act. In the event of an MDRO outbreak, the Health and Youth Care Inspectorate emphasizes the importance of early reporting to the Healthcare-associated Infections and Antimicrobial Resistance Monitoring Group (SO-ZI/AMR), a national advisory body dedicated to providing timely national monitoring and risk assessment of nosocomial outbreaks ( 50 ). Surveillance of MDRO National / regional Building on organizational efforts to manage MDROs, effective surveillance is important for monitoring and controlling their spread. In the Netherlands, national surveillance is conducted by the RIVM for CP/CRAB and carbapenemase-producing Pseudomonas aeruginosa . Additionally, sharing information about MDRO spread within healthcare institutions is encouraged through regional healthcare networks to facilitate earlier detection and prevent transmission. Specialist medical care Under the current risk assessment, some MDRO carriers may not be identified promptly within specialist medical care. However, it is important to recognize the early spread of MDROs. Medical microbiologists and IPC experts are responsible for implementing an effective surveillance system that includes monitoring MDROs through clinical cultures and routine screening swabs, investigating potential epidemiological links, and performing typing when needed. Additional methods, such as screening all currently hospitalized patients at a certain point in time (point prevalence study), or screening patients with a prolonged hospital stay (e.g. 7 or 10 days), may enhance early detection and outbreak prevention. At present, not all resistant microorganisms are categorized as MDROs. However, some resistant organisms may eventually meet the criteria and be classified as such. The plasmid AmpC-producing Klebsiella spp. (except K. aerogenes ), E. coli and P. mirabilis are not currently designated as MDROs. Nevertheless, hospitals should implement surveillance to detect the emergence of new, successful AmpC gene-carrying Enterobacterales. This can be done, for example, by monitoring the presence of ESBL-negative isolates of these species with a cefotaxime and/or ceftazidime MIC ≥ 8 ug/ml in clinical cultures. Recommendation 9 - Share information about the spread of MDROs within the healthcare institution nationally and regionally. - Establish a surveillance system to detect the early spread of MDROs. Epilogue In 2021, the Ministry of Health, Welfare, and Sport launched a new initiative called the Dutch Collaborative Partnership for Infection Prevention Guidelines (Samenwerkingsverband Richtlijnen Infectiepreventie, SRI) ( 8 , 9 ). The SRI is a collaboration among various key stakeholders to develop, maintain, and manage high-quality infection prevention and control (IPC) guidelines with broad support. One of the first guidelines published by the SRI was the guideline for IPC of multidrug-resistant organisms (MDROs) for hospitals. The previous national MDRO guideline served as the foundation for this new version. A key improvement was that the updated guideline was developed in line with the recommendations from The Appraisal of Guidelines for Research and Evaluation (AGREE-II) ( 13 ). This is a highly structured, transparent, and informative system for assessing the quality of evidence used in guideline development. Evidence-based guidelines are generally recognized for improving the effectiveness and quality of care, reducing variations in healthcare practices, and minimizing costly and avoidable adverse events ( 13 ). Unfortunately, there is often limited availability of high-quality graded evidence to support strong recommendations in IPC. A recent review by Mitchell et al. ( 75 ) evaluated 31 national and international IPC guidelines published over the last decade, revealing that most recommendations were based on low-quality evidence. This is primarily because conducting randomized controlled trials in this area is often neither feasible nor ethical. This lack of high-quality graded evidence presents a challenge for guideline developers. During the development of the MDRO guideline, the team systematically searched for relevant research to address the key questions posed. Some questions could be answered with the available evidence, while others could not be conclusively answered. The evidence-based methodology used in the guideline development process highlighted existing knowledge gaps. Consequently, the guideline development group (GDG) identified areas where scientific knowledge is limited, and further research is required to strengthen future recommendations ( Additional file 7 ). In the initial phases of the guideline development, the GDG consulted relevant professional organizations to gather input on the challenges encountered in caring for patients with MDROs. These consultations provided a comprehensive overview of challenges in the field, which were subsequently prioritized by the GDG to formulate draft key questions. While this structured approach ensured a focus on the most pressing issues, it also highlighted a wide range of challenges that extended beyond the scope of the clinical questions ultimately addressed in this guideline. Due to time and resource constraints, not all identified challenges could be addressed in this version of the guideline. This underscores the need for sustained efforts and sufficient resources to address the existing and new challenges in IPC. As this guideline specifically focuses on medical specialist care, particularly hospitals, a separate guideline for prevention and control of MDRO in long-term care settings is currently under development by the SRI as a derivative of the hospital guideline and is scheduled for publication in 2025. This ensures that IPC measures are appropriately tailored to the distinct contexts and needs of both hospital and long-term care sectors. To conclude, this guideline aims to provide recommendations on the definitions of MDRO and measures to prevent the transmission of MDRO in hospitals, thereby contributing to maintaining low levels of antimicrobial resistance in the Netherlands. However, additional research is essential to provide more precise answers to practical and unanswered questions in the future. Abbreviations AGREE-II: Appraisal of Guidelines for Research and Evaluation II CP: carbapenemase-producing Acinetobacter baumannii-calcoaceticus complex CPE: carbapenemase-producing Enterobacterales CRAB: carbapenem-resistant Acinetobacter baumannii-calcoaceticus complex CRE: carbapenem-resistant Enterobacterales ESBL: extended-spectrum beta-lactamase EU/EEA: European Union / European Economic Area GDG: Guideline Development Group GRADE: Grading of Recommendations Assessment, Development and Evaluation IGJ: Dutch Health and Youth Care Inspectorate (Inspectie Gezondheidszorg en Jeugd) IPC: Infection prevention and control MDR-TB: multidrug-resistant tuberculosis MDRO: multidrug-resistant organisms MRSA: methicillin-resistant Staphylococcus aureus NIV: Dutch Society of Internal Medicine NVAB Netherlands Society of Occupational Medicine NVDV: Dutch Society of Dermatology and Venereology NVMM: Dutch Society of Medical Microbiology PCR: polymerase chain reaction PFNL: Patient Federation Netherlands RIVM: National Institute for Public Health and the Environment SO-ZI/AMR: Healthcare-associated Infections and Antimicrobial Resistance Monitoring Group SRI: Dutch Collaborative Partnership for Infection Prevention Guidelines (Samenwerkingsverband Richtlijnen Infectiepreventie) V&VN: Dutch Nursing Association Verenso: Dutch Association of Elderly Care Physicians and Social Geriatricians VHIG: Dutch Society of Infection Prevention and Control in the healthcare setting VRE: vancomycin-resistant Enterococcus faecium VWS: Dutch Ministry of Health, Welfare, and Sport WHO: World Health Organization WIP: Dutch Working Party on Infection Prevention (Werkgroep Infectie Preventie) Declarations Ethics approval and consent to participate Not applicable. Consent for publication Not applicable. Funding The development of the SRI guideline MDRO was funded by the Dutch Ministry of Health, Welfare, and Sport (VWS). The funder had no influence on the guideline’s content. Authors' contributions AS and VW were equal contributors to the draft of the manuscript. AS, VW, EB, MT, JO, BV, PB, YR, JV, PM, RN, MK, AV, HG, BV and JS contributed to conceptualization, formal analysis, and writing and editing of the guideline. AS, MK, HG and BV provided methodological guidance and support. All authors read and approved the final manuscript. Acknowledgements We thank information specialist Ingeborg van Dusseldorp of the Knowledge Institute of the Dutch Association of Medical Specialists for her help and support with the literature searches. We also thank Rosa van Mansfeld and Wil van der Zwet for their contribution to defining which microorganisms should be classified as MDRO during the NVMM consultation with its members. 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Antimicrob Resist Infect Control 7:100 Choi HE, Lee JH, Sim YJ, Jeong HJ, Kim GC (2021) Predictors of prolonged vancomycin-resistant enterococci colonization in acute stroke patients admitted to an intensive care unit: A retrospective cohort study. Med (Baltim) 100(32):e26913 Haverkate MR, Derde LP, Brun-Buisson C, Bonten MJ, Bootsma MC (2014) Duration of colonization with antimicrobial-resistant bacteria after ICU discharge. Intensive Care Med 40(4):564–571 Jimenez A, Fennie K, Munoz-Price LS, Ibrahimou B, Pekovic V, Abbo LM et al (2021) Duration of carbapenemase-producing Enterobacteriales carriage among ICU patients in Miami, FL: A retrospective cohort study. Am J Infect Control 49(10):1281–1286 Lim YJ, Park HY, Lee JY, Kwak SH, Kim MN, Sung H et al (2018) Clearance of carbapenemase-producing Enterobacteriaceae (CPE) carriage: a comparative study of NDM-1 and KPC CPE. Clin Microbiol Infect 24(10):1104 e5- e8 Nordberg V, Jonsson K, Giske CG, Iversen A, Aspevall O, Jonsson B et al (2018) Neonatal intestinal colonization with extended-spectrum beta-lactamase-producing Enterobacteriaceae-a 5-year follow-up study. Clin Microbiol Infect 24(9):1004–1009 Gedik H, Yildirmak T, Simsek F, Kanturk A, Arica D, Aydin D et al (2014) Vancomycin-resistant enterococci colonization and bacteremia in patients with hematological malignancies. J Infect Dev Ctries 8(9):1113–1118 Lister DM, Tan K, Carse E, Stuart RL (2016) Clearance of infant vancomycin-resistant Enterococcus faecium carriage after a neonatal inpatient outbreak. Am J Infect Control 44(10):1172–1173 Miu D, Ling S, Tse C (2016) Epidemiology of vancomycin-resistant enterococci in postacute care facility and predictors of clearance: a 5-year retrospective cohort study. J Clin Gerontol Geriatr 7(4):153–157 Overdevest I, Haverkate M, Veenemans J, Hendriks Y, Verhulst C, Mulders A et al (2016) Prolonged colonisation with Escherichia coli O25:ST131 versus other extended-spectrum beta-lactamase-producing E. coli in a long-term care facility with high endemic level of rectal colonisation, the Netherlands, 2013 to 2014. Euro Surveill. ;21(42) Sohn KM, Peck KR, Joo EJ, Ha YE, Kang CI, Chung DR et al (2013) Duration of colonization and risk factors for prolonged carriage of vancomycin-resistant enterococci after discharge from the hospital. Int J Infect Dis 17(4):e240–e246 Weterings V, van den Bijllaardt W, Bootsma M, Hendriks Y, Kilsdonk L, Mulders A et al (2022) Duration of rectal colonization with extended-spectrum beta-lactamase-producing Escherichia coli: results of an open, dynamic cohort study in Dutch nursing home residents (2013–2019). Antimicrob Resist Infect Control 11(1):98 Wangchinda W, Laohasakprasit K, Lerdlamyong K, Thamlikitkul V (2022) Epidemiology of Carbapenem-Resistant Enterobacterales Infection and Colonization in Hospitalized Patients at a University Hospital in Thailand. Infect Drug Resist 15:2199–2210 NVMM (2021) Richtlijn Laboratoriumdetectie bijzonder resistente micro-organismen (BRMO) Meijer E, Voss A, Meis J (2022) Candida auris: huidige inzichten. Ned Tijdschr Med Microbiol 30(2):61 Oren I, Sprecher H, Finkelstein R, Hadad S, Neuberger A, Hussein K et al (2013) Eradication of carbapenem-resistant Enterobacteriaceae gastrointestinal colonization with nonabsorbable oral antibiotic treatment: A prospective controlled trial. Am J Infect Control 41(12):1167–1172 Sinnige JCWR, Ruijs GJHM, Mascini E, Arends JP, Troelstra A (2015) NVMM Guideline HRMO VRE Fonville JM, van Herk CMC, Das P, van de Bovenkamp JHB, van Dommelen L (2017) A Single Negative Result for van Quantitative PCR on Enrichment Broth Can Replace Five Rectal Swab Cultures in Screening for Vancomycin-Resistant Enterococci. J Clin Microbiol 55(7):2261–2267 Mitchell A, Spencer M, Edmiston C (2015) Jr. Role of healthcare apparel and other healthcare textiles in the transmission of pathogens: a review of the literature. J Hosp Infect 90(4):285–292 Livermore DM, Winstanley TG, Shannon KP (2001) Interpretative reading: recognizing the unusual and inferring resistance mechanisms from resistance phenotypes. J Antimicrob Chemother 48(Suppl 1):87–102 Sandner-Miranda L, Vinuesa P, Cravioto A, Morales-Espinosa R (2018) The Genomic Basis of Intrinsic and Acquired Antibiotic Resistance in the Genus Serratia. Front Microbiol 9:828 Additional Declarations The authors declare no competing interests. Supplementary Files Additionalfile1.docx Additional file 1 Additionalfile2.docx Additional file 2 Additionalfile2.docx Additional file 2 Additionalfile4.docx Additional file 4 Additionalfile5.docx Additional file 5 Additionalfile5.docx Additional file 5 Additionalfile1.docx Additional file 1 Additionalfiles.