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Technology for the prevention of antimicrobial resistance and healthcare-associated infections; 2017 Geneva IPC-Think Tank (Part 2)

Technology for the prevention of antimicrobial resistance and healthcare-associated infections;... Background: The high burden of healthcare-associated infections (HAIs) and antimicrobial resistance (AMR) is partially due to excessive antimicrobial use both in human and animal medicine worldwide. How can technology help to overcome challenges in infection prevention and control (IPC) and to prevent HAI and emerging AMR? Methods: In June 2017, 42 international experts convened in Geneva, Switzerland to discuss four potential domains of technology in IPC and AMR: 1) role and potential contribution of microbiome research; 2) whole genome sequencing; 3) effectiveness and benefit of antimicrobial environmental surfaces; and 4) future research in hand hygiene. Results: Research on the microbiome could expand understanding of antimicrobial use and also the role of probiotics or even faecal transplantation for therapeutic purposes. Whole genome sequencing will provide new insights in modes of transmission of infectious diseases. Although it is a powerful tool for public health epidemiology, some challenges with interpretation and costs still need to be addressed. The effectiveness and cost-effectiveness of antimicrobially coated or treated environmental high-touch surfaces requires further research before they can be recommended for routine use. Hand hygiene implementation can be advanced, where technological enhancement of surveillance, technique and compliance are coupled with reminders for healthcare professionals. Conclusions: The four domains of technological innovation contribute to the prevention of HAI and AMR at different levels. Microbiome research may offer innovative concepts for future prevention, whole genome sequencing could detect new modes of transmission and become an additional tool for effective public health epidemiology, antimicrobial surfaces might help to decrease the environment as source of transmission but continue to raise more questions than answers, and technological innovation may have a role in improving surveillance approaches and supporting best practice in hand hygiene. Keywords: Technology, Infection prevention and control, Microbiome, Whole genome sequencing, Copper, Hand hygiene, CDC, ECDC, WHO * Correspondence: Walter.Zingg@hcuge.ch Infection control programme and WHO collaborating center, University of Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle Perret-Gentil, 1211, Geneva 14, Switzerland Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zingg et al. Antimicrobial Resistance and Infection Control (2019) 8:83 Page 2 of 5 Background The use of antibiotics interferes with the balance of the A panel of 42 international experts with backgrounds in microbiota, which results in diseases such as Clostridoides infection prevention and control (IPC), microbiology, in- difficile infection (CDI), or can promote the selection of fectious diseases, public health, psychology, medical tech- multidrug-resistance microorganisms (MDROs) [2]. Im- nology, and social sciences, convened for two days at the proved understanding on the impact of antimicrobials on Geneva Think Tank on IPC and antimicrobial resistance the microbiome could improve stewardship efforts. Probio- (AMR) in June 2017 under the auspices of the US Centers tics and faecal transplantation are two examples of micro- for Disease Control and Prevention (CDC), the World biota restoration -related interventions with potential for Health Organization (WHO), and the University of Gen- prevention and treatment [3–5], respectively. Probiotics eva Hospitals and Faculty of Medicine (HUG). The experts can be preventive (e.g. in the prevention of necrotizing en- were from both high- and low-and-middle-income coun- terocolitis in preterm infants) but also have the potential to tries, and from all five continents. The objectives were to be harmful (e.g. in causing probiotic species-related infec- develop a vision on IPC and AMR and to agree on a road tion in immunocompromised patients). IPC professionals map for research and public health activities. Three dimen- may be concerned particularly with the latter, but micro- sions on IPC and AMR were discussed: 1) implementation biota-based intervention as a prevention strategy for AMR of IPC and antimicrobial stewardship; 2) technology in IPC is innovative with beneficial potential. Microbiome research and AMR; and 3) broadening the global IPC network. This can help in directing researchers to ask the right questions is thesecondina series of three2017GenevaIPC-Think on benefits and risks of such interventions, and to design Tank papers; it summarises the discussions about technol- clinical studies with new products. Faecal transplantation ogy in the prevention of healthcare-associated infections is a different way of influencing the microbiota, and (HAIs) and AMR. has been successfully tested to treat recurrent CDI. However, in terms of AMR, additional research is still needed to understand the impact and best uses of Methods this strategy. Four domains of technological innovation for IPC and AMR were assessed: 1) role and potential of microbiome research; 2) potential of whole genome sequencing Whole genome sequencing (WGS); 3) effectiveness and cost-effectiveness of anti- Whole genome