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Figure 1.
Study Flowchart
Study Flowchart

Individuals with index community-associated, methicillin-resistant Staphylococcus aureus infections and members of their households in Northern Manhattan and South Bronx.

aReasons for exclusion included being a resident in a long-term care facility, being hospitalized within the past 6 months, being homeless or living in a shelter, being younger than 1 year, being a member of a household that already participated in the study, or having a chronic illness, such as end-stage renal disease.

Figure 2.
Distribution of Staphylococcal Protein A (spa) Types
Distribution of Staphylococcal Protein A (spa) Types

The 61 clinical isolates available for spa typing are shown as distributed among infected individuals (index patients), index patients with isolate colonization (colonized), households with a nonindex household member with isolate colonization, and environmentally contaminated households. MRSA indicates methicillin-resistant Staphylococcus aureus.

Figure 3.
Kaplan-Meier Product-Limit Survival Estimates
Kaplan-Meier Product-Limit Survival Estimates

The curves depict rates of recurrent infection among index patients in households with concordant environmental contamination compared with index patients in households without concordant environmental contamination. Cross signs indicate censored.

Table.  
Demographic and Clinical Characteristics and Presence of Clinical Isolates in the Household Among Individuals With CA-MRSA Infections
Demographic and Clinical Characteristics and Presence of Clinical Isolates in the Household Among Individuals With CA-MRSA Infections
1.
David  MZ, Daum  RS.  Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic.  Clin Microbiol Rev. 2010;23(3):616-687.PubMedGoogle ScholarCrossref
2.
Fridkin  SK, Hageman  JC, Morrison  M,  et al; Active Bacterial Core Surveillance Program of the Emerging Infections Program Network.  Methicillin-resistant Staphylococcus aureus disease in three communities.  N Engl J Med. 2005;352(14):1436-1444.PubMedGoogle ScholarCrossref
3.
Uhlemann  AC, Knox  J, Miller  M,  et al.  The environment as an unrecognized reservoir for community-associated methicillin resistant Staphylococcus aureus USA300: a case-control study.  PLoS One. 2011;6(7):e22407.PubMedGoogle ScholarCrossref
4.
Knox  J, Uhlemann  AC, Miller  M,  et al.  Environmental contamination as a risk factor for intra-household Staphylococcus aureus transmission.  PLoS One. 2012;7(11):e49900.PubMedGoogle ScholarCrossref
5.
Uhlemann  AC, Dordel  J, Knox  JR,  et al.  Molecular tracing of the emergence, diversification, and transmission of S aureus sequence type 8 in a New York community.  Proc Natl Acad Sci U S A. 2014;111(18):6738-6743.PubMedGoogle ScholarCrossref
6.
Davis  MF, Iverson  SA, Baron  P,  et al.  Household transmission of methicillin-resistant Staphylococcus aureus and other staphylococci.  Lancet Infect Dis. 2012;12(9):703-716.PubMedGoogle ScholarCrossref
7.
Lautenbach  E, Tolomeo  P, Nachamkin  I, Hu  B, Zaoutis  TE.  The impact of household transmission on duration of outpatient colonization with methicillin-resistant Staphylococcus aureus.  Epidemiol Infect. 2010;138(5):683-685.PubMedGoogle ScholarCrossref
8.