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-6957898","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Method Article","associatedPublications":[],"authors":[{"id":475622392,"identity":"a5b780e8-1255-483b-a340-75b89390635d","order_by":0,"name":"Annelotte E. Sussenbach","email":"data:image/png;base64,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","orcid":"https://orcid.org/0000-0002-0849-9200","institution":"Knowledge Institute of the Dutch Association of Medical Specialists, Utrecht, The Netherlands, and Department of Medical Microbiology and Infection prevention, University Medical Center Groningen, Groningen, The Netherlands","correspondingAuthor":true,"prefix":"","firstName":"Annelotte","middleName":"E.","lastName":"Sussenbach","suffix":""},{"id":475628536,"identity":"f97cf15c-0abd-4de0-8cc4-3d66fbc09597","order_by":1,"name":"Veronica Weterings","email":"","orcid":"","institution":"Department of Infection Prevention and control, Amphia Hospital, Breda, The Netherlands","correspondingAuthor":false,"prefix":"","firstName":"Veronica","middleName":"","lastName":"Weterings","suffix":""},{"id":475628537,"identity":"966b5770-e2c1-447d-91ea-0963ab1c255a","order_by":2,"name":"Erik Bathoorn","email":"","orcid":"","institution":"Department of Medical Microbiology and Infection prevention, University Medical Center Groningen, Groningen, The Netherlands","correspondingAuthor":false,"prefix":"","firstName":"Erik","middleName":"","lastName":"Bathoorn","suffix":""},{"id":475628538,"identity":"d92e2a3b-43ea-4c45-a47e-4ef8ddf67732","order_by":3,"name":"Myrte J. 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03:37:57","extension":"docx","order_by":8,"title":"","display":"","copyAsset":false,"role":"supplement","size":15715,"visible":true,"origin":"","legend":"","description":"","filename":"Additionalfiles.docx","url":"https://assets-eu.researchsquare.com/files/rs-6957898/v1/cb131fbf97d8d81d63b8eacb.docx"}],"financialInterests":"The authors declare no competing interests.","formattedTitle":"\u003cp\u003eDutch guideline for the prevention and control of multidrug-resistant organisms in the hospital setting, 2024 update\u003c/p\u003e","fulltext":[{"header":"Introduction","content":"\u003cp\u003eAntimicrobial resistance is rising to alarmingly high levels worldwide, leading to increased medical costs, prolonged hospital stays, and higher morbidity and mortality rates (\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e). The Netherlands remains one of the countries with the lowest antimicrobial resistance rates in clinical isolates across Europe (\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e). For instance, the prevalence of vancomycin-resistant \u003cem\u003eEnterococcus faecium\u003c/em\u003e (VRE) in blood cultures is substantially lower in the Netherlands, at 0.5%, compared to the European Union /European Economic Area (EU/EEA) population-weighted mean percentage of 19.8% in 2023 (\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e). Similarly, the prevalence of carbapenem-resistant Enterobacterales remains low, with 0.1% for \u003cem\u003eEscherichia coli\u003c/em\u003e and 0.4% for \u003cem\u003eKlebsiella pneumoniae\u003c/em\u003e versus 0.3% and 13.3% across the EU (\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e). Only the prevalence of third-generation cephalosporin-resistant Enterobacterales has increased in recent years in the Netherlands, with resistance in \u003cem\u003eE. coli\u003c/em\u003e rising from 6.1\u0026ndash;8.0% and in \u003cem\u003eK. pneumoniae\u003c/em\u003e from 7.6\u0026ndash;10.2% over the past 10 years (\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e, \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e). However, it remains below the EU average (2023: 16.2% for \u003cem\u003eE. coli\u003c/em\u003e and 34.8% for \u003cem\u003eK. pneumoniae\u003c/em\u003e) (\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe low prevalence of antimicrobial resistance in the Netherlands is largely attributed to the prudent and restrictive use of antibiotics (\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e), and effective infection prevention and control (IPC) policies in healthcare settings. These measures are guided by national guidelines and overseen by the Dutch Health and Youth Care Inspectorate (IGJ). The first Dutch guideline for multidrug-resistant organisms (MDRO) was published in 2005 and updated in 2012 as part of a planned revision (\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e). However, no further revisions have been made since 2012, highlighting the need to update the MDRO guideline. New insights, such as revised MDRO criteria and updated IPC measures, should be incorporated.\u003c/p\u003e \u003cp\u003eFrom 1981 to 2017, the Dutch Working Party on Infection Prevention (Werkgroep Infectie Preventie [WIP]) was responsible for developing national IPC guidelines to reduce nosocomial infections and the transmission of pathogens in healthcare settings (\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e). After the dissolution of the WIP, a new infrastructure was established, and in 2021, the Dutch Ministry of Health, Welfare and Sport (VWS) launched the Dutch Collaborative Partnership for Infection Prevention Guidelines (Samenwerkingsverband Richtlijnen Infectiepreventie [SRI](\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e)), a new guideline organization dedicated to developing evidence-based IPC guidelines (\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e). During the interim period, no revisions were made to the existing WIP guidelines. The SRI has since published its first set of guidelines online, including the guideline for MDRO (\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe SRI guideline on MDROs outlines IPC measures in specialist medical care settings\u0026mdash;primarily hospitals\u0026mdash;to prevent the transmission of MDROs, excluding methicillin-resistant \u003cem\u003eStaphylococcus aureus\u003c/em\u003e (MRSA) and multidrug-resistant tuberculosis (MDR-TB), as these are addressed in separate SRI guidelines. The guideline is intended for healthcare professionals involved in the care of patients with MDROs and those responsible for developing and implementing local IPC policies. The guideline was developed using the GRADE (Grading of Recommendations Assessment, Development and Evaluation) Evidence-to-Decision Framework, which allows clinical questions to be addressed using evidence from systematic literature reviews, supplemented by expert opinions and additional literature (\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e). In this paper, we describe the methodology, results and recommendations of the MDRO guideline developed by the SRI.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eThe guideline was developed following recommendations from established manuals on guideline development, including the Appraisal of Guidelines for Research and Evaluation II (AGREE-II) (\u003cspan additionalcitationids=\"CR12\" citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e).\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eGuideline development group\u003c/h2\u003e \u003cp\u003eA multidisciplinary Guideline Development Group (GDG) with a balanced range of expertise was formed. The GDG consisted of representatives from the Dutch Society of Medical Microbiology (NVMM), the Dutch Society of Internal Medicine (NIV), the Dutch Society of Dermatology and Venereology (NVDV), the Dutch Society of Infection Prevention and Control in the healthcare setting (VHIG), the National Institute for Public Health and the Environment (RIVM), the Dutch Association of Elderly Care Physicians and Social Geriatricians (Verenso), the Dutch Nursing Association (V\u0026amp;VN), the Patient Federation Netherlands (PFNL) and the Netherlands Society of Occupational Medicine (NVAB). The GDG held regular meetings with support from a guideline methodologist (\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cem\u003eKey questions\u003c/em\u003e \u003c/p\u003e \u003cp\u003eDuring the preparatory phase, the GDG consulted relevant stakeholders to gather input on the challenges faced in the care of patients with MDROs. Additional feedback was collected from stakeholders during an invitational conference. Recommendations from the previous guideline (\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e) were also reviewed to identify areas for potential revisions. Based on these inputs, the GDG prioritized the challenges and formulated draft key questions, which were subsequently finalized.\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eEvidence review and grading\u003c/h3\u003e\n\u003cp\u003eThe clinical questions focused on the effectiveness of various IPC aspects. Comprehensive searches were conducted in Embase, Ovid/Medline, and Cinahl to identify relevant studies published in English. These databases were searched up to date as stated in each review protocol (see Additional files). Studies were selected based on their design, study population, and interventions.\u003c/p\u003e \u003cp\u003eFor each clinical question, the data were summarized and evaluated using the GRADE methodology, which categorizes the quality of evidence as high, moderate, low, or very low (\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e, \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e). If the GDG determined that the evidence was insufficient in a particular area, further research to address identified knowledge gaps could be recommended.\u003c/p\u003e\n\u003ch3\u003eGuideline recommendations\u003c/h3\u003e\n\u003cp\u003eWhen formulating guideline recommendations, the GDG used conclusions from the systematic literature review to answer the clinical questions. However, these conclusions were not always directly applicable as practical recommendations. Therefore, the evidence-to-decision framework required the GDG to consider other aspects, such as patient perspectives, sustainability, preferences, costs, and organizational aspects (\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e). These considerations, often based on expert opinion or literature not included in the systematic literature review, were explicitly and systematically documented, presenting arguments both in favour and against various IPC measures (\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e). Recommendations were thus based on a combination of the scientific conclusions from the systematic literature review (if applicable) and additional considerations. The quality of evidence and the weight of the additional considerations influenced the strength of each recommendation.\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eThe key questions and recommendations were structured into six distinct modules.