sequencing is another rapidly growing microbial surfaces; and 4) future research in hand hy- field of research within IPC and AMR, and reports using giene surveillance and improvement. The domains were this technology are growing in numbers. Organisations selected as a consensus by CDC, WHO, and HUG. Each such as the US CDC and the European Centre for Dis- domain was introduced with a short summary presenta- ease Prevention and Control (ECDC) promote the use of tion by one of the experts, before they were allocated to WGS because of its many strengths such as detailed spe- four focus groups. The discussions were guided by a cies identification, detection of antimicrobial resistance moderator, tape recorded, and documented by writers. at the mechanism level, reproducibility, and objective The experts were invited to express their personal views, comparison of data. For example, in 2018, all Swiss uni- expectations and concerns in relation to using technol- versity hospitals are routinely using this technology to ogy in IPC and AMR. At the end of the four discussion identify clusters and epidemics on a local, national and rounds a plenary session was organised, where abstracts international scale. Combining information on species from the groups were summarized. and antimicrobial resistance using WGS would be a par- ticularly interesting advance in the monitoring of AMR Results on regional, national and international levels. The role of the microbiome This technology is still growing and a number of chal- The populations of microbial species living on or in the lenges need to be addressed. At least today, phenotypic in- human body are known as the microbiota; the micro- formation is needed to inform genotypic interpretation, biome is the total of the genes of the microbiota. While and data interpretation will constantly change over time. the total number of human cells and microbial cells is Although some countries are investing in national data- similar, there are 50 times more bacterial genes than hu- base platforms, there is a lack of valid international refer- man genes in or on a human individual (10 versus 2 × ence platforms. Today, WGS still is a research tool – 10 )[1]. The majority of the microbiota, and of the although advancing rapidly – and as such, many re- microbiome, is found in the intestines. Research on the searchers use their own standards and references for data microbiome as part of our immune system is rapidly interpretation. Epidemiological use of WGS on the other progressing but has not yet emerged into a mature tech- hand would need valid standards and international librar- nology in relation to IPC or AMR. ies, even if the latter grow and change over time. Zingg et al. Antimicrobial Resistance and Infection Control (2019) 8:83 Page 3 of 5 Costs are currently still high, but new, less expensive efforts to incorporate technology into hand hygiene meas- kits are becoming available. However, for low-and-mid- urement. For example, a study using video surveillance dle-income countries, these kits might still be too expen- did highlight some success [9], while surveillance using sive. Whole genome sequencing needs highly trained handrub counters showed effectiveness only after imple- people, particularly for data analysis and interpretation, menting a positive deviance strategy [10]. which adds to the costs of this technology. Open source Non-alcohol-based hand cleansing agents (with spori- software makes interpretation easier and faster than in the cidal activity) were considered to improve compliance and past, and software integrating epidemiology data with act longer (particularly relevant for surgery), but no such those from WGS are getting on the market. product is available for daily routine use at the frontline. The experts perceived automated surveillance positively. Antimicrobial surfaces They decided that more research should be invested there, There is agreement that hospital cleaning is key for pa- with a view to providing more credible data than is cur- tient safety and that materials and design should facili- rently obtained in many settings. The use of new tate cleanliness. Surfaces in hospital environments are un-obtrusive surveillance technologies would be preferable, often contaminated with microorganisms, however, to even at the cost of accuracy. However, is such technology what extent this contamination contributes to MDRO affordable? Compared to the time needed for direct hand transmission is not yet clear [6, 7]. It is known that hygiene observation, automated surveillance might be cleaning practices are inconsistent, and that surfaces cost-effective and would give IPC professionals time to re-contaminate rapidly after cleaning. do other tasks. An emerging question is how new techno- Antimicrobial surfaces are intended to keep bacterial logical innovation could guide healthcare workers to per- loads low, and thus reduce the risk of pathogen trans- form hand hygiene at the right moment. Colour changing mission. The added value of antimicrobial surfaces to a products or electronic reminders were proposed as imagin- clean hospital environment is largely unknown, and able, forward-looking strategies. The ideal hand hygiene other technologies may contribute more to patient agent would have to be fast acting, long-lasting, safety. Ideally, antimicrobial surfaces would not need quick-drying, and skin-friendly with a wide range of effect- maintenance, but