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- Open Access
Spatial relationships among public places frequented by families plagued by methicillin-resistant Staphylococcus aureus
BMC Research Notes volume 11, Article number: 692 (2018)
To understand factors associated with community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) acquisition and infection, we mapped public places (including personal service establishments, fitness centers, pools, schools, and daycares) visited by members of households affected by CA-MRSA skin and soft tissue infection.
From January 2012 to October 2015, households of children with CA-MRSA SSTI in metropolitan St. Louis were enrolled in the HOME: Household Observation of MRSA in the Environment study. Addresses of public places visited within 3 months of enrollment were reported by 671 participants and were analyzed using a geographic information system (GIS). The Nearest Neighbor Tool in ArcGIS assessed clustering of public places within the study region. Public places were significantly clustered within the study area compared to the expected distance between locations (p < 0.001). Additionally, one-third (48/150) of participating households visited at least one public place in common with other households. No significant relationship between participants visiting the public places within 3 months of enrollment and subsequent colonization or SSTI were found. Understanding community behavior is critical to informing public health initiatives to reduce the prevalence of CA-MRSA infections.
Staphylococcus aureus is a commensal organism, colonizing approximately one-third of the population . S. aureus is also a successful pathogen, causing a spectrum of infections from skin and soft tissue infection (SSTI) to severe, life-threatening infections . Community-associated methicillin-resistant S. aureus (CA-MRSA) has emerged as the leading cause of SSTI in otherwise healthy people . CA-MRSA is transmitted by direct skin-to-skin contact or contact with a contaminated surface, and can survive on surfaces for months . Currently, there is equipoise surrounding the most effective measures to combat the transmission of S. aureus in the community.
Staphylococcus aureus contamination has been documented in public places such as locker rooms, exercise facilities and daycare centers [5, 6]. Understanding community transmission dynamics which contribute to S. aureus acquisition is essential. There may be an underlying spatial relationship in populations where CA-MRSA prevalence is high. Utilizing tools such as geographic information systems (GIS) allows researchers to reveal and understand disease trends within populations that may not be visible using other methods. Previous studies have investigated the role of geography as a risk factor for developing MRSA SSTI ; to our knowledge, no study has mapped public places visited by pediatric patients and their household contacts to elucidate factors contributing to MRSA acquisition and transmission.
We mapped public places visited by pediatric index patients with acute MRSA SSTI and their household contacts—enrolled in a larger study of household MRSA transmission—in order to determine whether: (1) public places visited by participants were significantly clustered within the study area; (2) household members from different households affected by CA-MRSA were visiting the same public places; and (3) public places visited by household members in the 3 months prior to index patient acute MRSA SSTI were associated with S. aureus colonization or incidence of SSTI.
Recruitment for the HOME: Household Observation of MRSA in the Environment study took place between January 2012 and October 2015, as previously described, following approval from the Washington University Institutional Review Board . Otherwise healthy pediatric patients presenting with a recent culture-confirmed CA-MRSA SSTI (i.e., index patients) living in metropolitan St. Louis were enrolled along with their household contacts. Participants were recruited from St. Louis Children’s Hospital (SLCH), Cardinal Glennon Children’s Hospital, and Washington University Pediatric and Adolescent Ambulatory Research Consortium (WU PAARC)-affiliated community practices. All participants provided written informed consent/assent and parents/guardians provided consent on behalf of minors.
At enrollment the investigative team swabbed participants in the anterior nares, axillae, and inguinal folds (Eswab, Becton–Dickinson [BD], Franklin Lakes, NJ) to determine S. aureus colonization status. S. aureus isolation, identification, and antibiotic susceptibility testing methods have been previously reported . A survey was administered regarding potential factors associated with S. aureus colonization and infection including medical history, hygiene practices, and activities. Questions about activities assessed whether participants had been to public places such as a hair salon, day spa, nail salon, tanning bed, fitness gym, used a public locker room, used a public shower, swam in a public pool, and/or used a public sauna/hot tub within 3 months of enrollment. Additionally, information was collected regarding daycare, school, or before/after school program attendance. The name/location of all non-residential facilities were recorded.