\u003c/p\u003e\n\u003ch3\u003eModule I: Definition of multidrug-resistant organisms (MDRO)\u003c/h3\u003e\n\u003cp\u003eVarious definitions of MDRO exist in the international literature. In 2012, an international group of experts proposed interim standard definitions for \u0026ldquo;multidrug-resistant\u0026rdquo;, \u0026ldquo;extensively drug-resistant\u0026rdquo;, and \u0026ldquo;pan drug-resistant\u0026rdquo; bacteria to enhance global uniformity (\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e). These definitions have been criticized for being overly broad and for assigning equal weight to all antimicrobial classes. In 2017, the World Health Organization (WHO) published a list of resistant bacteria that should be prioritized for the development of new antibiotics (\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e). Although widely used to guide IPC measures globally, this WHO list was not initially intended for that purpose. Recently, an update of the list was published, but again, primarily focused on research and development (\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eSince 2005, a context-specific definition for MDRO has been developed, tailored to the Dutch healthcare system. This approach built on the aforementioned international publications and focused on more pragmatic criteria. According to this definition, MDROs are characterized by three core criteria: (\u003cem\u003ea\u003c/em\u003e) the microorganism causes disease, (\u003cem\u003eb\u003c/em\u003e) it has acquired antimicrobial resistance that hampers (empirical) therapy, and (\u003cem\u003ec\u003c/em\u003e) it has the potential to spread if transmission-based precautions are not implemented (\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eTo further establish consensus, in 2021, the Dutch Society of Medical Microbiology (NVMM) consulted its members to define which microorganisms should be classified as MDROs based on these criteria. Potential MDROs were assessed by medical microbiologists, with microorganisms primarily transmitted outside healthcare settings (e.g., \u003cem\u003eStreptococcus pneumoniae\u003c/em\u003e, \u003cem\u003eSalmonella\u003c/em\u003e spp., and \u003cem\u003eNeisseria gonorrhoeae\u003c/em\u003e) excluded. Consensus that a microorganism met all three criteria provided a solid rationale for the GDG to designate it as an MDRO.\u003c/p\u003e \u003cp\u003eThe GDG based its recommendations largely on the previous national guideline (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e), expert opinion, and consensus, while also considering additional factors such as the clinical impact of limited treatment options on patient outcomes, the organism's transmissibility, and the effectiveness of IPC measures. These factors informed decisions regarding the classification of MDROs and the implementation of screening, isolation, and other IPC interventions.\u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eEvidence and rationale for the recommendations\u003c/h2\u003e \u003cp\u003eBased on the abovementioned considerations, a list of microorganisms classified as MDRO has been compiled and presented in Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e. One new pathogen, \u003cem\u003eCandida auris\u003c/em\u003e, is added to the updated MDRO list (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e). Given the high prevalence of antifungal resistance (\u003cspan additionalcitationids=\"CR20 CR21 CR22\" citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e), the rapid resistance development (\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e, \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e), and the lack of consensus on antifungal susceptibility testing and clinical breakpoints (\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e), \u003cem\u003eC. auris\u003c/em\u003e is classified as an MDRO in all cases, regardless of susceptibility test results. Conversely, some microorganisms previously classified as MDROs are no longer considered as such. For example, Enterobacterales resistant to aminoglycosides and fluoroquinolones are no longer defined as MDROs, as these organisms do not significantly hinder treatment with standard therapies.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eAn overview of microorganisms defined as MDRO.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"2\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMicroorganism\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eResistance (mechanism)\u003csup\u003e1\u003c/sup\u003e\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEnterobacterales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eESBL\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEnterobacterales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eCarbapenem\u003csup\u003e2\u003c/sup\u003e or carbapenemase\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEnterobacterales group II\u003csup\u003e3\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eAminoglycosides\u003csup\u003e4\u003c/sup\u003e\u0026thinsp;+\u0026thinsp;fluoroquinolones\u003csup\u003e5\u003c/sup\u003e\u0026thinsp;+\u0026thinsp;sulfamethoxazole/trimethoprim\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAcinetobacter baumannii-calcoaceticus\u003c/em\u003e complex\u003csup\u003e6\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eAminoglycosides\u003csup\u003e4\u003c/sup\u003e\u0026thinsp;+\u0026thinsp;ciprofloxacin or levofloxacin\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAcinetobacter baumannii-calcoaceticus\u003c/em\u003e complex\u003csup\u003e6\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eCarbapenemase\u003csup\u003e7\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ePseudomonas aeruginosa\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003e\u0026ge;\u003c/span\u003e\u0026thinsp;3 of the following:\u003c/p\u003e \u003cp\u003e● Tobramycin or amikacin\u003c/p\u003e \u003cp\u003e● Carbapenem\u003csup\u003e8\u003c/sup\u003e or carbapenemase\u003c/p\u003e \u003cp\u003e● Piperacillin\u003c/p\u003e \u003cp\u003e● Ceftazidime\u003c/p\u003e \u003cp\u003e● Fluoroquinolones\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eEnterococcus faecium\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eVancomycin or vanA gene or vanB gene\u0026thinsp;+\u0026thinsp;penicillin-group\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eCandida auris\u003c/em\u003e\u003csup\u003e9\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eRegardless of resistance\u003csup\u003e10\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colspan=\"2\" nameend=\"c2\" namest=\"c1\"\u003e \u003cp\u003e\u003cb\u003eNote\u003c/b\u003e: In specific settings, such as neonatology or haematology, local policies may define MDRO differently, often due to specific antimicrobial prophylaxis. During outbreaks of resistant pathogens not yet classified as MDROs, additional infection prevention measures may be necessary.\u003c/p\u003e \u003cp\u003eESBL\u0026thinsp;=\u0026thinsp;extended-spectrum beta-lactamase.\u003c/p\u003e \u003cp\u003e\u003csup\u003e1\u003c/sup\u003e Resistance is determined based on clinical breakpoints (see \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://www.eucast.org/\u003c/span\u003e\u003cspan address=\"https://www.eucast.org/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003e).\u003c/span\u003e\u003c/p\u003e \u003cp\u003e\u003csup\u003e2\u003c/sup\u003e For \u003cem\u003eProteus\u003c/em\u003e spp., \u003cem\u003eProvidencia\u003c/em\u003e spp., \u003cem\u003eSerratia marcescens\u003c/em\u003e and \u003cem\u003eMorganella morganii\u003c/em\u003e imipenem is not considered.\u003c/p\u003e \u003cp\u003e\u003csup\u003e3\u003c/sup\u003e Includes \u003cem\u003eCitrobacter freundii, Enterobacter\u003c/em\u003e spp., \u003cem\u003eKlebsiella aerogenes, Hafnia alvei, Morganella morganii, Providencia\u003c/em\u003e spp., \u003cem\u003eSerratia marcescens\u003c/em\u003e, and other Enterobacterales typically carrying chromosomal AmpC.\u003c/p\u003e \u003cp\u003e\u003csup\u003e4\u003c/sup\u003e Resistance to gentamicin or tobramycin or amikacin; for \u003cem\u003eS. marcescens\u003c/em\u003e tobramycin and amikacin are not considered (\u003cspan citationid=\"CR76\" class=\"CitationRef\"\u003e76\u003c/span\u003e, \u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e77\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e\u003csup\u003e5\u003c/sup\u003e Resistance to ciprofloxacin, norfloxacin, or levofloxacin.\u003c/p\u003e \u003cp\u003e\u003csup\u003e6\u003c/sup\u003e Includes \u003cem\u003eAcinetobacter calcoaceticus, A. baumannii, A. pittii\u003c/em\u003e, and \u003cem\u003eA. nosocomialis.\u003c/em\u003e\u003c/p\u003e \u003cp\u003e\u003csup\u003e7\u003c/sup\u003e The \u003cem\u003ebla\u003c/em\u003e\u003csub\u003eOXA\u0026minus;51\u003c/sub\u003e gene is not considered a carbapenemase gene, as it is an intrinsic chromosomal resistance gene. If the laboratory cannot detect relevant carbapenemase genes or carbapenemase production, resistance to imipenem and/or meropenem should be determined based on clinical breakpoints.\u003c/p\u003e \u003cp\u003e\u003csup\u003e8\u003c/sup\u003e Excluding ertapenem.\u003c/p\u003e \u003cp\u003e\u003csup\u003e9\u003c/sup\u003e See \u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003eWHO fungal priority pathogens list\u003c/span\u003e.\u003c/p\u003e \u003cp\u003e\u003csup\u003e10\u003c/sup\u003e Susceptibility testing is always indicated\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003ePlasmid-mediated AmpC beta-lactamase-producing Enterobacterales\u003c/h3\u003e\n\u003cp\u003ePlasmid-mediated AmpC beta-lactamase-producing Enterobacterales were not classified as MDRO in the previous national guideline (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e), primarily due to the absence of reported outbreaks in the Netherlands and the low prevalence of plasmid-mediated AmpC beta-lactamase Enterobacterales. Additionally, differentiating between chromosomal and plasmid-mediated AmpC beta-lactamase production was challenging with the laboratory methods available at the time (\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e). However, advancements in diagnostic techniques since the 2012 guideline have prompted a reassessment of whether plasmid-mediated AmpC beta-lactamase-producing Enterobacterales meet the criteria for MDRO classification.\u003c/p\u003e \u003cp\u003eWhile plasmid-mediated AmpC beta-lactamase-producing Enterobacterales meet the first two core criteria (disease causation and obstruction of standard therapy), it was unclear if they also met the third criterion (transmissibility). A systematic literature review was conducted to explore the following question in addressing this issue: \u003cem\u003eAre outbreaks caused by E. coli, K. pneumoniae, Klebsiella oxytoca, or Proteus mirabilis with a plasmid-encoded AmpC beta-lactamase (without extended-spectrum beta-lactamase or carbapenemase) observed in healthcare facilities, if only basic IPC measures are implemented?\u003c/em\u003e See \u003cb\u003eAdditional file 1\u003c/b\u003e for the corresponding Population, Intervention, Comparison, and Outcomes (PICO) question, summary of the literature, results, and evidence tables. Three studies were included in the literature analysis (\u003cspan additionalcitationids=\"CR29\" citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e). The GDG concluded that available data from these studies did not justify classifying Enterobacterales with a plasmid-encoded AmpC gene as MDRO requiring additional IPC measures. The literature suggests that the spread of these bacteria in specialized medical care settings has been minimal. Furthermore, a surveillance study in the Netherlands reported a decrease in the carriage of these microorganisms among hospitalized patients from 2013 to 2016, even without additional IPC measures (\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e). Consequently, the GDG concludes that plasmid-mediated AmpC beta-lactamase-producing Enterobacterales do not currently meet the criteria for classification as MDRO. However, given the dynamic nature of hospital-associated bacteria and the unpredictable evolution of microbial trends, there remains a possibility that successful Enterobacterales strains with plasmid-encoded AmpC genes could emerge. Therefore, ongoing surveillance in hospitals is essential to detect any potential rise of such strains.