exhibit permanent effectiveness. How- iveness (also towards spores and non-enveloped viruses). ever, such a technology is not yet in sight. Copper ap- Longer-lasting agents would be good, but more important pears to be effective in reducing bioburden, but is than duration is effectiveness. In addition to effectiveness, expensive and may even be stolen from hospitals (there other aspects such as price, local production, and ecological is an illegal market for copper in some countries). properties (waste) must be considered for future products. Low-and-middle-income countries do not have the re- Appropriate exposure time, application technique and opti- sources to buy copper or other even more sophisticated mal number and placement of handrub dispensers are add- surfaces. Furthermore, all marketed products today need itional research questions. to be manually cleaned. Thus, cost-effectiveness has been difficult to be demonstrated. A number of ques- Discussion tions (rather than answers) were raised for antimicrobial The IPC community has focussed on best practices for surfaces by the experts: which surfaces in a hospital the prevention of HAI and AMR in recent years, includ- should be coated: high-touch surfaces (used by different ing aspects related to implementation and behaviour people) such as door handles, surfaces in the patient change. However, at the same time new technologies are zone including textiles, toilets and showers, or any sur- being evaluated or are becoming more broadly available. face in a patient room? Could there be resistance to sur- The microbiota has a number of functions in nutrition, face antimicrobials? Maybe, surfaces and equipment that metabolism, and maturation of the immune system, and are carefully designed for easy cleaning would be more thus, research on this topic going beyond probiotics and effective and cost effective in the end. faecal transplantation, including diagnostics, should draw the attention of the IPC community. The benefits Hand hygiene in the prevention of HAI and AMR need to be more Hand hygiene is the most widely promoted single inter- fully established. Whole genome sequencing is a promis- vention for the prevention of HAI and transmission of ing technology and a powerful tool for future epidemi- MDROs. Direct hand hygiene observation is considered ology in both IPC and AMR. Public health interests are the best method to assess compliance, but, among key on- different from research interests, and using WGS for going challenges with hand hygiene improvement, the public health purposes requires coordinated standards Hawthorne effect limits its validity [8]. There may be bet- and infrastructure. International organisations should ter methods of measurement and feedback than direct work together with national public health bodies, experts hand hygiene observation: there has been an explosion of and researchers of the IPC community to foster outputs Zingg et al. Antimicrobial Resistance and Infection Control (2019) 8:83 Page 4 of 5 of interest for public health such as quality assurance of Eggimann; Petra Gastmeier; M. Lindsay Grayson; Stephan Harbarth; Marcela Hernandez; Loreen Herwaldt; Alison Holmes; John A. Jernigan; Claire Kilpa- WGS, standardised methodologies, and international li- trick; Amy Kolwaite; Karl-Heinz Krause; Elaine Larson; Sarah Masson-Roy; Shah- braries. Antimicrobial surfaces are unlikely to play an een Mehtar; Marc Mendelson; Ling Moi Lin; Andreea Moldovan; Dominique important role in the short term given their expense and Monnet; Babacar Ndoye; Peter Nthumba; Folasade Ogunsola; Ben Park; Eli Perencevich; Didier Pittet; Matthew Samore; Wing Hong Seto; Arjun Sriniva- lack of efficacy data supporting wide adoption. There is san; Julie Storr; Evelina Tacconelli; Carolyn Tarrant; Maha Talaat; Sara Tomczyk; agreement that the evidence for measurable effectiveness Maria Virginia Villegas; Andreas Voss; Tim Walsh; Andreas Widmer; Walter is poor and thus, broad recommendations of antimicro- Zingg. bial surfaces cannot be justified at this time. Hand hy- Funding giene research now needs to be taken to the next level; The 2017 Geneva IPC-Think Tank was supported by the US Centers for Dis- in particular, accurate surveillance, appropriate tech- ease Prevention and Control, and the University of Geneva Hospitals, Switzerland. nique, required amount of handrub, and automatic re- minders for healthcare professionals would be of Availability of data and materials interest. However, given that hand hygiene is and re- Not applicable. mains driven by the behaviour of healthcare profes- US CDC disclaimer sionals, all future aspects taking into account new The findings and conclusions in this report are those of the authors and do technology should be considered within a multimodal not necessarily represent the official position of CDC. improvement strategy. The time available to discuss technology was short, WHO disclaimer The authors alone are responsible for the views expressed in this article and limiting the aim to obtain consensus on a road map for they do not necessarily represent the views, decisions or policies of the all four topics. The role of the microbiota in IPC was a institutions with which they are affiliated. new concept, and except from using probiotics and ap- plying faecal transplantation to treat CDI and to address Authors’ contributions WZ, BP, BA, DC, and DP organised the think tank. All authors contributed to AMR, there