One Health in hospitals: how understanding the dynamics of people, animals, and the hospital built-environment can be used to better inform interventions for antimicrobial-resistant gram-positive infections

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Abstract

Despite improvements in hospital infection prevention and control, healthcare associated infections (HAIs) remain a challenge with significant patient morbidity, mortality, and cost for the healthcare system. In this review, we use a One Health framework (human, animal, and environmental health) to explain the epidemiology, demonstrate key knowledge gaps in infection prevention policy, and explore improvements to control Gram-positive pathogens in the healthcare environment. We discuss patient and healthcare worker interactions with the hospital environment that can lead to transmission of the most common Gram-positive hospital pathogens – methicillin-resistant Staphylococcus aureus, Clostridioides ( Clostridium) difficile, and vancomycin-resistant Enterococcus – and detail interventions that target these two One Health domains. We discuss the role of animals in the healthcare settings, knowledge gaps regarding their role in pathogen transmission, and the absence of infection risk mitigation strategies targeting animals. We advocate for novel infection prevention and control programs, founded on the pillars of One Health, to reduce Gram-positive hospital-associated pathogen transmission.

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Most cited references 131

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Invasive methicillin-resistant Staphylococcus aureus infections in the United States.

R. Monina Klevens, Melissa Morrison, Joelle Nadle … (2007)

As the epidemiology of infections with methicillin-resistant Staphylococcus aureus (MRSA) changes, accurate information on the scope and magnitude of MRSA infections in the US population is needed. To describe the incidence and distribution of invasive MRSA disease in 9 US communities and to estimate the burden of invasive MRSA infections in the United States in 2005. Active, population-based surveillance for invasive MRSA in 9 sites participating in the Active Bacterial Core surveillance (ABCs)/Emerging Infections Program Network from July 2004 through December 2005. Reports of MRSA were investigated and classified as either health care-associated (either hospital-onset or community-onset) or community-associated (patients without established health care risk factors for MRSA). Incidence rates and estimated number of invasive MRSA infections and in-hospital deaths among patients with MRSA in the United States in 2005; interval estimates of incidence excluding 1 site that appeared to be an outlier with the highest incidence; molecular characterization of infecting strains. There were 8987 observed cases of invasive MRSA reported during the surveillance period. Most MRSA infections were health care-associated: 5250 (58.4%) were community-onset infections, 2389 (26.6%) were hospital-onset infections; 1234 (13.7%) were community-associated infections, and 114 (1.3%) could not be classified. In 2005, the standardized incidence rate of invasive MRSA was 31.8 per 100,000 (interval estimate, 24.4-35.2). Incidence rates were highest among persons 65 years and older (127.7 per 100,000; interval estimate, 92.6-156.9), blacks (66.5 per 100,000; interval estimate, 43.5-63.1), and males (37.5 per 100,000; interval estimate, 26.8-39.5). There were 1598 in-hospital deaths among patients with MRSA infection during the surveillance period. In 2005, the standardized mortality rate was 6.3 per 100,000 (interval estimate, 3.3-7.5). Molecular testing identified strains historically associated with community-associated disease outbreaks recovered from cultures in both hospital-onset and community-onset health care-associated infections in all surveillance areas. Invasive MRSA infection affects certain populations disproportionately. It is a major public health problem primarily related to health care but no longer confined to intensive care units, acute care hospitals, or any health care institution.

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Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic.

Michael David, Robert S Daum (2010)

Staphylococcus aureus is an important cause of skin and soft-tissue infections (SSTIs), endovascular infections, pneumonia, septic arthritis, endocarditis, osteomyelitis, foreign-body infections, and sepsis. Methicillin-resistant S. aureus (MRSA) isolates were once confined largely to hospitals, other health care environments, and patients frequenting these facilities. Since the mid-1990s, however, there has been an explosion in the number of MRSA infections reported in populations lacking risk factors for exposure to the health care system. This increase in the incidence of MRSA infection has been associated with the recognition of new MRSA clones known as community-associated MRSA (CA-MRSA). CA-MRSA strains differ from the older, health care-associated MRSA strains; they infect a different group of patients, they cause different clinical syndromes, they differ in antimicrobial susceptibility patterns, they spread rapidly among healthy people in the community, and they frequently cause infections in health care environments as well. This review details what is known about the epidemiology of CA-MRSA strains and the clinical spectrum of infectious syndromes associated with them that ranges from a commensal state to severe, overwhelming infection. It also addresses the therapy of these infections and strategies for their prevention.

