Healthcare-associated infections in adult intensive care unit patients: Changes in epidemiology, diagnosis, prevention and contributions of new technologies

Stijn Blot, Etienne Ruppé, Stephan Harbarth, Karim Asehnoune, Garyphalia Poulakou, Charles-Edouard Luyt, Jordi Rello, Michael Klompas, Pieter Depuydt, Christian Eckmann, Ignacio Martin-Loeches, Pedro Povoa, Lila Bouadma, Jean-Francois Timsit, Jean-Ralph Zahar, Stijn Blot, Etienne Ruppé, Stephan Harbarth, Karim Asehnoune, Garyphalia Poulakou, Charles-Edouard Luyt, Jordi Rello, Michael Klompas, Pieter Depuydt, Christian Eckmann, Ignacio Martin-Loeches, Pedro Povoa, Lila Bouadma, Jean-Francois Timsit, Jean-Ralph Zahar

Abstract

Patients in intensive care units (ICUs) are at high risk for healthcare-acquired infections (HAI) due to the high prevalence of invasive procedures and devices, induced immunosuppression, comorbidity, frailty and increased age. Over the past decade we have seen a successful reduction in the incidence of HAI related to invasive procedures and devices. However, the rate of ICU-acquired infections remains high. Within this context, the ongoing emergence of new pathogens, further complicates treatment and threatens patient outcomes. Additionally, the SARS-CoV-2 (COVID-19) pandemic highlighted the challenge that an emerging pathogen provides in adapting prevention measures regarding both the risk of exposure to caregivers and the need to maintain quality of care. ICU nurses hold a special place in the prevention and management of HAI as they are involved in basic hygienic care, steering and implementing quality improvement initiatives, correct microbiological sampling, and aspects antibiotic stewardship. The emergence of more sensitive microbiological techniques and our increased knowledge about interactions between critically ill patients and their microbiota are leading us to rethink how we define HAIs and best strategies to diagnose, treat and prevent these infections in the ICU. This multidisciplinary expert review, focused on the ICU setting, will summarise the recent epidemiology of ICU-HAI, discuss the place of modern microbiological techniques in their diagnosis, review operational and epidemiological definitions and redefine the place of several controversial preventive measures including antimicrobial-impregnated medical devices, chlorhexidine-impregnated washcloths, catheter dressings and chlorhexidine-based mouthwashes. Finally, general guidance is suggested that may reduce HAI incidence and especially outbreaks in ICUs.

Keywords: Bloodstream infection; Catheter-related infections; Critically ill; Hospital-acquired infection; Infection prevention and control; Intensive care; Multidrug resistance; Pneumonia; Sepsis; Urinary tract infections.

Conflict of interest statement

JFT declares research grants from Pfizer, Merck, 3M, Astellas, Biomerieux; scientific Board participation with Merck, Bayer pharma, Gilead; lecture fees for Merck, Pfizer, Biomerieux. GP declares Speaker’s Honoraria by Merck, Angellini, Biorad, Pfizer; research grants by Merck, Pfizer, Roche. CE declares scientific board participation and lecture fees for Correvio, Menarini, Merck and Pfizer. PD received fees from Belgian Health Care Knowledge Centre. SH declares SAB fees from Sandoz. SB declares conflict of interest with Pfizer, Halyard and 3M.CEL declares research grants from Bayer Healthcare and Maquet; scientific board participation with Bayer Healthcare, ThermoFischer Brahms, Carmat, Faron; lecture fees from Merck, Biomérieux. JR declares consultancy and speakers bureau fees for Pfizer and Nebriva. MK declares receiving research grants from the US Centers for Disease Control and Prevention and royalties from UpToDate Inc. CE declares scientific board participation and lecture fees for Correvio, Menarini, Merck and Pfizer. IML declares lecture fees from accelerate, MSD and Gilead. PP declares lectures fees from Pfizer and Orion. JRZ declares research grants from Pfizer, Merck; scientific Board participation with Merck, BioMerieux, Eumedica, Pfizer; lecture fees for Merck, Pfizer, Correvio, Gilead. No other conflicts of interests to declare.

Copyright © 2022 Elsevier Ltd. All rights reserved.