\u003c/p\u003e\n\u003ch3\u003eRecommendation 1\u003c/h3\u003e\n\u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Taba\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eConsider the following microorganism as MDRO:\u003c/p\u003e \u003cp\u003e\u003cb\u003e[\u003c/b\u003e Table \u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e \u003cb\u003e]\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eRecommendation 2\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabb\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDo not classify Enterobacterales with a plasmid-mediated AmpC gene as MDRO. Monitor in hospital settings for increases based on phenotype to detect nosocomial transmission of Enterobacterales with a plasmid-mediated AmpC gene, and implement outbreak management measures to control outbreaks.\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eModule II: Risk assessment for screening of MDRO and recommendations for MDRO selection per risk\u003c/h2\u003e \u003cp\u003eFor the past 20 years, Dutch hospitals have implemented a risk-based screening policy for asymptomatic MDRO carriage upon admission (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e). This policy (search and destroy/control) targeted known MDRO carriers, patients who had been hospitalized in another Dutch healthcare setting with an outbreak within the past two months during an ongoing outbreak, and patients who had been hospitalized in a foreign healthcare setting within the past two months, as they were all considered at higher risk for MDRO carriage. These patients were screened upon admission and (pre-emptively) isolated while awaiting culture results to reduce patient-to-patient transmission. Since 2015, it has also been recommended to additionally screen individuals residing in refugee centers, although this recommendation was based on limited evidence (\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e). Patients treated in foreign healthcare settings were screened for Gram-negative MDRO, while the recommendation to screen individuals from refugee centers did not specify which MDRO to screen for.\u003c/p\u003e \u003cp\u003eThe previous national MDRO guideline (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e), international guidelines, and relevant scientific articles were reviewed to evaluate whether the current risk groups still have an increased risk of MDRO carriage. This review also aimed to determine whether potential new risk groups, such as travelers without healthcare-related contacts, should be added, taking into account the (low) background prevalence of MDROs in the Netherlands.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec13\" class=\"Section2\"\u003e \u003ch2\u003eEvidence and rationale for the recommendations\u003c/h2\u003e \u003cdiv id=\"Sec14\" class=\"Section3\"\u003e \u003ch2\u003eForeign healthcare setting\u003c/h2\u003e \u003cp\u003eSeveral recent studies have examined the risk of MDRO carriage associated with recent admissions to foreign healthcare settings, all of which support the inclusion of hospitalization abroad as a risk factor. See \u003cb\u003eAdditional file 2\u003c/b\u003e for an overview of studies from primarily low-endemic MDRO countries that report the prevalence of MDRO carriage among patients treated in foreign hospitals or otherwise provide data on this risk factor. Based on this data, the GDG recommends maintaining the current risk assessment, which includes recent admission to a healthcare facility abroad for Gram-negative MDRO. However, the GDG also recommends screening for VRE for this group, given the currently low prevalence of VRE in the Dutch population (\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e) and the occasionally high carriage rates within this risk group (\u003cb\u003eAdditional file 2\u003c/b\u003e). Additionally, screening for \u003cem\u003eC. auris\u003c/em\u003e is recommended as \u003cem\u003eC. auris\u003c/em\u003e is an emerging pathogen causing outbreaks of invasive healthcare-related infections worldwide, including in Europe (\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e, \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003eRefugee shelters\u003c/h2\u003e \u003cp\u003eIn recent years, several studies have investigated the prevalence of MDRO among asylum seekers and refugees. See \u003cb\u003eAdditional file 2\u003c/b\u003e for an overview of studies reporting MDRO prevalence among individuals residing in refugee centres. Compared to the background prevalence in the Netherlands, a higher prevalence of MDRO was observed in individuals living in or recently staying at refugee centres. For this reason, the GDG recommends screening individuals who have resided in a refugee centre within the past two months for at least ESBL-producing Enterobacterales and carbapenemase-producing or carbapenem-resistant Enterobacterales (CPE/CRE). The GDG does not recommend screening this group for multidrug-resistant \u003cem\u003eP. aeruginosa\u003c/em\u003e, resistant \u003cem\u003eA. baumannii-calcoaceticus\u003c/em\u003e complex, or \u003cem\u003eC. auris\u003c/em\u003e due to a lack of evidence.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec16\" class=\"Section2\"\u003e \u003ch2\u003ePatients recently traveling abroad (without healthcare contact)\u003c/h2\u003e \u003cp\u003eTraveling abroad is often cited as a risk factor for MDRO carriage. A recent systematic review of 22 studies concluded that the risk of acquiring an MDRO depends on the travel destination and the use of antibiotics during the trip. The highest rates of MDRO carriage were observed after travel to South Asia (median 71%), followed by North Africa (median 41%), with ESBL-producing \u003cem\u003eE. coli\u003c/em\u003e being the most found. Although CPE was found in only a few cases, the culture methods used were not always aimed at detecting it (\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e). A study by Wuerz, which included 15 studies, also showed an increased prevalence of ESBL-producing Enterobacterales among travellers, particularly if fluoroquinolones were used during the trip (\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e). The duration of MDRO carriage acquired during travel is generally short, ranging from a median of 30 days (\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e) to 1\u0026ndash;2 months (\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e), although this can vary depending on the clone.\u003c/p\u003e \u003cp\u003eBased on this data, the GDG concludes that patients who have recently travelled to Asia (including Turkey) and/or Africa have an increased risk of carrying ESBL-producing Enterobacterales and possibly CPE or CRE. The GDG advises healthcare facilities to be vigilant for possible ESBL-producing Enterobacterales and CPE/CRE carriage in travellers from these regions and leaves it to the local healthcare facility, whether to include this group in the risk assessment.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec17\" class=\"Section2\"\u003e \u003ch2\u003eRisk assessment in the outpatient setting\u003c/h2\u003e \u003cp\u003eThe risk assessment is indicated upon or shortly before admission to a healthcare facility, not during outpatient clinic visits (\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e). However, in some outpatient settings, invasive procedures are performed. Additionally, there are outpatient departments that can be considered clinical departments based on the patient population or type of care provided (such as dialysis and oncology day centres). In these cases, the risk of MDRO transmission may be higher or have a larger impact, making a risk assessment necessary. The GDG considers it the responsibility of the healthcare facility to determine which outpatient departments are classified as \u0026ldquo;clinical\u0026rdquo; depending on the invasiveness of the procedures performed or the characteristics of the patient population.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec18\" class=\"Section2\"\u003e \u003ch2\u003eRecommendation 3\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabc\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eConduct following risk assessment upon or shortly before admission to a healthcare facility, as well as during visits to outpatient clinics that the healthcare facility designates as clinical departments:\u003c/p\u003e \u003cp\u003e1. Determine if the patient is a known carrier of an MDRO and implement appropriate infection control measures\u003c/p\u003e \u003cp\u003e2. Screen for carriage of all MDROs listed in Recommendation 1 in patients who meet the following criteria:\u003c/p\u003e \u003cp\u003e● Patients who stayed in a healthcare facility abroad for more than 24 hours within the last two months\u003c/p\u003e \u003cp\u003e● Patients who stayed in a healthcare facility abroad for less than 24 hours within the last two months and underwent an invasive procedure\u003c/p\u003e \u003cp\u003e● Patients who stayed in a healthcare facility abroad between two and twelve months ago and underwent an invasive procedure\u003c/p\u003e \u003cp\u003e3. Screen for MDRO carriage in patients transferred from another Dutch healthcare facility with an ongoing MDRO outbreak. Screen for the specific MDRO causing the outbreak.\u003c/p\u003e \u003cp\u003e4. Screen for extended-spectrum beta-lactamase-producing Enterobacterales (ESBL-E) and carbapenemase-producing or carbapenem-resistant Enterobacterales (CPE/CRE) in patients who have resided in a refugee center within the past two months.\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec19\" class=\"Section2\"\u003e \u003ch2\u003eModule III: Isolation and infection prevention measures\u003c/h2\u003e \u003cp\u003eWhile standard precautions apply to all patient interactions (regardless of their MDRO status), the GDG considers them insufficient to prevent MDRO transmission; therefore, additional organism-specific measures are recommended. While substantial evidence supports these additional measures to prevent MDRO transmission, many studies assessed bundled strategies. These strategies typically combine interventions such as specific personal protective equipment (PPE), single-room or isolation settings, and environmental disinfection. This bundling complicates assessment of the effectiveness of individual interventions. Furthermore, many studies are conducted during outbreaks, often lacking control groups and are prone to performance bias.\u003c/p\u003e \u003cp\u003eTo provide recommendations on which IPC measures should be taken to prevent MDRO transmission, specified by each MDRO, the GDG considered most recommendations from the previous national MDRO guideline (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e), along with international guidelines and expert opinions. A systematic review of the literature was conducted to assess the scientific evidence supporting the need for terminal disinfection of patient rooms when a patient is infected with or colonized by ESBL-producing \u003cem\u003eE. coli\u003c/em\u003e. Another systematic review was performed to determine if additional IPC measures are necessary in the outpatient setting.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec20\" class=\"Section2\"\u003e \u003ch2\u003eEvidence and rationale for the recommendations\u003c/h2\u003e \u003cdiv id=\"Sec21\" class=\"Section3\"\u003e \u003ch2\u003eIsolation and infection prevention measures in the inpatient setting\u003c/h2\u003e \u003cp\u003eTable\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e provides an overview of the isolation and additional IPC measures for each MDRO in the inpatient setting, while \u003cb\u003eAdditional file 3\u003c/b\u003e details the evidence and rationale behind these recommendations.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003ean overview of the isolation and infection prevention measures described for each multidrug-resistant microorganism.