Eells  SJ, David  MZ, Taylor  A,  et al.  Persistent environmental contamination with USA300 methicillin-resistant Staphylococcus aureus and other pathogenic strain types in households with S aureus skin infections.  Infect Control Hosp Epidemiol. 2014;35(11):1373-1382.PubMedGoogle ScholarCrossref
9.
Knox  J, Uhlemann  AC, Lowy  FD.  Staphylococcus aureus infections: transmission within households and the community.  Trends Microbiol. 2015;23(7):437-444.PubMedGoogle ScholarCrossref
10.
Macal  CM, North  MJ, Collier  N,  et al.  Modeling the transmission of community-associated methicillin-resistant Staphylococcus aureus: a dynamic agent-based simulation.  J Transl Med. 2014;12:124.PubMedGoogle ScholarCrossref
11.
Alam  MT, Read  TD, Petit  RA  III,  et al.  Transmission and microevolution of USA300 MRSA in US households: evidence from whole-genome sequencing.  MBio. 2015;6(2):e00054.PubMedGoogle ScholarCrossref
12.
Jones  TF, Creech  CB, Erwin  P, Baird  SG, Woron  AM, Schaffner  W.  Family outbreaks of invasive community-associated methicillin-resistant Staphylococcus aureus infection.  Clin Infect Dis. 2006;42(9):e76-e78.PubMedGoogle ScholarCrossref
13.
Cook  HA, Furuya  EY, Larson  E, Vasquez  G, Lowy  FD.  Heterosexual transmission of community-associated methicillin-resistant Staphylococcus aureus.  Clin Infect Dis. 2007;44(3):410-413.PubMedGoogle ScholarCrossref
14.
Zafar  U, Johnson  LB, Hanna  M,  et al.  Prevalence of nasal colonization among patients with community-associated methicillin-resistant Staphylococcus aureus infection and their household contacts.  Infect Control Hosp Epidemiol. 2007;28(8):966-969.PubMedGoogle Scholar
15.
Johansson  PJ, Gustafsson  EB, Ringberg  H.  High prevalence of MRSA in household contacts.  Scand J Infect Dis. 2007;39(9):764-768.PubMedGoogle ScholarCrossref
16.
Ho  PL, Cheung  C, Mak  GC,  et al.  Molecular epidemiology and household transmission of community-associated methicillin-resistant Staphylococcus aureus in Hong Kong.  Diagn Microbiol Infect Dis. 2007;57(2):145-151.PubMedGoogle ScholarCrossref
17.
Stone  A, Quittell  L, Zhou  J,  et al.  Staphylococcus aureus nasal colonization among pediatric cystic fibrosis patients and their household contacts.  Pediatr Infect Dis J. 2009;28(10):895-899.PubMedGoogle ScholarCrossref
18.
Huang  YC, Ho  CF, Chen  CJ, Su  LH, Lin  TY.  Nasal carriage of methicillin-resistant Staphylococcus aureus in household contacts of children with community-acquired diseases in Taiwan.  Pediatr Infect Dis J. 2007;26(11):1066-1068.PubMedGoogle ScholarCrossref
19.
Busato  CR, Carneiro Leão  MT, Gabardo  J.  Staphylococcus aureus nasopharyngeal carriage rates and antimicrobial susceptibility patterns among health care workers and their household contacts.  Braz J Infect Dis. 1998;2(2):78-84.PubMedGoogle Scholar
20.
Wagenvoort  JH, Toenbreker  HM, Nurmohamed  A, Davies  BI.  Transmission of methicillin-resistant Staphylococcus aureus within a household.  Eur J Clin Microbiol Infect Dis. 1997;16(5):399-400.PubMedGoogle ScholarCrossref
21.
Miller  LG, Eells  SJ, David  MZ,  et al.  Staphylococcus aureus skin infection recurrences among household members: an examination of host, behavioral, and pathogen-level predictors.  Clin Infect Dis. 2015;60(5):753-763.PubMedGoogle ScholarCrossref
22.
Huijsdens  XW, van Santen-Verheuvel  MG, Spalburg  E,  et al.  Multiple cases of familial transmission of community-acquired methicillin-resistant Staphylococcus aureus.  J Clin Microbiol. 2006;44(8):2994-2996.PubMedGoogle ScholarCrossref
23.