was limited time to discuss this concept in a conducting this dimension of the think tank. WZ wrote the first draft of the wider range (e.g. the role of the hospital microbiota). In manuscript. WZ, BP, JS, RA, CT, ECS, EP, AW, KHK, CK, ST, BA, DC, and DP the discussion on WGS, some experts expressed con- reviewed and contributed to subsequent drafts. All authors approved the final version for publication. cerns about this technology being already sufficiently ad- vanced and reproducible to serve as a gold standard. Ethics approval and consent to participate Thus, both microbiota and WGS will be the two topics Not applicable. to be discussed in the next Geneva think tank. Consent for publication Not applicable. Conclusion The four domains of technological innovation contribute Competing interests The authors declare that they have no competing interests. to the prevention of HAI and AMR at different levels. Microbiome research may offer innovative concepts for future prevention, whole genome sequencing could detect Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in new modes of transmission and become an additional tool published maps and institutional affiliations. for effective public health epidemiology, antimicrobial sur- faces might help to decrease the environment as source of Author details Infection control programme and WHO collaborating center, University of transmission but continue to raise more questions than Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle Perret-Gentil, answers, and technological innovation may have a role in 1211, Geneva 14, Switzerland. US Centers for Disease Control and improving surveillance approaches and supporting best Prevention, Atlanta, GA, USA. Infection Prevention and Control Global Unit, World Health Organization, Geneva, Switzerland. National Institute for Health practice in hand hygiene. Research in Healthcare Associated Infection and Antimicrobial Resistance, Imperial College London, London, UK. Department of Health Sciences, Abbreviations University of Leicester, Leicester, UK. Carver College of Medicine, University AMR: Antimicrobial resistance; ARHAI: Antimicrobial Resistance and of Iowa, Iowa City, USA. Infection Control Programme, University Hospitals Healthcare-Associated Infection (−network); CDC: US Centers for Disease of Basel, Basel, Switzerland. Institute of Genetics and Genomics, University of Control and Prevention; CDI: Clostridioides difficile infection; ECDC: European Geneva, Geneva, Switzerland. Centre for Disease Prevention and Control; HAI: Healthcare-associated infection; HUG: University of Geneva Hospitals; IPC: Infection prevention and Received: 14 February 2019 Accepted: 13 May 2019 control; MDRO: Multidrug-resistant organism; WGS: Whole genome sequencing; WHO: World Health Organization Acknowledgments References We would like to thank Tatiana Galperine, Mirko Saam and Derek Christie for 1. Sender R, Fuchs S, Milo R. Are we really vastly outnumbered? Revisiting the taking notes. ratio of bacterial to host cells in humans. Cell. 2016;164:337–40. The 2017 Geneva IPC-Think Tank: Mohamed Abbas; Raheelah Ahmad; 2. Hertz FB, Lobner-Olesen A, Frimodt-Moller N. Antibiotic selection of Benedetta Allegranzi; Antoine Andremont; Mike Bell; Michael Borg; Denise Escherichia coli sequence type 131 in a mouse intestinal colonization Cardo; Yehuda Carmeli; Enrique Castro-Sanchez; John Conly; Philippe model. Antimicrob Agents Chemother. 2014;58:6139–44. Zingg et al. Antimicrobial Resistance and Infection Control (2019) 8:83 Page 5 of 5 3. Manzoni P, Stolfi I, Messner H, Cattani S, Laforgia N, Romeo MG, et al. Bovine lactoferrin prevents invasive fungal infections in very low birth weight infants: a randomized controlled trial. Pediatrics. 2012;129:116–23. 4. He Y, Cao L, Yu J. Prophylactic lactoferrin for preventing late-onset sepsis and necrotizing enterocolitis in preterm infants: a PRISMA-compliant systematic review and meta-analysis. Medicine. 2018;97:e11976. 5. Rubin TA, Gessert CE, Aas J, Bakken JS. Fecal microbiome transplantation for recurrent Clostridium difficile infection: report on a case series. Anaerobe. 2013;19:22–6. 6. Maki DG, Alvarado CJ, Hassemer CA, Zilz MA. Relation of the inanimate hospital environment to endemic nosocomial infection. New Engl J Med. 1982;307:1562–6. 7. Salgado CD, Sepkowitz KA, John JF, Cantey JR, Attaway HH, Freeman KD, et al. Copper surfaces reduce the rate of healthcare-acquired infections in the intensive care unit. Infect Control Hosp Epidemiol. 2013;34:479–86. 8. Yin J, Reisinger HS, Vander Weg M, Schweizer ML, Jesson A, Morgan DJ, et al. Establishing evidence-based criteria for directly observed hand hygiene compliance monitoring programs: a prospective, multicenter cohort study. Infect Control Hosp Epidemiol. 2014;35:1163–8. 9. Armellino D, Hussain E, Schilling ME, Senicola W, Eichorn A, Dlugacz Y, et al. Using high-technology to enforce low-technology safety measures: the use of third-party remote video auditing and real-time feedback in healthcare. Clin Infect Dis. 2012;54:1–7. 10. Marra AR, Moura DF Jr, Paes AT, dos Santos OF, Edmond MB. Measuring rates of hand hygiene adherence in the intensive care setting: a comparative study of direct observation, product usage, and electronic counting devices. Infect Contrl Hosp Epidemiol. 2010;31:796–801. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance & Infection Control Springer Journals