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"7\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eMicroorganism\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eResistance\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003ePatient room\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"3\" nameend=\"c6\" namest=\"c4\"\u003e \u003cp\u003ePersonal protective equipment\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eTerminal cleaning and disinfection after discharge, transfer, or death\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eGown\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eSurgical mask\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eGloves\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEnterobacterales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eESBL\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSingle patient room with dedicated sanitary facilities\u003c/p\u003e \u003cp\u003e\u003cb\u003eException\u003c/b\u003e:\u003c/p\u003e \u003cp\u003e\u003cem\u003eA multiple-occupancy room is permitted if no single patient room is available, provided there is a 1.5-meter space around the bed and dedicated sanitary facilities.\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEnterobacterales\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eCarbapenem or carbapenemase\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSingle patient room with dedicated sanitary facilities\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEnterobacterales group II\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eAminoglycosides\u0026thinsp;+\u0026thinsp;fluoroquinolones\u0026thinsp;+\u0026thinsp;sulfamethoxazole/trimethoprim\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSingle patient room with dedicated sanitary facilities\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAcinetobacter baumannii-calcoaceticus\u003c/em\u003e complex\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eAminoglycoside\u0026thinsp;+\u0026thinsp;ciprofloxacin or levofloxacin\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eNegative-pressure isolation room\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAcinetobacter baumannii-calcoaceticus\u003c/em\u003e complex\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eCarbapenemase\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eNegative-pressure isolation room\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ePseudomonas aeruginosa\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003e\u0026ge;\u003c/span\u003e\u0026thinsp;3 of the following:\u003c/p\u003e \u003cp\u003e● Tobramycin or amikacin\u003c/p\u003e\u003cp\u003e● Carbapenem or carbapenemase\u003c/p\u003e\u003cp\u003e● Piperacillin\u003c/p\u003e\u003cp\u003e● Ceftazidime\u003c/p\u003e\u003cp\u003e● Fluoroquinolones\u003c/p\u003e\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSingle patient room with dedicated sanitary facilities\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eEnterococcus faecium\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eVancomycin or \u003cem\u003evanA\u003c/em\u003e gene or \u003cem\u003evanB\u003c/em\u003e gene\u0026thinsp;+\u0026thinsp;penicillin-group\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSingle patient room with dedicated sanitary facilities\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eCandida auris\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eRegardless of resistance\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eNegative-pressure isolation room\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHigh risk for MDRO carriage, regardless of type (e.g. a recent admission to a foreign healthcare facility)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSingle patient room with dedicated sanitary facilities\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eNo\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003eYes\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e \u003cp\u003eYes (if culture results are not yet available)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eIn summary, alongside standard precautions such as hand hygiene according to the WHO's 5 Moments (\u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e), healthcare workers are advised to wear gowns and gloves when in direct contact with patients or their immediate environment in all cases of MDRO. This practice reduces the risk of contaminating hands and clothing, which could otherwise contribute to the transmission of MDRO.\u003c/p\u003e \u003cp\u003eFor the \u003cem\u003eA. baumannii-calcoaceticus\u003c/em\u003e complex and \u003cem\u003eC. auris\u003c/em\u003e, the use of a surgical mask is recommended during patient care. In the case of \u003cem\u003eA. baumannii-calcoaceticus\u003c/em\u003e complex, this is recommended due to insufficient evidence to revise the recommendation from the previous national MDRO guideline (\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e). For \u003cem\u003eC. auris\u003c/em\u003e, a surgical mask is recommended because much remains unknown about the transmission routes of this emerging microorganism.\u003c/p\u003e \u003cp\u003e \u003cem\u003eA. baumannii-calcoaceticus\u003c/em\u003e complex and \u003cem\u003eC. auris\u003c/em\u003e are the only microorganisms for which an isolation room with an anteroom and specific air management (e.g., ventilation control) is recommended. \u003cem\u003eA. baumannii-calcoaceticus\u003c/em\u003e complex can potentially spread via airborne transmission (\u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e, \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e). For \u003cem\u003eC. auris\u003c/em\u003e, although the exact transmission route is not yet fully understood and airborne transmission is unlikely, current literature indicates that it can spread easily and cause outbreaks in healthcare settings (\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e). The presence of an anteroom may improve adherence to infection control measures. For all other MDRO, the GDG advises using a single patient room with dedicated sanitary facilities. An exception is made for ESBL-producing Enterobacterales, for which isolation in a multiple-occupancy room may be permitted under certain conditions. This exception is supported by a recent cluster-randomized study that found no difference in ESBL-producing Enterobacterales infection risk between single and multiple-occupancy rooms (\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e). However, the GDG still prefers single rooms for ESBL-producing Enterobacterales to reduce contamination risk and improve adherence to infection control measures. If a single room is unavailable, contact isolation in a multiple-occupancy room may be allowed, provided a 1.5-meter clearance around the bed and dedicated sanitary facilities.\u003c/p\u003e \u003cp\u003eFinally, terminal disinfection of a patient room following the discharge, transfer, or death of a patient with an MDRO infection or carriage is a widely accepted routine practice in Dutch hospitals. However, the necessity for terminal disinfection specifically for ESBL-producing \u003cem\u003eE. coli\u003c/em\u003e is sometimes debated. In response to this debate, a systematic review of the literature was conducted to address the following question: \u003cem\u003eIs terminal disinfection of a patient room necessary after the discharge, transfer, or death of a patient infected with or carrying ESBL-producing Escherichia coli?\u003c/em\u003e See \u003cb\u003eAdditional file 4\u003c/b\u003e for the PICO criteria and the result of the search. Unfortunately, no studies meeting the PICO criteria were identified. Consequently, the GDG concluded that scientific evidence to support the de-implementation of terminal disinfection for ESBL-producing \u003cem\u003eE. coli\u003c/em\u003e is currently lacking. Therefore, the recommendation remains unchanged from the previous national guideline: terminal disinfection (following cleaning) of the room is always recommended after the discharge, transfer, or death of a patient with any MDRO.\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec22\" class=\"Section2\"\u003e \u003ch2\u003e[ Table \u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e ]\u003c/h2\u003e \u003cdiv id=\"Sec23\" class=\"Section3\"\u003e \u003ch2\u003eRecommendation 4\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabd\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eIn the inpatient setting, when caring for or treating a patient with an MDRO (or a suspected MDRO) involving direct patient contact and/or contact with the patient\u0026rsquo;s immediate environment, apply isolation and additional infection prevention measures as outlined in Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e.\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec24\" class=\"Section2\"\u003e \u003ch2\u003eRecommendation 5\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabe\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFollowing the discharge, transfer, or death of a patient with an MDRO, including ESBL-producing \u003cem\u003eEscherichia coli\u003c/em\u003e, perform terminal cleaning and disinfection of the patient room and the sanitary facility. This recommendation applies to single- and multi-occupancy patient rooms.\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cdiv id=\"Sec25\" class=\"Section3\"\u003e \u003ch2\u003eIsolation and infection prevention measures in the outpatient setting\u003c/h2\u003e \u003cp\u003eIt is unknown whether MDRO transmission occurs during outpatient visits. To address this research question, a systematic review of the literature was conducted. The GDG focused the literature search on evaluating the need for additional IPC measures specifically for VRE, CPE/CRE, and carbapenemase-producing or carbapenem-resistant \u003cem\u003eAcinetobacter baumannii-calcoaceticus\u003c/em\u003e complex (CP/CRAB). This selection was based on the potential risk of spread within healthcare facilities and the challenges of treating infections with limited antibiotic options. The review aimed to answer the following question: \u003cem\u003eAre there outbreaks in outpatient clinics caused by vancomycin-resistant Enterococcus faecium, carbapenemase-producing or carbapenem-resistant Enterobacterales, or carbapenemase-producing or carbapenem-resistant Acinetobacter baumannii-calcoaceticus complex in the absence of additional measures beyond standard precautions\u003c/em\u003e? See \u003cb\u003eAdditional file 5\u003c/b\u003e for the PICO question, a summary of the literature and evidence tables.\u003c/p\u003e \u003cp\u003eThe literature search yielded three outbreak studies (\u003cspan additionalcitationids=\"CR44\" citationid=\"CR43\" class=\"CitationRef\"\u003e43\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e45\u003c/span\u003e) involving VRE and CPE/CRE in outpatient settings. Additionally, one observational study (\u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e46\u003c/span\u003e) described the risk of environmental contamination with VRE during outpatient visits. These outbreak studies indicate that CPE transmission can occur in outpatient clinics and have, in rare cases, initiated outbreaks in healthcare settings. Two studies describe extensive VRE contamination in dialysis units, which can lead to outbreaks. No studies were found regarding outbreaks of CP/CRAB in outpatient settings.\u003c/p\u003e \u003cp\u003eDespite the above findings, the GDG concluded that there is insufficient scientific evidence to support the routine implementation of additional IPC measures in outpatient clinics, as the transmission risk is generally lower than inpatients clinics. The GDG considered that contact and care moments in outpatient clinics are typically shorter and less intensive than inpatient settings. However, in situations where the outpatient clinic functions similarly to an inpatient unit - based on the type of care and/or patient population (e.g., dialysis and oncology day centers) - the GDG identified a higher risk and impact of transmission of VRE, CPE/CRE, and CP/CRAB. Therefore, additional IPC measures for these MDROs are indicated in such settings.