L’Hériteau  F, Lucet  JC, Scanvic  A, Bouvet  E.  Community-acquired methicillin-resistant Staphylococcus aureus and familial transmission.  JAMA. 1999;282(11):1038-1039.PubMedGoogle ScholarCrossref
24.
Yamamoto  T, Takano  T, Yabe  S,  et al.  Super-sticky familial infections caused by Panton-Valentine leukocidin-positive ST22 community-acquired methicillin-resistant Staphylococcus aureus in Japan.  J Infect Chemother. 2012;18(2):187-198.PubMedGoogle ScholarCrossref
25.
Yabe  S, Takano  T, Higuchi  W, Mimura  S, Kurosawa  Y, Yamamoto  T.  Spread of the community-acquired methicillin-resistant Staphylococcus aureus USA300 clone among family members in Japan.  J Infect Chemother. 2010;16(5):372-374.PubMedGoogle ScholarCrossref
26.
Amir  NH, Rossney  AS, Veale  J, O’Connor  M, Fitzpatrick  F, Humphreys  H.  Spread of community-acquired meticillin-resistant Staphylococcus aureus skin and soft-tissue infection within a family: implications for antibiotic therapy and prevention.  J Med Microbiol. 2010;59(pt 4):489-492.PubMedGoogle ScholarCrossref
27.
Dancer  SJ.  The role of environmental cleaning in the control of hospital-acquired infection.  J Hosp Infect. 2009;73(4):378-385.PubMedGoogle ScholarCrossref
28.
Dancer  SJ.  Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning.  Lancet Infect Dis. 2008;8(2):101-113.PubMedGoogle ScholarCrossref
29.
Gwizdala  RA, Miller  M, Bhat  M,  et al.  Staphylococcus aureus colonization and infection among drug users: identification of hidden networks.  Am J Public Health. 2011;101(7):1268-1276.PubMedGoogle ScholarCrossref
30.
Miko  BA, Herzig  CT, Mukherjee  DV,  et al.  Is environmental contamination associated with Staphylococcus aureus clinical infection in maximum security prisons?  Infect Control Hosp Epidemiol. 2013;34(5):540-542.PubMedGoogle ScholarCrossref
31.
Fritz  SA, Hogan  PG, Singh  LN,  et al.  Contamination of environmental surfaces with Staphylococcus aureus in households with children infected with methicillin-resistant S aureus.  JAMA Pediatr. 2014;168(11):1030-1038.PubMedGoogle ScholarCrossref
32.
Miller  LG, Diep  BA.  Clinical practice: colonization, fomites, and virulence: rethinking the pathogenesis of community-associated methicillin-resistant Staphylococcus aureus infection.  Clin Infect Dis. 2008;46(5):752-760.PubMedGoogle ScholarCrossref
33.
Miller  LG, Tan  J, Eells  SJ, Benitez  E, Radner  AB.  Prospective investigation of nasal mupirocin, hexachlorophene body wash, and systemic antibiotics for prevention of recurrent community-associated methicillin-resistant Staphylococcus aureus infections.  Antimicrob Agents Chemother. 2012;56(2):1084-1086.PubMedGoogle ScholarCrossref
34.
Fritz  SA, Hogan  PG, Hayek  G,  et al.  Household versus individual approaches to eradication of community-associated Staphylococcus aureus in children: a randomized trial.  Clin Infect Dis. 2012;54(6):743-751.PubMedGoogle ScholarCrossref
35.
Fritz  SA, Hogan  PG, Camins  BC,  et al.  Mupirocin and chlorhexidine resistance in Staphylococcus aureus in patients with community-onset skin and soft tissue infections.  Antimicrob Agents Chemother. 2013;57(1):559-568.PubMedGoogle ScholarCrossref
36.
Kaplan  SL, Forbes  A, Hammerman  WA,  et al.  Randomized trial of “bleach baths” plus routine hygienic measures vs routine hygienic measures alone for prevention of recurrent infections.  Clin Infect Dis. 2014;58(5):679-682.PubMedGoogle ScholarCrossref
37.