Technology for the prevention of antimicrobial resistance and healthcare-associated infections; 2017 Geneva IPC-Think Tank (Part 2)

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Biomedicine; Medical Microbiology; Drug Resistance; Infectious Diseases
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Abstract

Background: The high burden of healthcare-associated infections (HAIs) and antimicrobial resistance (AMR) is partially due to excessive antimicrobial use both in human and animal medicine worldwide. How can technology help to overcome challenges in infection prevention and control (IPC) and to prevent HAI and emerging AMR? Methods: In June 2017, 42 international experts convened in Geneva, Switzerland to discuss four potential domains of technology in IPC and AMR: 1) role and potential contribution of microbiome research; 2) whole genome sequencing; 3) effectiveness and benefit of antimicrobial environmental surfaces; and 4) future research in hand hygiene. Results: Research on the microbiome could expand understanding of antimicrobial use and also the role of probiotics or even faecal transplantation for therapeutic purposes. Whole genome sequencing will provide new insights in modes of transmission of infectious diseases. Although it is a powerful tool for public health epidemiology, some challenges with interpretation and costs still need to be addressed. The effectiveness and cost-effectiveness of antimicrobially coated or treated environmental high-touch surfaces requires further research before they can be recommended for routine use. Hand hygiene implementation can be advanced, where technological enhancement of surveillance, technique and compliance are coupled with reminders for healthcare professionals. Conclusions: The four domains of technological innovation contribute to the prevention of HAI and AMR at different levels. Microbiome research may offer innovative concepts for future prevention, whole genome sequencing could detect new modes of transmission and become an additional tool for effective public health epidemiology, antimicrobial surfaces might help to decrease the environment as source of transmission but continue to raise more questions than answers, and technological innovation may have a role in improving surveillance approaches and supporting best practice in hand hygiene. Keywords: Technology, Infection prevention and control, Microbiome, Whole genome sequencing, Copper, Hand hygiene, CDC, ECDC, WHO * Correspondence: Walter.Zingg@hcuge.ch Infection control programme and WHO collaborating center, University of Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle Perret-Gentil, 1211, Geneva 14, Switzerland Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zingg et al. Antimicrobial Resistance and Infection Control (2019) 8:83 Page 2 of 5 Background The use of antibiotics interferes with the balance of the A panel of 42 international experts with backgrounds in microbiota, which results in diseases such as Clostridoides infection prevention and control (IPC), microbiology, in- difficile infection (CDI), or can promote the selection of fectious diseases, public health, psychology, medical tech- multidrug-resistance microorganisms (MDROs) [2]. Im- nology, and social sciences, convened for two days at the proved understanding on the impact of antimicrobials on Geneva Think Tank on IPC and antimicrobial resistance the microbiome could improve stewardship efforts. Probio- (AMR) in June 2017 under the auspices of the US Centers tics and faecal transplantation are two examples of micro- for Disease Control and Prevention (CDC), the World biota restoration -related interventions with potential for Health Organization (WHO), and the University of Gen- prevention and treatment [3–5], respectively. Probiotics eva Hospitals and Faculty of Medicine (HUG). The experts can be preventive (e.g. in the prevention of necrotizing en- were from both high- and low-and-middle-income coun- terocolitis in preterm infants) but also have the potential to tries, and from all five continents. The objectives were to be harmful (e.g. in causing probiotic species-related infec- develop a vision on IPC and AMR and to agree on a road tion in immunocompromised patients). IPC professionals map for research and public health activities. Three dimen- may be concerned particularly with the latter, but micro- sions on IPC and AMR were discussed: 1) implementation biota-based intervention as a prevention strategy for AMR of IPC and antimicrobial stewardship; 2) technology in IPC is innovative with beneficial potential. Microbiome research and AMR; and 3) broadening the global IPC network. This can help in directing researchers to ask the right questions is thesecondina series of three2017GenevaIPC-Think on benefits and risks of such interventions, and to design Tank papers; it summarises the discussions about technol- clinical studies with new products. Faecal transplantation ogy in the prevention of healthcare-associated infections is a different way of influencing the microbiota, and (HAIs) and AMR. has been successfully tested to treat recurrent CDI. However, in terms of AMR, additional research is still needed to understand the impact and best uses of Methods this strategy. Four domains of technological innovation for IPC and AMR were assessed: 1) role and potential of microbiome research; 2) potential of whole genome sequencing Whole genome sequencing (WGS); 3) effectiveness and cost-effectiveness of anti- Whole genome