Transmission of health care-associated infections from roommates and prior room occupants: a systematic review

Introduction

Despite decades of infection prevention research and quality improvement initiatives, health care-associated infections (HAIs) remain common adverse events in hospitals and long-term care facilities.¹ Over 700,000 HAIs occur annually in the USA alone, leading to death in 6% of cases and costing the health care system 28–45 billion US dollars each year.^2–4 Recently, there has been renewed interest in understanding the role of the physical environment in the spread of HAIs.^5,6 Countless studies have reported that pathogenic organisms can survive on a variety of fomites in health care settings, including those at the patient bedside (eg, mattresses, linens, pillows, bedframes, bedrails), inside patient bathrooms (eg, toilets, floors, soap dispensers), and on medical instruments (eg, blood pressure cuffs, suctioning systems).^7–14 Moreover, the effectiveness of cleaning regimens has been called into question as a number of studies have reported that pathogens remain on hospital surfaces even after they have been disinfected in accordance with recommended protocols.^15–18 Pathogens that survive on fomites can subsequently be transferred from contaminated surfaces to patients through direct contact, indirect contact through the hands and gloves of health care workers, or by aerosolization of surface particles.^8,11,19–21

Patients hospitalized with infections frequently contaminate their surrounding environments with pathogenic organisms; therefore, roommates and previous room occupants may serve as potential sources of exposure to other patients.^8,22 Yet, our understanding of how such exposures contribute to a patient’s overall risk of infection remains limited, and the effects of these exposures may be dependent on a variety of factors unique to each organism species, such as their robustness to atmospheric conditions, susceptibility to cleaning agents, and virulence. Therefore, the aim of this study was to systematically review the literature describing organism transmission from concurrent roommates or previous room occupants in health care settings.

Methods

Inclusion criteria

This systematic literature review was performed in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines.²³ Studies were included if they met the following criteria: 1) compared infection and/or colonization rates between patients known to be exposed to infectious roommates and/or prior room occupants and patients not known to be exposed, 2) were conducted in an acute or long-term health care setting, 3) were original research studies, 4) were published in English, and 5) were published from January 1, 1990 through December 31, 2014.

Search strategy

The literature search was conducted in February 2015 to ensure that all manuscripts published within the inclusion period had been indexed. All databases indexed within PubMed were searched using the following combination of keywords and Medical Subject Heading (MeSH) search terms linked with Boolean operators: ([MeSH {Patients’ Rooms}] AND [MeSH {Infection Control Practitioners} OR MeSH {Infection Control} OR MeSH {Cross Infection} OR MeSH {Infection} OR MeSH {Wound Infection} OR MeSH {Surgical Wound Infection} OR Keyword {Infection}]) OR (Keyword [Prior Room Occupant*]) OR (Keyword [Roommate] AND Keyword [Transmission] OR Keyword [Infection*] OR Keyword [Outbreak*]).

Article selection, review, and quality scoring

Three reviewers (BC, CCC, and BL) independently assessed each article at all stages of the review and quality scoring processes. Discrepancies among reviewers were discussed as a group until a consensus was reached. First, the reviewers screened the titles and abstracts of all articles and eliminated those that were not relevant to the aims of the review. The remaining articles underwent full-text review to determine whether they met the inclusion criteria. A hand search of the references of all articles meeting the inclusion criteria was also performed. Articles meeting the inclusion criteria were scored according to a modified 20-item version of the Checklist for Measuring Study Quality developed by Downs and Black (Table 1).²⁴ Some measures were not applicable to all articles; these items were removed from the score denominator and not assessed for studies in which they were not relevant. Final scores were converted to percentages.

Table 1 Assessment of study quality Note: aData collection tool from Downs and Black.24

Results

The database search returned 330 articles. No additional articles were identified from the hand search and no duplicates were found. Twenty articles were excluded during the title screening phase, and 223 articles were excluded during the abstract screening phase. The remaining 87 articles underwent full-text review, and 18 of these were determined to meet the inclusion criteria. Figure 1 describes the reasons for exclusion during the full-text review. Ten articles investigated the effects of exposure to infected or colonized roommates,^25–34 six investigated the effects of exposure to infected or colonized prior room occupants,^35–40 and two investigated both exposures.^41,42

Figure 1 Identification, screening, eligibility, and inclusion of articles according to the PRISMA guidelines. Notes: Three hundred and thirty articles were identified by database search and no additional records were identified from other sources. No duplicates were identified. Abbreviation: PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses.