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec26\" class=\"Section3\"\u003e \u003ch2\u003eRecommendation 6\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabf\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFor patients with (suspected) vancomycin-resistant \u003cem\u003eEnterococcus faecium\u003c/em\u003e (VRE), carbapenemase-producing or carbapenem-resistant \u003cem\u003eEnterobacterales\u003c/em\u003e (CPE/CRE), or carbapenemase-producing, carbapenem-resistant \u003cem\u003eAcinetobacter baumannii-calcoaceticus\u003c/em\u003e complex (CP/CRAB) in outpatient setting, additional infection prevention measures should be implemented if there is a high risk of transmission due to the nature of the care provided or if transmission would significantly impact the patient population.\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec27\" class=\"Section3\"\u003e \u003ch2\u003eModule IV: Source and contact tracing\u003c/h2\u003e \u003cp\u003eSource and contact tracing are generally considered essential components of IPC policies. They provide insights into the potential spread of an MDRO, enabling early detection and helping prevent further transmission between patients. However, conducting these investigations requires additional resources, including materials, tools, and personnel, which leads to increased costs. Therefore, it is important to determine when and how source and contact tracing should be implemented in cases of unexpected carriage or infection with an MDRO.\u003c/p\u003e \u003cp\u003eIn developing considerations and recommendations, the GDG primarily focused on inpatient care.\u003c/p\u003e \u003cp\u003eTo provide recommendations for conducting source and contact tracing, the GDG reviewed the previous national MDRO guideline (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e), and supplemented it with expert opinion. Consideration was also given to the (low) background prevalence of MDRO in the Netherlands.\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec28\" class=\"Section2\"\u003e \u003ch2\u003eEvidence and rationale for the recommendations\u003c/h2\u003e \u003cp\u003eIn cases of an unexpected MDRO detection, the source and contact investigation follow the \"ring principle\". This method starts by screening those with the highest risk of exposure, typically the patient\u0026rsquo;s roommates or immediate contacts. If another positive case is identified, the screening circle is widened to include patients at moderate or lower risk of exposure. The scope of screening is determined by infection control professionals, such as medical microbiologists or infection control practitioners (\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e). Decisions regarding whether to implement additional isolation and IPC measures for close contacts while awaiting culture results are also made by these specialists as additional infection control measures may not always be necessary. Contact tracing and screening among healthcare workers is generally unnecessary, because MDRO carriage in staff rarely leads to transmission when standard precautionary measures are properly followed (\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec29\" class=\"Section2\"\u003e \u003ch2\u003eException policy for ESBL-producing Escherichia coli in non-outbreak situations\u003c/h2\u003e \u003cp\u003eIn the previous national MDRO guideline, an exception was made for ESBL-producing bacteria, stating that contact tracing was not required for an unexpected ESBL case in non-outbreak situations, provided adequate surveillance was in place within the healthcare facility to detect any increase in cases (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e). The rationale at the time was that approximately 4% of the Dutch population carried ESBL-producing bacteria, making it challenging to identify nosocomial transmission, particularly because accurate typing methods were not yet widely available.\u003c/p\u003e \u003cp\u003eAlthough the prevalence of ESBL carriage in the Netherlands has remained stable at around 5% (\u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e49\u003c/span\u003e), the GDG has revised its recommendation on source and contact tracing. The previous policy remains valid for cases of unprotected contact with ESBL-producing \u003cem\u003eE. coli\u003c/em\u003e, where contact tracing can be omitted if adequate surveillance is in place. However, for other ESBL-producing Enterobacterales, source and contact tracing is now recommended. This revision is due to the global dissemination of ESBL genes among virulent non-\u003cem\u003eE. coli\u003c/em\u003e Enterobacterales lineages, which have increasingly spread within healthcare settings. In recent years, several outbreaks involving ESBL-producing non- \u003cem\u003eE. coli\u003c/em\u003e Enterobacterales have been reported in Dutch hospitals (\u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e50\u003c/span\u003e). These non- \u003cem\u003eE. coli\u003c/em\u003e ESBL-producing Enterobacterales pose a higher transmission risk than \u003cem\u003eE. coli\u003c/em\u003e (\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e), and carriers also face an increased risk of infection (\u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e51\u003c/span\u003e). As a result, source and contact tracing is recommended for all cases of unprotected contact.\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eRecommendation 7\u003c/h3\u003e\n\u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabg\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eConduct source and contact tracing using the ring principle, targeting at least close contacts, when a patient who has been cared for without infection control measures is unexpectedly identified with an MDRO. For unexpected cases of extended-spectrum beta-lactamase (ESBL)-producing \u003cem\u003eEscherichia coli\u003c/em\u003e, source and contact tracing can be omitted if adequate surveillance is implemented.\u003c/p\u003e \u003cp\u003eIt is not necessary to extend source and contact tracing to healthcare workers.\u003c/p\u003e \u003cp\u003eConsult with an expert (e.g., medical microbiologist, or infection control practitioner) to determine whether additional isolation and infection prevention measures should be implemented for close contacts of the patient while awaiting the results of MDRO screening.\u003c/p\u003e \u003cp\u003eIf source and contact tracing indicate that transmission has occurred, initiate an investigation for a potential outbreak.\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cdiv id=\"Sec31\" class=\"Section2\"\u003e \u003ch2\u003eModule V: Discontinuation of isolation and infection prevention measures\u003c/h2\u003e \u003cp\u003eAlthough infection prevention and isolation measures are essential to prevent MDRO transmission, they can reduce patient satisfaction, lower the quality of care provided, and increase healthcare workers' workload (\u003cspan additionalcitationids=\"CR53\" citationid=\"CR52\" class=\"CitationRef\"\u003e52\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e). Therefore, it is important to discontinue these measures once a patient is no longer an MDRO carrier. However, clear criteria for ending isolation remain lacking, and the previous guideline (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e) did not specify the requirements needed to confirm MDRO clearance.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec32\" class=\"Section2\"\u003e \u003ch2\u003eEvidence and rationale for the recommendations\u003c/h2\u003e \u003cp\u003eThe absence of clear criteria to determine when a patient is no longer an MDRO carrier raises important questions for clinical practice. To address these, a systematic review of the literature was conducted. The review aimed to answer the following question: \u003cem\u003eWhen can a patient with a previously detected MDRO be considered MDRO-free (i.e., after what duration and/or under what conditions)?\u003c/em\u003e Details of the PICO framework, a summary of the literature, and evidence tables, can be found in \u003cb\u003eAdditional file 6\u003c/b\u003e. A systematic search was performed to provide evidence-based answers to the clinical question.\u003c/p\u003e \u003cp\u003eThe literature search led to the inclusion of 15 studies (\u003cspan additionalcitationids=\"CR56 CR57 CR58 CR59 CR60 CR61 CR62 CR63 CR64 CR65 CR66 CR67 CR68\" citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e69\u003c/span\u003e). The GDG noted significant variation in the reported duration of MDRO carriage across these studies. This variability can be partly explained by differences in diagnostic methods for detecting MDRO, variations in the number and locations of cultures collected, and the intrinsic characteristics of the microorganisms. Although spontaneous loss of an MDRO often occurs within a few months, some individuals may carry MDRO for several years. Because the duration of carriage is unpredictable at the individual level, follow-up cultures are necessary to confirm MDRO clearance. Moreover, insights into the course of MDRO carriage have motivated recommendations regarding the optimal timing of follow-up cultures.\u003c/p\u003e \u003cp\u003eThe literature shows that multiple cultures are needed to confirm the end of MDRO carriage reliably. Studies suggest using 1 to 3 negative cultures to define loss of carriage of ESBL-producing Enterobacterales and CPE/CRE. For VRE, 2 to 5 negative cultures are suggested. Misclassifying an MDRO carrier as MDRO-negative can increase the risk of an outbreak due to the premature discontinuation of isolation and IPC measures. The likelihood that a patient is correctly identified as MDRO-negative depends partly on the duration of carriage and the number of negative cultures obtained.\u003c/p\u003e \u003cp\u003eGiven the very low level of evidence regarding the optimal timing and number of cultures, the GDG based its recommendations on insights from the literature and expert opinion. These recommendations take into account the risk of MDRO transmission within healthcare facilities and the potential for these organisms to cause infections that are difficult to treat with antibiotics.\u003c/p\u003e \u003cp\u003eFor sampling sites, the GDG refers to the Dutch national guideline \u003cem\u003eLaboratory Detection of Multidrug-Resistant Organisms\u003c/em\u003e (\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e70\u003c/span\u003e), which generally includes rectal swabs or feces and, if applicable, clinical sites. \u003cem\u003eC. auris\u003c/em\u003e is currently not included in the laboratory detection guideline. Pending a revision of this guideline, the GDG recommends following the guidance of Meijer et al. (\u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e71\u003c/span\u003e): obtaining throat, nasal, and (peri-)anal swabs, along with additional swabs from the axilla, groin, and any other previously identified positive sites.\u003c/p\u003e \u003cp\u003eFor patients known to be MDRO carriers who are likely to require readmission or future care, follow-up cultures are advised to confirm the clearance of MDRO carriage. Patients should be informed about the importance of these follow-up cultures and the process for obtaining them.\u003c/p\u003e \u003cp\u003eThe GDG recommends follow-up cultures starting three months after the last positive culture to determine the loss of carriage of ESBL-producing Enterobacterales. The study with the largest number of patients (\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e) showed that after three months, 25% of the carriers have spontaneously lost the MDRO. The GDG considers the impact of incorrectly declaring loss of carriage for this MDRO type minimal. Therefore, the GDG advises confirming the end of carriage with two negative cultures taken on separate days, in line with common practice in studies and reflecting current practice in Dutch healthcare facilities. If the patient has received antibiotics to which the ESBL-producing Enterobacterales is susceptible, the first culture should be obtained at least 48 hours after the antibiotics have been discontinued.