sequencing is another rapidly growing microbial surfaces; and 4) future research in hand hy- field of research within IPC and AMR, and reports using giene surveillance and improvement. The domains were this technology are growing in numbers. Organisations selected as a consensus by CDC, WHO, and HUG. Each such as the US CDC and the European Centre for Dis- domain was introduced with a short summary presenta- ease Prevention and Control (ECDC) promote the use of tion by one of the experts, before they were allocated to WGS because of its many strengths such as detailed spe- four focus groups. The discussions were guided by a cies identification, detection of antimicrobial resistance moderator, tape recorded, and documented by writers. at the mechanism level, reproducibility, and objective The experts were invited to express their personal views, comparison of data. For example, in 2018, all Swiss uni- expectations and concerns in relation to using technol- versity hospitals are routinely using this technology to ogy in IPC and AMR. At the end of the four discussion identify clusters and epidemics on a local, national and rounds a plenary session was organised, where abstracts international scale. Combining information on species from the groups were summarized. and antimicrobial resistance using WGS would be a par- ticularly interesting advance in the monitoring of AMR Results on regional, national and international levels. The role of the microbiome This technology is still growing and a number of chal- The populations of microbial species living on or in the lenges need to be addressed. At least today, phenotypic in- human body are known as the microbiota; the micro- formation is needed to inform genotypic interpretation, biome is the total of the genes of the microbiota. While and data interpretation will constantly change over time. the total number of human cells and microbial cells is Although some countries are investing in national data- similar, there are 50 times more bacterial genes than hu- base platforms, there is a lack of valid international refer- man genes in or on a human individual (10 versus 2 × ence platforms. Today, WGS still is a research tool – 10 )[1]. The majority of the microbiota, and of the although advancing rapidly – and as such, many re- microbiome, is found in the intestines. Research on the searchers use their own standards and references for data microbiome as part of our immune system is rapidly interpretation. Epidemiological use of WGS on the other progressing but has not yet emerged into a mature tech- hand would need valid standards and international librar- nology in relation to IPC or AMR. ies, even if the latter grow and change over time. Zingg et al. Antimicrobial Resistance and Infection Control (2019) 8:83 Page 3 of 5 Costs are currently still high, but new, less expensive efforts to incorporate technology into hand hygiene meas- kits are becoming available. However, for low-and-mid- urement. For example, a study using video surveillance dle-income countries, these kits might still be too expen- did highlight some success [9], while surveillance using sive. Whole genome sequencing needs highly trained handrub counters showed effectiveness only after imple- people, particularly for data analysis and interpretation, menting a positive deviance strategy [10]. which adds to the costs of this technology. Open source Non-alcohol-based hand cleansing agents (with spori- software makes interpretation easier and faster than in the cidal activity) were considered to improve compliance and past, and software integrating epidemiology data with act longer (particularly relevant for surgery), but no such those from WGS are getting on the market. product is available for daily routine use at the frontline. The experts perceived automated surveillance positively. Antimicrobial surfaces They decided that more research should be invested there, There is agreement that hospital cleaning is key for pa- with a view to providing more credible data than is cur- tient safety and that materials and design should facili- rently obtained in many settings. The use of new tate cleanliness. Surfaces in hospital environments are un-obtrusive surveillance technologies would be preferable, often contaminated with microorganisms, however, to even at the cost of accuracy. However, is such technology what extent this contamination contributes to MDRO affordable? Compared to the time needed for direct hand transmission is not yet clear [6, 7]. It is known that hygiene observation, automated surveillance might be cleaning practices are inconsistent, and that surfaces cost-effective and would give IPC professionals time to re-contaminate rapidly after cleaning. do other tasks. An emerging question is how new techno- Antimicrobial surfaces are intended to keep bacterial logical innovation could guide healthcare workers to per- loads low, and thus reduce the risk of pathogen trans- form hand hygiene at the right moment. Colour changing mission. The added value of antimicrobial surfaces to a products or electronic reminders were proposed as imagin- clean hospital environment is largely unknown, and able, forward-looking strategies. The ideal hand hygiene other technologies may contribute more to patient agent would have to be fast acting, long-lasting, safety. Ideally, antimicrobial surfaces would not need quick-drying, and skin-friendly with a wide range of effect- maintenance, but