Addresses for public places were compiled from participant survey responses. Locations were excluded from the analysis if the description was too vague to find a corresponding address (e.g., participants provided nonspecific names of franchises with multiple nearby locations). Addresses were assigned geographical coordinates using ArcGIS version 10.4.1 (Esri, Redlands, California) and analyzed using the Average Nearest Neighbor tool, which provides a ratio of the observed mean distance and the expected mean distance between locations (Nearest Neighbor Index) . An index of < 1 indicates that the locations exhibit clustering within the study area compared to the distance expected by chance alone; p-values < 0.05 were considered significant. The Nearest Neighbor Index was calculated for daycare centers, schools, and before/after school programs for children < 18 years old (N = 360). Clustering of all other public places was analyzed for the entire cohort (N = 671). Additionally, address frequency analysis and Nearest Neighbor analysis were performed at the household level to determine whether study participants from more than one household visited the same public places, and if these locations were spatially related. Sub-analysis was conducted to determine the median driving distance from participating households’ home addresses to the most commonly visited public places. Logistic regression was performed in SPSS version 25 for Windows (IBM SPSS, Chicago, IL) to determine whether visiting any public places at least once a month in the 3 months prior to enrollment was associated with SSTI and/or S. aureus colonization.
One-hundred fifty households comprised of 671 participants were enrolled. Participants resided in metropolitan St. Louis, Missouri, extending into western Illinois, spanning 120 miles. Median household distance from SLCH was 17.3 miles (range 0.9–76.0 miles). Forty-seven percent of participants were male and the median age among participants was 15.0 years (0.1-82.3). Participants mostly identified as Caucasian (69%), while 27% were African-American; 5% of participants identified as Latino/Hispanic. Forty-one percent of participants were colonized with S. aureus at enrollment: 21% with MRSA, 17% with methicillin-susceptible S. aureus (MSSA), and 3% with both MRSA and MSSA at different anatomic sites.
Among daycare centers, schools, and before/after school programs, the Nearest Neighbor Index was 0.109 (p < 0.001), indicating clustering. For hair salons, day spas, nail salons, tanning beds, fitness gyms/exercise facilities, public showers, public locker rooms, public pools, and public saunas/hot tubs/Jacuzzis, the Nearest Neighbor Index was 0.129 (p < 0.001), also indicating clustering. Clustering within the most frequently visited categories of public places (Fig. 1a) (fitness gyms, hair salons, nail salons, and public pools) was also significant (p < 0.001 for each analysis). Median driving distance between the locations visited by more than one household and the home address of the households that visited them was 12.5 miles (range 0.8–58.5 miles), suggesting that these frequently visited locations were not shared among households based solely on geographic proximity to their homes.
Address frequency analysis revealed that 48 of 150 households (32%) had a member who visited at least one of the same public places as a member of another participating household. Five households (3%) had at least one member that visited a public place that was also visited by a member of two or more participating households. For example, a member(s) of Household B went to three different locations within the three months prior to study enrollment—a nail salon, a pool, and a fitness center—that had been visited by members of four, three and two other study households, respectively (Fig. 1b). Members of Household T visited the same locations as study participants from six other households, twice overlapping with Household K. Members of Household X visited three public locations that a member(s) of 12 other households also visited. There were no independent associations between visiting any of the public places at least one time per month in the 3 months prior to enrollment and S. aureus colonization or SSTI (Table 1).
Residential addresses have been shown to be a risk factor for MRSA infection [7, 10]. In order to devise interventions to stop the spread of S. aureus, it is important to understand community reservoirs for transmission. There is a dearth of information regarding visiting public places and risk of CA-MRSA infection. In this study, we demonstrated that, overall, public places visited by members of households affected by CA-MRSA infections are clustered within the study radius, meaning that there is a significant, non-random spatial relationship observed among them. Additionally, many study households were visiting the same public places, suggesting that those locations may be related to CA-MRSA transmission. We demonstrated that approximately one-third of the households in our study have been patrons of the same nail salons, hair salons, fitness centers, and swimming pools in the 3 months prior to enrollment in the study.
Previously published studies have shown a significant, positive relationship between utilizing personal care service establishments and SSTI . Nail salons and hair salons are places where, if present, suboptimal sanitation and hygiene practices, such as the improper cleaning of tools (e.g. nail trimmers, towels, hairbrushes) could propagate MRSA on items used for multiple customers, leading to transmission. While nail salons have been established as a reservoir for infectious agents, such as Mycobacteria , there was no similar association in the present study between having been to locations named by participants in the 3 months prior to enrollment and having had an SSTI.
In the present study, participants visited many of the same public places (e.g., hair and nail salons and swimming pools) despite distance from their homes, which demonstrates the community-wide nature of the CA-MRSA threat. Further studies assessing the temporal relationship between CA-MRSA and public locations, as well as other community reservoirs, are necessary to understand community behavior, inform the development of interventions, and prevent transmission.