\u003c/p\u003e \u003cp\u003eFor CPE/CRE, similar to ESBL-producing Enterobacterales, 25% of patients spontaneously lost the MDRO after three months, as reported in the previously mentioned study (\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e). However, Oren et al. (\u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e72\u003c/span\u003e) reported that 45% of patients who initially tested negative for CPE/CRE had subsequent positive cultures. Due to the significant impact of the spread of CPE/CRE and based on the GDG\u0026rsquo;s experience that individuals who test negative in the first year may remain carriers in subsequent follow-up cultures, the GDG advises that a CPE/CRE carrier should be considered MDRO-positive during the first year after the last positive culture, even if negative cultures are obtained. After one year, the likelihood of decolonization increases, and the end of carriage can be confirmed with two negative cultures, similar to the approach for ESBL-producing Enterobacterales. To minimize the risk of incorrectly declaring a patient MDRO-free, the GDG recommends that follow-up cultures (one set) be taken during the year following the end of carriage if the patient is admitted to a healthcare facility. If antibiotics to which CPE/CRE are susceptible have been administered, the first culture should be obtained at least 48 hours after the antibiotics have been discontinued.\u003c/p\u003e \u003cp\u003eLong-term carriage for VRE is common, and the risk of VRE transmission in healthcare settings is high. The GDG recommends managing VRE carriers in a manner similar to CPE/CRE, considering them positive during the first year after the last positive culture, even if negative cultures are obtained. False-negative culture results are more common for VRE compared than for antimicrobial-resistant Enterobacterales. Current evidence suggests that the end of VRE carriage can be reliably confirmed (\u0026ge;\u0026thinsp;95%) with five negative cultures, provided selective broth enrichment is used (\u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e73\u003c/span\u003e). Sensitivity increases to 99.3% when molecular diagnostics and a selective broth enrichment step are used together (\u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e74\u003c/span\u003e). If both a selective broth enrichment and polymerase chain reaction (PCR) are performed, the GDG advises establishing the end of carriage with three negative cultures. Additionally, the GDG recommends taking follow-up cultures (one set) during the first year after the end of carriage when the patient is admitted to a healthcare facility. If antibiotics susceptible to VRE have been given, the first culture should be taken at least 48 hours after discontinuation of antibiotic therapy.\u003c/p\u003e \u003cdiv id=\"Sec33\" class=\"Section3\"\u003e \u003ch2\u003eOther MDRO\u003c/h2\u003e \u003cp\u003eFor multidrug-resistant group II Enterobacterales, multidrug-resistant \u003cem\u003ePseudomonas aeruginosa\u003c/em\u003e, resistant \u003cem\u003eAcinetobacter baumannii-calcoaceticus\u003c/em\u003e complex and \u003cem\u003eC. auris\u003c/em\u003e, the GDG is not aware of adequate studies on timing and number of cultures required to determine the end of carriage. However, since there is a need for recommendations for these MDRO, the same reasoning was applied as for ESBL-producing Enterobacterales, CPE/CRE, and VRE. For multidrug-resistant group II Enterobacterales, the expected duration of carriage and the associated impact are considered like those for ESBL-producing Enterobacterales. Therefore, the GDG makes the same recommendation as for ESBL-producing Enterobacterales. For multidrug-resistant \u003cem\u003ePseudomonas aeruginosa\u003c/em\u003e, resistant \u003cem\u003eAcinetobacter baumannii-calcoaceticus complex\u003c/em\u003e, and \u003cem\u003eC. auris\u003c/em\u003e, GDG considers the risks and the sensitivity of detection methods to be comparable to CPE/CRE. Thus, the recommendations for the timing and number of cultures are the same as those for CPE/CRE.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec34\" class=\"Section3\"\u003e \u003ch2\u003eRecommendation 8\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabh\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eWhen expecting readmission or future care, take follow-up cultures to demonstrate the end of MDRO carrier status based on the MDRO schedule outlined below. Cultures should only be collected if the patient has not received antimicrobials that suppress the growth of the relevant MDRO during and up to 48 hours prior to the culture collection.\u003c/p\u003e \u003cp\u003e\u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003eESBL-producing Enterobacterales (ESBL-E) and multidrug-resistant (MDR) group II Enterobacterales\u003c/span\u003e\u003c/p\u003e \u003cp\u003e- Confirm the end of ESBL-E and MDR group II Enterobacterales carriage with two negative culture sets, collected on separate days, starting at least three months after the last positive culture.\u003c/p\u003e \u003cp\u003e\u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003eCarbapenemase-producing or carbapenem-resistant\u003c/span\u003e \u003cspan type=\"ItalicUnderline\" class=\"ItalicUnderline\" name=\"Emphasis\"\u003eEnterobacterales\u003c/span\u003e \u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003e(CPE/CRE)\u003c/span\u003e\u003c/p\u003e \u003cp\u003e- Confirm the end of CPE/CRE carriage with two negative culture sets, collected on separate days, starting one year after the last positive culture.\u003c/p\u003e \u003cp\u003e- Take follow-up cultures (one culture set) if a patient is admitted to a healthcare institution in the first year after termination of carrier status to check for recurrences.\u003c/p\u003e \u003cp\u003e\u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003eVancomycin-resistant\u003c/span\u003e \u003cspan type=\"ItalicUnderline\" class=\"ItalicUnderline\" name=\"Emphasis\"\u003eEnterococcus faecium\u003c/span\u003e \u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003e(VRE)\u003c/span\u003e\u003c/p\u003e \u003cp\u003e- Confirm the end of VRE carriage with five negative culture sets, collected on different days, starting one year after the last positive culture. Three negative culture sets are sufficient if both a selective broth enrichment and PCR are used for detection.\u003c/p\u003e \u003cp\u003e- Take follow-up cultures (one culture set) if a person is admitted to a healthcare institution in the first year after the end of carriage to check for recurrences.\u003c/p\u003e \u003cp\u003e\u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003eMultidrug-resistant\u003c/span\u003e \u003cspan type=\"ItalicUnderline\" class=\"ItalicUnderline\" name=\"Emphasis\"\u003eP. aeruginosa\u003c/span\u003e \u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003eand resistant\u003c/span\u003e \u003cspan type=\"ItalicUnderline\" class=\"ItalicUnderline\" name=\"Emphasis\"\u003eAcinetobacter baumannii-calcoaceticus\u003c/span\u003e \u003cspan type=\"Underline\" class=\"Underline\" name=\"Emphasis\"\u003ecomplex\u003c/span\u003e\u003c/p\u003e \u003cp\u003e- Confirm the end of multidrug-\u003cem\u003eresistant P. aeruginosa\u003c/em\u003e and resistant \u003cem\u003eA. baumannii-calcoaceticus\u003c/em\u003e complex carriage with two negative culture sets, collected on separate days, starting one year after the last positive culture.\u003c/p\u003e \u003cp\u003e- Take follow-up cultures (one culture set) if a person is admitted to a healthcare institution in the first year after the end of carriage to check for recurrences.\u003c/p\u003e \u003cp\u003e\u003cspan type=\"ItalicUnderline\" class=\"ItalicUnderline\" name=\"Emphasis\"\u003eCandida auris\u003c/span\u003e\u003c/p\u003e \u003cp\u003e- Confirm the end of \u003cem\u003eCandida auris\u003c/em\u003e carriage with two negative culture sets collected on separate days, starting one year after the last positive culture.\u003c/p\u003e \u003cp\u003e- Take follow-up cultures (one culture set) if a person is admitted to a healthcare institution in the first year after the end of carriage status to check for recurrences.\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003c/div\u003e \u003c/div\u003e\n\u003ch3\u003eModule VI: Organization of care\u003c/h3\u003e\n\u003cp\u003eThe Netherlands is recognized for having a significantly lower MDRO prevalence compared to many other countries (\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e, \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e). In order to preserve this low prevalence, there are essential organizational requirements for managing patients with a suspected or confirmed MDRO infection or carrier status.\u003c/p\u003e \u003cp\u003eHealthcare facilities must ensure safe care by implementing transparent IPC policies and clearly communicating MDRO status to care providers and patients. Patient MDRO status should be shared with care providers and explained to patients. Outbreaks require a coordinated response by an outbreak management team, including isolation, contact tracing, and reporting to public health authorities. In addition to managing outbreaks, institutional MDRO policies should carefully balance IPC with the individual care needs, behaviour, and well-being of patients. Special consideration is required for the impact of prolonged isolation or restrictions, ensuring patient well-being is preserved while safeguarding public health.\u003c/p\u003e \u003cp\u003eTo support epidemiology and regional/national outbreak management, outbreaks must be reported in accordance with the Public Health Act. Healthcare institutions must notify the Health and Youth Care Inspectorate of incidents as specified in the Healthcare Quality Act. In the event of an MDRO outbreak, the Health and Youth Care Inspectorate emphasizes the importance of early reporting to the Healthcare-associated Infections and Antimicrobial Resistance Monitoring Group (SO-ZI/AMR), a national advisory body dedicated to providing timely national monitoring and risk assessment of nosocomial outbreaks (\u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e50\u003c/span\u003e).\u003c/p\u003e\n\u003ch3\u003eSurveillance of MDRO\u003c/h3\u003e\n\u003cdiv id=\"Sec37\" class=\"Section2\"\u003e \u003ch2\u003eNational / regional\u003c/h2\u003e \u003cp\u003eBuilding on organizational efforts to manage MDROs, effective surveillance is important for monitoring and controlling their spread. In the Netherlands, national surveillance is conducted by the RIVM for CP/CRAB and carbapenemase-producing \u003cem\u003ePseudomonas aeruginosa\u003c/em\u003e. Additionally, sharing information about MDRO spread within healthcare institutions is encouraged through regional healthcare networks to facilitate earlier detection and prevent transmission.\u003c/p\u003e \u003cdiv id=\"Sec38\" class=\"Section3\"\u003e \u003ch2\u003eSpecialist medical care\u003c/h2\u003e \u003cp\u003eUnder the current risk assessment, some MDRO carriers may not be identified promptly within specialist medical care. However, it is important to recognize the early spread of MDROs. Medical microbiologists and IPC experts are responsible for implementing an effective surveillance system that includes monitoring MDROs through clinical cultures and routine screening swabs, investigating potential epidemiological links, and performing typing when needed. Additional methods, such as screening all currently hospitalized patients at a certain point in time (point prevalence study), or screening patients with a prolonged hospital stay (e.g. 7 or 10 days), may enhance early detection and outbreak prevention.\u003c/p\u003e \u003cp\u003eAt present, not all resistant microorganisms are categorized as MDROs. However, some resistant organisms may eventually meet the criteria and be classified as such. The plasmid AmpC-producing \u003cem\u003eKlebsiella\u003c/em\u003e spp. (except \u003cem\u003eK. aerogenes\u003c/em\u003e), \u003cem\u003eE. coli\u003c/em\u003e and \u003cem\u003eP. mirabilis\u003c/em\u003e are not currently designated as MDROs. Nevertheless, hospitals should implement surveillance to detect the emergence of new, successful AmpC gene-carrying Enterobacterales. This can be done, for example, by monitoring the presence of ESBL-negative isolates of these species with a cefotaxime and/or ceftazidime MIC\u0026thinsp;\u0026ge;\u0026thinsp;8 ug/ml in clinical cultures.