exhibit permanent effectiveness. How- iveness (also towards spores and non-enveloped viruses). ever, such a technology is not yet in sight. Copper ap- Longer-lasting agents would be good, but more important pears to be effective in reducing bioburden, but is than duration is effectiveness. In addition to effectiveness, expensive and may even be stolen from hospitals (there other aspects such as price, local production, and ecological is an illegal market for copper in some countries). properties (waste) must be considered for future products. Low-and-middle-income countries do not have the re- Appropriate exposure time, application technique and opti- sources to buy copper or other even more sophisticated mal number and placement of handrub dispensers are add- surfaces. Furthermore, all marketed products today need itional research questions. to be manually cleaned. Thus, cost-effectiveness has been difficult to be demonstrated. A number of ques- Discussion tions (rather than answers) were raised for antimicrobial The IPC community has focussed on best practices for surfaces by the experts: which surfaces in a hospital the prevention of HAI and AMR in recent years, includ- should be coated: high-touch surfaces (used by different ing aspects related to implementation and behaviour people) such as door handles, surfaces in the patient change. However, at the same time new technologies are zone including textiles, toilets and showers, or any sur- being evaluated or are becoming more broadly available. face in a patient room? Could there be resistance to sur- The microbiota has a number of functions in nutrition, face antimicrobials? Maybe, surfaces and equipment that metabolism, and maturation of the immune system, and are carefully designed for easy cleaning would be more thus, research on this topic going beyond probiotics and effective and cost effective in the end. faecal transplantation, including diagnostics, should draw the attention of the IPC community. The benefits Hand hygiene in the prevention of HAI and AMR need to be more Hand hygiene is the most widely promoted single inter- fully established. Whole genome sequencing is a promis- vention for the prevention of HAI and transmission of ing technology and a powerful tool for future epidemi- MDROs. Direct hand hygiene observation is considered ology in both IPC and AMR. Public health interests are the best method to assess compliance, but, among key on- different from research interests, and using WGS for going challenges with hand hygiene improvement, the public health purposes requires coordinated standards Hawthorne effect limits its validity [8]. There may be bet- and infrastructure. International organisations should ter methods of measurement and feedback than direct work together with national public health bodies, experts hand hygiene observation: there has been an explosion of and researchers of the IPC community to foster outputs Zingg et al. Antimicrobial Resistance and Infection Control (2019) 8:83 Page 4 of 5 of interest for public health such as quality assurance of Eggimann; Petra Gastmeier; M. Lindsay Grayson; Stephan Harbarth; Marcela Hernandez; Loreen Herwaldt; Alison Holmes; John A. Jernigan; Claire Kilpa- WGS, standardised methodologies, and international li- trick; Amy Kolwaite; Karl-Heinz Krause; Elaine Larson; Sarah Masson-Roy; Shah- braries. Antimicrobial surfaces are unlikely to play an een Mehtar; Marc Mendelson; Ling Moi Lin; Andreea Moldovan; Dominique important role in the short term given their expense and Monnet; Babacar Ndoye; Peter Nthumba; Folasade Ogunsola; Ben Park; Eli Perencevich; Didier Pittet; Matthew Samore; Wing Hong Seto; Arjun Sriniva- lack of efficacy data supporting wide adoption. There is san; Julie Storr; Evelina Tacconelli; Carolyn Tarrant; Maha Talaat; Sara Tomczyk; agreement that the evidence for measurable effectiveness Maria Virginia Villegas; Andreas Voss; Tim Walsh; Andreas Widmer; Walter is poor and thus, broad recommendations of antimicro- Zingg. bial surfaces cannot be justified at this time. Hand hy- Funding giene research now needs to be taken to the next level; The 2017 Geneva IPC-Think Tank was supported by the US Centers for Dis- in particular, accurate surveillance, appropriate tech- ease Prevention and Control, and the University of Geneva Hospitals, Switzerland. nique, required amount of handrub, and automatic re- minders for healthcare professionals would be of Availability of data and materials interest. However, given that hand hygiene is and re- Not applicable. mains driven by the behaviour of healthcare profes- US CDC disclaimer sionals, all future aspects taking into account new The findings and conclusions in this report are those of the authors and do technology should be considered within a multimodal not necessarily represent the official position of CDC. improvement strategy. The time available to discuss technology was short, WHO disclaimer The authors alone are responsible for the views expressed in this article and limiting the aim to obtain consensus on a road map for they do not necessarily represent the views, decisions or policies of the all four topics. The role of the microbiota in IPC was a institutions with which they are affiliated. new concept, and except from using probiotics and ap- plying faecal transplantation to treat CDI and to address Authors’ contributions WZ, BP, BA, DC, and DP organised the think tank. All authors contributed to AMR, there