Study designs and definitions of exposures and outcomes

The articles in this review represent a range of observational and interventional designs, including retrospective and prospective cohort studies (n=11),^{26,28–32,35,38–40,42} case–control studies (n=4),^25,27,33,34 and quasi-experimental studies (n=3).^36,37,41 The studies varied considerably in their definitions of exposure and outcome measures. Among studies that examined exposure to roommates with nonviral pathogens, four (44%) defined the exposure as having a roommate with a clinical infection^25–27,42 and five (56%) defined the exposure as having a roommate who was either infected or colonized.^31–34,41 Among studies that examined exposure to previous room occupants, there was variation both in the determination of whether a previous occupant was infectious and in the timeframe during which they occupied the room. Four studies (50%) defined the exposure as a previous occupant who was infected or colonized,^35,38,39,41 two studies (25%) – both of Clostridium difficile – defined the exposure as a previous occupant with a history of infection,^40,41 and two studies (25%) did not specify.^36,37

With regard to timing of the exposure, most of the studies implied that only the occupant immediately prior to the study subject was included, although only three articles stated this explicitly.^35,37,40 One study also analyzed exposure to any infectious patient who had occupied the same room within the previous 2-week period.³⁷ Finally, there was notable variation in the definition of study outcomes. Half of the articles used an outcome measure of infection,^{25–30,32,40,42} while the other half used an outcome measure of infection or colonization.^{31,33–39,41} Methods of case detection ranged from universal screening to sampling based on clinical indication.

Findings of studies examining exposure to infected or colonized roommates

The 12 articles investigating the effects of exposure to infected or colonized roommates are described in Table 2 and their findings are summarized in Figure 2. Five studies evaluated bacterial pathogens that are transmitted by contact.^{31,33,34,41,42} No significant associations between roommate exposure and infection with methicillin-resistant Staphylococcus aureus (MRSA), C. difficile, or Pseudomonas cepacia were identified.^31,33,42 Results for vancomycin-resistant enterococci (VRE) were inconsistent, with Bass et al⁴¹ reporting a statistically significant positive association (hazard ratio [HR]: 18.8, 95% confidence interval: [5.4–66.2]) and Shorman and Al-Tawfiq³⁴ reporting a statistically significant negative association (odds ratio [OR]: 0.04 [0.004–0.4]).

Table 2 Summary and quality assessment of studies reporting associations between health care-associated infection and exposure to infected or colonized roommates Abbreviations: BMI, body mass index; CF, cystic fibrosis; CHF, congestive heart failure; GAS, group A streptococcus; HCV, hepatitis C virus; HIV, human immunodeficiency virus; HR, hazard ratio; LOS, length of stay; MRSA, methicillin-resistant Staphylococcus aureus; neg, negative; OR, odds ratio; pos, positive; P. cepacia, Pseudomonas cepacia; pts, patients; PVD, peripheral vascular disease; RR, relative risk; VRE, vancomycin-resistant enterococci; w/, with; w/o, without.

Figure 2 Findings of studies investigating the association between health care-associated infection or colonization and exposure to infected or colonized roommates. Notes: Studies reporting significant positive associations are represented in black circles and those reporting significant negative associations are represented in white circles. Studies that did not find statistically significant associations are represented in gray circles. Circles display study authors, setting, investigation of endemic versus epidemic pathogen, and quality score.

Three studies conducted in long-term care settings examined group A streptococcus, which is transmitted by contact and droplet routes.^25,27,32 All three found significant positive associations between roommate exposure and infection, with ORs ranging from 2.0 (1.1–5.1) to 15.3 (2.5–110.9; point estimate not reported by Auerbach et al²⁵).