\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec39\" class=\"Section2\"\u003e \u003ch2\u003eRecommendation 9\u003c/h2\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"No\" id=\"Tabi\" border=\"1\"\u003e \u003ccolgroup cols=\"1\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e- Share information about the spread of MDROs within the healthcare institution nationally and regionally.\u003c/p\u003e \u003cp\u003e- Establish a surveillance system to detect the early spread of MDROs.\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cdiv id=\"Sec40\" class=\"Section3\"\u003e \u003ch2\u003eEpilogue\u003c/h2\u003e \u003cp\u003eIn 2021, the Ministry of Health, Welfare, and Sport launched a new initiative called the Dutch Collaborative Partnership for Infection Prevention Guidelines (Samenwerkingsverband Richtlijnen Infectiepreventie, SRI) (\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e). The SRI is a collaboration among various key stakeholders to develop, maintain, and manage high-quality infection prevention and control (IPC) guidelines with broad support. One of the first guidelines published by the SRI was the guideline for IPC of multidrug-resistant organisms (MDROs) for hospitals.\u003c/p\u003e \u003cp\u003eThe previous national MDRO guideline served as the foundation for this new version. A key improvement was that the updated guideline was developed in line with the recommendations from The Appraisal of Guidelines for Research and Evaluation (AGREE-II) (\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e). This is a highly structured, transparent, and informative system for assessing the quality of evidence used in guideline development. Evidence-based guidelines are generally recognized for improving the effectiveness and quality of care, reducing variations in healthcare practices, and minimizing costly and avoidable adverse events (\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eUnfortunately, there is often limited availability of high-quality graded evidence to support strong recommendations in IPC. A recent review by Mitchell et al. (\u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e75\u003c/span\u003e) evaluated 31 national and international IPC guidelines published over the last decade, revealing that most recommendations were based on low-quality evidence. This is primarily because conducting randomized controlled trials in this area is often neither feasible nor ethical.\u003c/p\u003e \u003cp\u003eThis lack of high-quality graded evidence presents a challenge for guideline developers. During the development of the MDRO guideline, the team systematically searched for relevant research to address the key questions posed. Some questions could be answered with the available evidence, while others could not be conclusively answered. The evidence-based methodology used in the guideline development process highlighted existing knowledge gaps. Consequently, the guideline development group (GDG) identified areas where scientific knowledge is limited, and further research is required to strengthen future recommendations (\u003cb\u003eAdditional file 7\u003c/b\u003e).\u003c/p\u003e \u003cp\u003eIn the initial phases of the guideline development, the GDG consulted relevant professional organizations to gather input on the challenges encountered in caring for patients with MDROs. These consultations provided a comprehensive overview of challenges in the field, which were subsequently prioritized by the GDG to formulate draft key questions. While this structured approach ensured a focus on the most pressing issues, it also highlighted a wide range of challenges that extended beyond the scope of the clinical questions ultimately addressed in this guideline. Due to time and resource constraints, not all identified challenges could be addressed in this version of the guideline. This underscores the need for sustained efforts and sufficient resources to address the existing and new challenges in IPC.\u003c/p\u003e \u003cp\u003eAs this guideline specifically focuses on medical specialist care, particularly hospitals, a separate guideline for prevention and control of MDRO in long-term care settings is currently under development by the SRI as a derivative of the hospital guideline and is scheduled for publication in 2025. This ensures that IPC measures are appropriately tailored to the distinct contexts and needs of both hospital and long-term care sectors.\u003c/p\u003e \u003cp\u003eTo conclude, this guideline aims to provide recommendations on the definitions of MDRO and measures to prevent the transmission of MDRO in hospitals, thereby contributing to maintaining low levels of antimicrobial resistance in the Netherlands. However, additional research is essential to provide more precise answers to practical and unanswered questions in the future.\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e"},{"header":"Abbreviations","content":"\u003cp\u003eAGREE-II: Appraisal of Guidelines for Research and Evaluation II\u003c/p\u003e\n\u003cp\u003eCP: carbapenemase-producing Acinetobacter baumannii-calcoaceticus complex\u003c/p\u003e\n\u003cp\u003eCPE: carbapenemase-producing Enterobacterales\u003c/p\u003e\n\u003cp\u003eCRAB: carbapenem-resistant Acinetobacter baumannii-calcoaceticus complex\u003c/p\u003e\n\u003cp\u003eCRE: carbapenem-resistant Enterobacterales\u003c/p\u003e\n\u003cp\u003eESBL: extended-spectrum beta-lactamase\u003c/p\u003e\n\u003cp\u003eEU/EEA: European Union / European Economic Area\u003c/p\u003e\n\u003cp\u003eGDG: Guideline Development Group\u003c/p\u003e\n\u003cp\u003eGRADE: Grading of Recommendations Assessment, Development and Evaluation\u003c/p\u003e\n\u003cp\u003eIGJ: Dutch Health and Youth Care Inspectorate (Inspectie Gezondheidszorg en Jeugd)\u003c/p\u003e\n\u003cp\u003eIPC: Infection prevention and control\u003c/p\u003e\n\u003cp\u003eMDR-TB: multidrug-resistant tuberculosis\u003c/p\u003e\n\u003cp\u003eMDRO: multidrug-resistant organisms\u003c/p\u003e\n\u003cp\u003eMRSA: methicillin-resistant \u003cem\u003eStaphylococcus aureus\u003c/em\u003e\u003c/p\u003e\n\u003cp\u003eNIV: Dutch Society of Internal Medicine\u003c/p\u003e\n\u003cp\u003eNVAB Netherlands Society of Occupational Medicine\u003c/p\u003e\n\u003cp\u003eNVDV: Dutch Society of Dermatology and Venereology\u003c/p\u003e\n\u003cp\u003eNVMM: Dutch Society of Medical Microbiology\u003c/p\u003e\n\u003cp\u003ePCR: polymerase chain reaction\u003c/p\u003e\n\u003cp\u003ePFNL: Patient Federation Netherlands\u003c/p\u003e\n\u003cp\u003eRIVM: National Institute for Public Health and the Environment\u003c/p\u003e\n\u003cp\u003eSO-ZI/AMR: Healthcare-associated Infections and Antimicrobial Resistance Monitoring Group\u003c/p\u003e\n\u003cp\u003eSRI: Dutch Collaborative Partnership for Infection Prevention Guidelines (Samenwerkingsverband Richtlijnen Infectiepreventie)\u003c/p\u003e\n\u003cp\u003eV\u0026amp;VN: Dutch Nursing Association\u003c/p\u003e\n\u003cp\u003eVerenso: Dutch Association of Elderly Care Physicians and Social Geriatricians\u003c/p\u003e\n\u003cp\u003eVHIG: Dutch Society of Infection Prevention and Control in the healthcare setting\u003c/p\u003e\n\u003cp\u003eVRE: vancomycin-resistant Enterococcus faecium\u003c/p\u003e\n\u003cp\u003eVWS: Dutch Ministry of Health, Welfare, and Sport\u003c/p\u003e\n\u003cp\u003eWHO: World Health Organization\u003c/p\u003e\n\u003cp\u003eWIP: Dutch Working Party on Infection Prevention (Werkgroep Infectie Preventie)\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eEthics approval and consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003ch2\u003eFunding\u003c/h2\u003e\n\u003cp\u003eThe development of the SRI guideline MDRO was funded by the Dutch Ministry of Health, Welfare, and Sport (VWS). The funder had no influence on the guideline\u0026rsquo;s content.\u003c/p\u003e\n\u003ch2\u003eAuthors\u0026apos; contributions\u003c/h2\u003e\n\u003cp\u003eAS and VW were equal contributors to the draft of the manuscript. AS, VW, EB, MT, JO, BV, PB, YR, JV, PM, RN, MK, AV, HG, BV and JS contributed to conceptualization, formal analysis, and writing and editing of the guideline. AS, MK, HG and BV provided methodological guidance and support. All authors read and approved the final manuscript.\u003c/p\u003e\n\u003ch2\u003eAcknowledgements\u003c/h2\u003e\n\u003cp\u003eWe thank information specialist Ingeborg van Dusseldorp of the Knowledge Institute of the Dutch Association of Medical Specialists for her help and support with the literature searches. We also thank Rosa van Mansfeld and Wil van der Zwet for their contribution to defining which microorganisms should be classified as MDRO during the NVMM consultation with its members. Additionally, we are grateful to all participants of the invitational conference and professional groups who attended the invitational conference, reviewed the draft guideline and provided important input for its final version. This guideline was prepared and approved by the Samenwerkingsverband Richtlijnen Infectiepreventie (SRI) and do not necessarily reflect the opinions of Antimicrobial Resistance and Infection Control or its Editors.\u003c/p\u003e\n\u003ch2\u003eAvailability of data and materials\u003c/h2\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003eCompeting interests\u003c/p\u003e\n\u003cp\u003eThe authors declare that they have no competing interests.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAntimicrobial Resistance C (2022) Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. 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Front Microbiol 9:828\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"hideJournal":true,"highlight":"","institution":"Samenwerkingsverband Richtlijnen Infectiepreventie","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Guidelines, infection control, cross infection, evidence-based practice, Microbial Drug Resistance, Transmission","lastPublishedDoi":"10.21203/rs.3.rs-6957898/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-6957898/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe emergence of multidrug-resistant organisms (MDROs) represents a significant challenge for global healthcare systems. The Netherlands maintains one of the lowest antimicrobial resistance rates in the world, attributed to prudent antibiotic use and effective infection prevention and control policies in healthcare settings. This report presents an updated national guideline for the infection prevention and control of MDROs in hospitals, developed by the Dutch Collaborative Partnership for Infection Prevention Guidelines (SRI). Using a multidisciplinary approach and evidence-based frameworks such as AGREE-II and GRADE, the guideline addresses the definition of MDRO, risk assessment and recommendations for MDRO screening, isolation and infection prevention measures, source and contact tracing, discontinuation of isolation measures, and organization of care. It incorporates new evidence, and other aspects such as patient perspectives, sustainability, costs, and organizational factors, providing practical recommendations to mitigate MDRO transmission. This update aims to strengthen national infection control practices and sustain the Dutch low antimicrobial resistance levels.\u003c/p\u003e","manuscriptTitle":"Dutch guideline for the prevention and control of multidrug-resistant organisms in the hospital setting, 2024 update","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-06-25 03:37:52","doi":"10.21203/rs.3.rs-6957898/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"db83b2da-5526-425b-81cd-0248c865f7b9","owner":[],"postedDate":"June 25th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":50503904,"name":"Infectious Diseases"},{"id":50503905,"name":"Hospital Medicine"},{"id":50503906,"name":"Health Policy"}],"tags":[],"updatedAt":"2025-06-25T03:37:52+00:00","versionOfRecord":[],"versionCreatedAt":"2025-06-25 03:37:52","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-6957898","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-6957898","identity":"rs-6957898","version":["v1"]},"buildId":"8U1c8b4HqxoKbykW_rLl7","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}