was limited time to discuss this concept in a conducting this dimension of the think tank. WZ wrote the first draft of the wider range (e.g. the role of the hospital microbiota). In manuscript. WZ, BP, JS, RA, CT, ECS, EP, AW, KHK, CK, ST, BA, DC, and DP the discussion on WGS, some experts expressed con- reviewed and contributed to subsequent drafts. All authors approved the final version for publication. cerns about this technology being already sufficiently ad- vanced and reproducible to serve as a gold standard. Ethics approval and consent to participate Thus, both microbiota and WGS will be the two topics Not applicable. to be discussed in the next Geneva think tank. Consent for publication Not applicable. Conclusion The four domains of technological innovation contribute Competing interests The authors declare that they have no competing interests. to the prevention of HAI and AMR at different levels. Microbiome research may offer innovative concepts for future prevention, whole genome sequencing could detect Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in new modes of transmission and become an additional tool published maps and institutional affiliations. for effective public health epidemiology, antimicrobial sur- faces might help to decrease the environment as source of Author details Infection control programme and WHO collaborating center, University of transmission but continue to raise more questions than Geneva Hospitals and Faculty of Medicine, 4 Rue Gabrielle Perret-Gentil, answers, and technological innovation may have a role in 1211, Geneva 14, Switzerland. US Centers for Disease Control and improving surveillance approaches and supporting best Prevention, Atlanta, GA, USA. Infection Prevention and Control Global Unit, World Health Organization, Geneva, Switzerland. National Institute for Health practice in hand hygiene. Research in Healthcare Associated Infection and Antimicrobial Resistance, Imperial College London, London, UK. Department of Health Sciences, Abbreviations University of Leicester, Leicester, UK. Carver College of Medicine, University AMR: Antimicrobial resistance; ARHAI: Antimicrobial Resistance and of Iowa, Iowa City, USA. Infection Control Programme, University Hospitals Healthcare-Associated Infection (−network); CDC: US Centers for Disease of Basel, Basel, Switzerland. Institute of Genetics and Genomics, University of Control and Prevention; CDI: Clostridioides difficile infection; ECDC: European Geneva, Geneva, Switzerland. Centre for Disease Prevention and Control; HAI: Healthcare-associated infection; HUG: University of Geneva Hospitals; IPC: Infection prevention and Received: 14 February 2019 Accepted: 13 May 2019 control; MDRO: Multidrug-resistant organism; WGS: Whole genome sequencing; WHO: World Health Organization Acknowledgments References We would like to thank Tatiana Galperine, Mirko Saam and Derek Christie for 1. Sender R, Fuchs S, Milo R. Are we really vastly outnumbered? Revisiting the taking notes. ratio of bacterial to host cells in humans. Cell. 2016;164:337–40. The 2017 Geneva IPC-Think Tank: Mohamed Abbas; Raheelah Ahmad; 2. Hertz FB, Lobner-Olesen A, Frimodt-Moller N. Antibiotic selection of Benedetta Allegranzi; Antoine Andremont; Mike Bell; Michael Borg; Denise Escherichia coli sequence type 131 in a mouse intestinal colonization Cardo; Yehuda Carmeli; Enrique Castro-Sanchez; John Conly; Philippe model. Antimicrob Agents Chemother. 2014;58:6139–44. Zingg et al. Antimicrobial Resistance and Infection Control (2019) 8:83 Page 5 of 5 3. Manzoni P, Stolfi I, Messner H, Cattani S, Laforgia N, Romeo MG, et al. Bovine lactoferrin prevents invasive fungal infections in very low birth weight infants: a randomized controlled trial. Pediatrics. 2012;129:116–23. 4. He Y, Cao L, Yu J. Prophylactic lactoferrin for preventing late-onset sepsis and necrotizing enterocolitis in preterm infants: a PRISMA-compliant systematic review and meta-analysis. Medicine. 2018;97:e11976. 5. Rubin TA, Gessert CE, Aas J, Bakken JS. Fecal microbiome transplantation for recurrent Clostridium difficile infection: report on a case series. Anaerobe. 2013;19:22–6. 6. Maki DG, Alvarado CJ, Hassemer CA, Zilz MA. Relation of the inanimate hospital environment to endemic nosocomial infection. New Engl J Med. 1982;307:1562–6. 7. Salgado CD, Sepkowitz KA, John JF, Cantey JR, Attaway HH, Freeman KD, et al. Copper surfaces reduce the rate of healthcare-acquired infections in the intensive care unit. Infect Control Hosp Epidemiol. 2013;34:479–86. 8. Yin J, Reisinger HS, Vander Weg M, Schweizer ML, Jesson A, Morgan DJ, et al. Establishing evidence-based criteria for directly observed hand hygiene compliance monitoring programs: a prospective, multicenter cohort study. Infect Control Hosp Epidemiol. 2014;35:1163–8. 9. Armellino D, Hussain E, Schilling ME, Senicola W, Eichorn A, Dlugacz Y, et al. Using high-technology to enforce low-technology safety measures: the use of third-party remote video auditing and real-time feedback in healthcare. Clin Infect Dis. 2012;54:1–7. 10. Marra AR, Moura DF Jr, Paes AT, dos Santos OF, Edmond MB. Measuring rates of hand hygiene adherence in the intensive care setting: a comparative study of direct observation, product usage, and electronic counting devices. Infect Contrl Hosp Epidemiol. 2010;31:796–801.

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Published: May 22, 2019

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