Three studies examined exposure to roommates infected with viral pathogens.^28–30 Two studies of influenza conducted within the same long-term care facility found significantly elevated risks of infection among those with infected roommates (relative risk: 3.1 [1.6–5.8] for influenza A and relative risk: 2.6 [1.2–5.6] for influenza B).^28,29 One study evaluated transmission of hepatitis C, a viral bloodborne pathogen, in a liver transplant ward of an acute care hospital and found significantly increased odds of infection after sharing a room with an infected patient (OR: 12.0 [1.4–103.0]).³⁰ One parasitic pathogen spread by fecal–oral contact, Cryptosporidium parvum, was evaluated in an acute care human immunodeficiency virus ward and no association was found.²⁶

Findings of studies examining exposure to rooms previously occupied by infected or colonized patients

The eight articles investigating the effects of exposure to rooms previously occupied by infected or colonized patients are described in Table 3 and their findings are summarized in Figure 3. All of the articles studied bacterial pathogens spread through contact transmission in acute care hospitals, with all but two^41,42 taking place in intensive care units. Nseir et al³⁹ found that exposure to rooms previously occupied by patients with Acinetobacter baumannii and Pseudomonas aeruginosa resulted in significantly higher odds of infection or colonization (OR: 4.2 [2.0–8.8] and OR: 2.3 [1.2–4.3], respectively), while the two studies that examined extended-spectrum beta-lactamase-producing gram-negative organisms found no association.^35,39 Effects of exposure to rooms previously occupied by patients with C. difficile, MRSA, and VRE were examined by at least two studies each. For each of these organisms, significant positive associations were reported by one article (C. difficile, HR: 2.4 [1.2–4.5];⁴⁰ MRSA, OR: 1.4 [p=0.04];³⁶ VRE, HR: 3.8 [2.0–7.4]³⁷), with the remainder of articles finding no significant associations.^38,41,42

Table 3 Summary and quality assessment of studies reporting associations between health care-associated infection and exposure to infected or colonized prior room occupants Abbreviations: APACHE II, acute physiology and chronic health evaluation II; ESBL, extended-spectrum beta-lactamase–producing organism; GLM, generalized linear mixed model; GNB, Gram-negative bacteria; HR, hazard ratio; ICU, intensive care unit; LOD, logistic organ dysfunction score; LOS, length of stay; MDR, multidrug resistant; MRSA, methicillin-resistant Staphylococcus aureus; neg, negative; OR, odds ratio; pts, patients; pos, positive; RR, relative risk; SAPS II, simplified acute physiology score II; VRE, vancomycin-resistant enterococci; w/, with; w/o, without.

Figure 3 Findings of studies investigating the association between health care-associated infection or colonization and exposure to infected or colonized prior room occupants. Notes: Studies reporting significant positive associations are represented in black circles. Studies that did not find statistically significant associations are represented in gray circles. No studies reported a significant negative association. Circles display study authors, setting, investigation of endemic versus epidemic pathogen, and quality score.

Quality of included articles

Quality scores ranged from 50% to 95%, with the majority of articles scoring at or above 80% (median=83%, mean=82%). Table 1 provides a summary of scores for each item. All of the articles had clearly stated aims, adequate descriptions of study populations, appropriate control groups, and acceptable reporting of results. However, many of the studies did not appropriately control for confounding (50%, n=9), address differential follow-up between exposed and unexposed patients (33%, n=6), or use acceptable statistical methods (17%, n=3). In addition, some articles did not include sufficient or precise definitions of the exposures (17%, n=3) or outcomes (6%, n=1) under investigation. Notably, none of the articles reported a sample size calculation indicating adequate power to detect differences between patients exposed versus unexposed to infected/colonized roommates or prior room occupants.

Discussion

More than half of the articles identified in this systematic literature review reported at least one statistically significant positive association between the infection/colonization status of a roommate or previous room occupant and the development of HAIs.^{25,27–30,32,36,37,39–41} Only a single article identified a statistically significant negative association.³⁴ The remainder found no associations that reached statistical significance, though this may be due to the fact that they were insufficiently powered; none of the articles reviewed included a statement indicating that statistical power was adequate for the analyses presented. Another factor that may have contributed to findings of no association is that many studies included patients who were either infected or colonized as potential sources of exposure. Patients with symptomatic infections may shed greater amounts of infectious body fluids to surrounding fomites, compared with patients who are asymptomatically colonized.⁴³ Therefore, if a causal association does indeed exist, including both infected and colonized patients as potential sources of exposure may have driven findings toward the null, since exposure to colonized roommates and prior room occupants could present less risk to patients. Heterogeneity of the exposure may have also arisen from variation in the infection or colonization site of a roommate or prior room occupant. In a study of patients with MRSA, environmental contamination was more prevalent on fomites surrounding patients with positive wound or urine cultures, compared with patients who had positive blood or sputum cultures.⁸