The cross-sectional nature of the study limits our ability to establish temporality among the study results. Additionally, study data were self-reported, thus there is the possibility of information bias, though it is likely nondifferential. Households were selected from a limited geographic region, and results may not be generalizable to other locations.
community-associated methicillin-resistant Staphylococcus aureus
geographic information system
methicillin-susceptible Staphylococcus aureus
methicillin-resistant Staphylococcus aureus
Saint Louis Children’s Hospital
skin and soft tissue infection
- WU PAARC:
Washington University Pediatric and Adolescent Ambulatory Research Consortium
Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001–2004. J Infect Dis. 2008;197(9):1226–34.
Chambers HF. The changing epidemiology of Staphylococcus aureus? J Emerg Infect Dis. 2001;7(2):178–82.
Kaplan SL. Community-acquired methicillin-resistant Staphylococcus aureus infections in children. Semin Pediatr Infect Dis. 2006;17(3):113–9.
Boyce JM. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect. 2007;65(Suppl 2):50–4.
Kazakova SV, Hageman JC, Matava M, Srinivasan A, Phelan L, Garfinkel B, et al. A clone of methicillin-resistant Staphylococcus aureus among professional football players. N Engl J Med. 2005;352(5):468–75.
Moritz ED, Hanson BM, Kates AE, Smith TC. Molecular characteristics of Staphylococcus aureus isolated from employees, children, and environmental surfaces in Iowa child daycare facilities. Am J Infect Control. 2015;43(5):482–8.
Rossini CJ, Moriarty KP, Tashjian DB, Garb JL, Wait RB. Geographic distribution of community-acquired methicillin-resistant Staphylococcus aureus soft tissue infections. J Pediatr Surg. 2011;46(6):1089–92.
Fritz SA, Hogan PG, Singh LN, Thompson RM, Wallace MA, Whitney K, et al. Contamination of environmental surfaces with Staphylococcus aureus in households with children infected with methicillin-resistant S aureus. JAMA Pediatr. 2014;168(11):1030–8.
Chang K-t. Introduction to geographic information systems. 1st ed. New City: McGraw-Hill Education; 2015.
Tosas Auguet O, Betley JR, Stabler RA, Patel A, Ioannou A, Marbach H, et al. Evidence for community transmission of community-associated but not health-care-associated methicillin-resistant Staphylococcus aureus strains linked to social and material deprivation: spatial analysis of cross-sectional data. PLoS Med. 2016;13(1):e1001944.
Winthrop KL, Abrams M, Yakrus M, Schwartz I, Ely J, Gillies D, et al. An outbreak of mycobacterial furunculosis associated with footbaths at a nail salon. N Engl J Med. 2002;346(18):1366–71.
KLP, PGH, and SAF contributed to the study concept and design. KLP, PGH, AAC, and SAF contributed to acquisition of clinical and laboratory data. KLP, PGH, and SAF contributed to statistical analysis. KLP, PGH, AAC, and SAF contributed to data interpretation. KLP, PGH, and SAF contributed to initial manuscript drafting. KLP, PGH, AAC, and SAF contributed to revisions for intellectual content. SAF obtained funding. All authors agreed to be accountable for all aspects of the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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Datasets generated and analyzed during the current study are not publicly available as addresses associated with patients constitute protected health information.
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Ethics approval and consent to participate
The Washington University Institutional Review Board approved study procedures; all participants provided written informed consent or assent. Consent was obtained from a parent/guardian on behalf of participants age 17 and younger.
This work was supported by the Children’s Discovery Institute of Washington University and St. Louis Children’s Hospital; National Institutes of Health/National Institute of Allergy and Infectious Diseases [Grant Number K23-AI091690 to S.A.F.]; the National Institutes of Health/National Center for Advancing Translational Sciences [Grant Number UL1-TR000448 to C.-A.D.B. and S.A.F.]; and the Agency for Healthcare Research and Quality [Grant Numbers R01-HS021736, R01-HS024269 to S.A.F.]. These funding sources had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health or the Agency for Healthcare Research and Quality.
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Parrish, K.L., Hogan, P.G., Clemons, A.A. et al. Spatial relationships among public places frequented by families plagued by methicillin-resistant Staphylococcus aureus. BMC Res Notes 11, 692 (2018). https://doi.org/10.1186/s13104-018-3797-4
- Staphylococcus aureus
- Community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA)
- Geographic information systems (GIS)