Figures

Fig. 1
Fig. 1
Prevalence of ICU-acquired infections, 2000–2018 (European Centre for Disease Prevention and Control, 2018, Ponce de León-Rosales et al., 2000, Rosenthal et al., 2003, Ortíz et al., 2014, Murni et al., 2015, Iwuafor et al., 2016, Mitharwal et al., 2016, Phu et al., 2016, Taylor et al., 2016, Yakovlev et al., 2016, Yallew et al., 2016, Chiang et al., 2018, Braga et al., 2019).
Fig. 2
Fig. 2
Rates of ventilator-associated pneumonia per 1000 days of intubation and ICU-central line-associated bloodstream infections per 1000 catheter days, respectively (2000–2018) (Public Health Agency of Canada, 2014, Lobo et al., 2005, Moreno et al., 2006, Rosenthal et al., 2006, Hajdu et al., 2007, Leblebicioglu et al., 2007, Mehta et al., 2007, Arabi et al., 2008, Korbkitjaroen et al., 2011, Navoa-Ng et al., 2011, Ramirez et al., 2011, Son et al., 2012, Charles et al., 2013, Dudeck et al., 2013, Medell et al., 2013, Leblebicioglu et al., 2013a, Leblebicioglu et al., 2013b, Ndegwa et al., 2014, Behari and Kalafatis, 2015, Dasgupta et al., 2015, Elliott et al., 2015, Entesari-Tatafi et al., 2015, Singh et al., 2015, Malek et al., 2018).
Fig. 3
Fig. 3
A reappraisal of the immunological effects of ICU acquired immunosuppression on respiratory defenses against pathogens. Normal response of Dendritic cell during primary pneumonia (left panel), and after immunosuppression-induced pneumonia (middle and right panel). The stimulation of dendritic cells activated by pathogen-associated molecular patterns (Act DCs) induces the production of inflammatory cytokines (such as Interleukin-12) which stimulate NK cells (innate-like lymphocyte) and prime naive CD4 T cells to fight against bacteria. During sepsis-induced immunosuppression (middle and right panels), bacterial clearance is decreased as compared to what is observed during “normal response” to pneumonia. (middle) Early after the first hit (sepsis, severe trauma) causing ICU-acquired immunosuppression, DCs are paralyzed (Par DC) and unable to respond to subsequent pathogens. Par DC also fail to produce cytokines and to prime new CD4 T cells or NK cells. (right) Lately, newly formed DCs locally acquire a tolerogenic phenotype (Tol. DCs). Upon stimulation by pathogens, Tol-DCs do not activate NK cells but induce the local accumulation of Treg cells that maintain an immunosuppressive milieu.
Fig. 4
Fig. 4
Immune response alterations in cancer patients (European Centre for Disease Prevention and Control, 2018, Smith et al., 2015, Taplitz et al., 2018).
Fig. 5
Fig. 5
Illustration of the role of the laboratory in the management of hospital-acquired pneumonia.
Fig. 6
Fig. 6
Global rules for hospital-acquired infection prevention programs in the ICU. HAI, hospital-acquired infection. MDR, multidrug resistance. HCWs, healthcare workers. Education awareness: must target all healthcare workers, including support staff (e.g. logistics, cleaning). Infection preventionists and nurse-practitioners can bridge communication between various stakeholders and fine-tune educational materials to target specific groups. Multimodal strategies: (1) reducing exposure and duration of invasive procedures, the need for invasive procedures must be evaluated on a daily basis. (2) Development and application of multimodal evidence-based prevention measures. Implementation within a care bundle or checklist is positively associated with adherence. Implementation process: During the implementation period, infection preventionists and/or nurse-practitioners must provide continual bedside education and support, and trigger a culture of accountability. Determinants and prevention measures for HAIs as well as outcomes need to be monitored with close feedback to unit leaders and bedside personnel to fuel constant quality improvement. These include reports on compliance with recommendations (adherence rates) and correlation with HAI rates (outcomes). Feedback is crucial to fine-tune prevention programs and to optimize the motivation of stakeholders.
Fig. 7
Fig. 7
Individual benefits and collective risks of active prevention measures in ICU-hospital-acquired infections. Rational use active antiseptic/antibiotic compounds for preventing nosocomial infections. Right upper quadrant: Prerequisites: prevention and control of multidrug resistant organisms (MDRO) spread, hand hygiene, and surveillance of nosocomial infections are prerequisites. If unobserved, any attempts in implementing prevention strategies using antiseptics or antibiotics will be futile. Right lower quadrant: To consider in high risk patients or when the risk of infection remains high despite the implementation of the prerequisites. Left upper quadrant: To consider when the prevalence of MDRO is low or if the evidence of spread of infections caused by MDRO is low. Left lower quadrant: Not to consider until further available data.

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