The studies we reviewed revealed consistent findings for some pathogens (influenza, group A streptococcus) and inconsistent findings for others (VRE, MRSA, C. difficile). For endemic health care pathogens such as VRE, MRSA, and C. difficile, it may be difficult to isolate the effects of roommates and previous room occupants, since the exposure and outcome are common and may originate from multiple sources.⁴⁴ On the contrary, pathogens such as influenza and group A streptococcus are more commonly associated with outbreak scenarios, making it easier to single out the effects of particular exposures.⁴⁵ Other factors that may have contributed to inconsistent findings across studies are variations in how exposures and outcomes were defined and operationalized (eg, differences in case definitions, case finding methods, and timing of exposure).

While the inconsistency of findings for some of the organisms could be due to artifact, there may nevertheless be real differences in the effects of roommate and prior room occupant exposure based on the biologic characteristics of the infecting species. Microorganisms vary in their abilities to produce spores and survive changes to atmospheric temperature and moisture conditions.⁴⁶ In addition, some organisms favor specific sites of colonization or infection that may produce greater shedding of infectious material and higher potential for environmental contamination.⁴⁶ For example, a study of multidrug-resistant pathogens found that environmental contamination was more common surrounding patients with gram-positive versus gram-negative infections.²² Furthermore, organism species differ in their resiliency to withstand cleaning agents and methods.^47,48

The preponderance of evidence presented in this review suggests that there is a link between exposure to infected or colonized roommates and previous room occupants and the risk of HAIs. These findings present a number of practice and policy implications. First, the fact that patient rooms may serve as a reservoir for pathogens deposited by roommates and previous occupants highlights the importance of proper hand hygiene, not just for staff but for competent patients and their visitors as well.⁴⁹ To underscore this point, a molecular typing study demonstrated that 12% of patients who became newly colonized with MRSA while in the intensive care unit acquired a strain that most probably came from contamination in their immediate environment.¹³ Second, these results emphasize the need for improved cleaning and disinfection of patient rooms, both during patients’ hospital stays and upon their discharge. For patients with known infection or colonization, targeted daily and terminal cleaning procedures that are tailored to specific organisms may reduce environmental contamination and infection rates.⁵⁰ Enhancement of routine cleaning measures should not be limited to patients with known infection or colonization, however, since patients may contaminate their environments during incubation periods before the infections are detected or when colonization is not detected through active surveillance.

There were some limitations to this systematic review. It is possible that some studies which would have met the inclusion criteria were not identified. Only databases indexed in PubMed were included, so any unpublished reports and other gray literature would not have been detected by our search. Similarly, studies that found significant positive associations may have been more likely to appear in the literature due to publication bias. Our restriction to articles published in English may have also excluded some relevant papers. While a major strength of this study is its coverage of two and a half decades of literature, changes in the epidemiology of HAIs, infection control policies and procedures, and study methodology over time may have introduced some variability to the studies we reviewed. Lastly, we were unable to conduct a meta-analysis or provide a funnel plot because the studies assessed a wide variety of outcomes.

Notwithstanding these limitations, it is notable that the studies which reported significant findings were conducted across a range of institutions in several different countries across multiple decades. Presumably, the diverse study facilities employed a variety of cleaning products, methods, and infection control policies. Despite possible variations in practice, exposure to roommates and prior room occupants may have played a role in infection outcomes. Several gaps in the literature remain, however, specifically with regard to organisms that are endemic in health care settings and, therefore, difficult to associate with specific sources of exposure. The use of molecular typing would provide more definitive evidence concerning the role of roommates and prior room occupants in the epidemiology of HAIs.

Acknowledgment

The abstract of this paper was presented at IDWeek 2015 as a poster presentation with interim findings. The poster’s abstract was published in “IDWeek 2015 Abstracts” in Open Forum Infectious Diseases: http://ofid.oxfordjournals.org/content/2/suppl_1/1706.full. doi: 10.1093/ofid/ofv133.1256

Disclosure

The authors report no conflicts of interest in this work.

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