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Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research

Nicholas A Turner, Batu Sharma-Kuinkel, Stacey A Maskarinec … (2019)

Methicillin-resistant Staphylococcus aureus (MRSA) is one of the most successful modern pathogens. The same organism that lives as a commensal and is transmitted in both health-care and community settings is also a leading cause of bacteraemia, endocarditis, skin and soft tissue infections, bone and joint infections and hospital-acquired infections. Genetically diverse, the epidemiology of MRSA is primarily characterized by the serial emergence of epidemic strains. Although its incidence has recently declined in some regions, MRSA still poses a formidable clinical threat, with persistently high morbidity and mortality. Successful treatment remains challenging and requires the evaluation of both novel antimicrobials and adjunctive aspects of care, such as infectious disease consultation, echocardiography and source control. In this Review, we provide an overview of basic and clinical MRSA research and summarize the expansive body of literature on the epidemiology, transmission, genetic diversity, evolution, surveillance and treatment of MRSA.

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Author and article information

Contributors

Kathryn R. Dalton:

ORCID: http://orcid.org/0000-0002-0105-7098

Kdalton4@jhu.edu

Clare Rock: Clare.Rock@jhmi.edu

Karen C. Carroll: kcarrol7@jhmi.edu

Meghan F. Davis: mdavis65@jhu.edu

Journal

Journal ID (nlm-ta): Antimicrob Resist Infect Control

Journal ID (iso-abbrev): Antimicrob Resist Infect Control

Title: Antimicrobial Resistance and Infection Control

Publisher: BioMed Central (London )

ISSN (Electronic): 2047-2994

Publication date (Electronic): 1 June 2020

Publication date PMC-release: 1 June 2020

Publication date Collection: 2020

Volume: 9

Electronic Location Identifier: 78

Affiliations

[1 ]GRID grid.21107.35, ISNI 0000 0001 2171 9311, Department of Environmental Health and Engineering, , Johns Hopkins Bloomberg School of Public Health, ; 615 N Wolfe St, W7034G JHSPH EHE, Baltimore, MD 21205 USA

[2 ]GRID grid.21107.35, ISNI 0000 0001 2171 9311, Division of Medical Microbiology, Department of Pathology, , Johns Hopkins University School of Medicine, ; Baltimore, MD USA

[3 ]GRID grid.21107.35, ISNI 0000 0001 2171 9311, Department of Molecular and Comparative Pathobiology, , Johns Hopkins University School of Medicine, ; Baltimore, MD USA

Author information

Kathryn R. Dalton http://orcid.org/0000-0002-0105-7098

Article

Publisher ID: 737

DOI: 10.1186/s13756-020-00737-2

PMC ID: 7268532

PubMed ID: 32487220

SO-VID: d1045c44-090c-4336-81d6-ad748e54be90

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Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.

History

Date received : 11 September 2019

Date accepted : 11 May 2020

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000125, National Institute for Occupational Safety and Health;

Award ID: T42 OH0008428

Award Recipient : Kathryn R. Dalton

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ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: infection prevention,infection control,hospital-associated infections,hospital environment,hai interventions,one health

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ScienceOpen disciplines: Infectious disease & Microbiology

Keywords: infection prevention, infection control, hospital-associated infections, hospital environment, hai interventions, one health

One Health in hospitals: how understanding the dynamics of people, animals, and the hospital built-environment can be used to better inform interventions for antimicrobial-resistant gram-positive infections

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JAMA Network: Coronavirus

Most cited references 131

Invasive methicillin-resistant Staphylococcus aureus infections in the United States.

Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic.

Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research

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