Kohler  P, Bregenzer-Witteck  A, Rettenmund  G, Otterbech  S, Schlegel  M.  MRSA decolonization: success rate, risk factors for failure and optimal duration of follow-up.  Infection. 2013;41(1):33-40.PubMedGoogle ScholarCrossref
38.
Shopsin  B, Gomez  M, Montgomery  SO,  et al.  Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains.  J Clin Microbiol. 1999;37(11):3556-3563.PubMedGoogle Scholar
39.
Harmsen  D, Claus  H, Witte  W,  et al.  Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management.  J Clin Microbiol. 2003;41(12):5442-5448.PubMedGoogle ScholarCrossref
40.
Milheiriço  C, Oliveira  DC, de Lencastre  H.  Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus.  Antimicrob Agents Chemother. 2007;51(9):3374-3377.PubMedGoogle ScholarCrossref
41.
Milheiriço  C, Oliveira  DC, de Lencastre  H.  Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: “SCCmec IV multiplex”.  J Antimicrob Chemother. 2007;60(1):42-48.PubMedGoogle ScholarCrossref
42.
Blanc  DS, Petignat  C, Moreillon  P, Wenger  A, Bille  J, Francioli  P.  Quantitative antibiogram as a typing method for the prospective epidemiological surveillance and control of MRSA: comparison with molecular typing.  Infect Control Hosp Epidemiol. 1996;17(10):654-659.PubMedGoogle ScholarCrossref
43.
Younger  JJ, Christensen  GD, Bartley  DL, Simmons  JC, Barrett  FF.  Coagulase-negative staphylococci isolated from cerebrospinal fluid shunts: importance of slime production, species identification, and shunt removal to clinical outcome.  J Infect Dis. 1987;156(4):548-554.PubMedGoogle ScholarCrossref
44.
Montesinos  I, Salido  E, Delgado  T, Cuervo  M, Sierra  A.  Epidemiologic genotyping of methicillin-resistant Staphylococcus aureus by pulsed-field gel electrophoresis at a university hospital and comparison with antibiotyping and protein A and coagulase gene polymorphisms.  J Clin Microbiol. 2002;40(6):2119-2125.PubMedGoogle ScholarCrossref
45.
Omar  NY, Ali  HA, Harfoush  RA, El Khayat  EH.  Molecular typing of methicillin resistant Staphylococcus aureus clinical isolates on the basis of protein A and coagulase gene polymorphisms.  Int J Microbiol. 2014;2014:650328.PubMedGoogle ScholarCrossref
46.
Mehndiratta  PL, Bhalla  P.  Typing of methicillin resistant Staphylococcus aureus: a technical review.  Indian J Med Microbiol. 2012;30(1):16-23.PubMedGoogle ScholarCrossref
47.
McDougal  LK, Steward  CD, Killgore  GE, Chaitram  JM, McAllister  SK, Tenover  FC.  Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database.  J Clin Microbiol. 2003;41(11):5113-5120.PubMedGoogle ScholarCrossref
48.
Miller  LG, Eells  SJ, Taylor  AR,  et al.  Staphylococcus aureus colonization among household contacts of patients with skin infections: risk factors, strain discordance, and complex ecology.  Clin Infect Dis. 2012;54(11):1523-1535.PubMedGoogle ScholarCrossref
49.
Knox  J, Van Rijen  M, Uhlemann  AC,  et al.  Community-associated methicillin-resistant Staphylococcus aureus transmission in households of infected cases: a pooled analysis of primary data from three studies across international settings.  Epidemiol Infect. 2015;143(2):354-365.PubMedGoogle ScholarCrossref
50.
Harbarth  S, Liassine  N, Dharan  S, Herrault  P, Auckenthaler  R, Pittet  D.  Risk factors for persistent carriage of methicillin-resistant Staphylococcus aureus.  Clin Infect Dis. 2000;31(6):1380-1385.PubMedGoogle ScholarCrossref
51.
Miller  M, Cook  HA, Furuya  EY,  et al.  Staphylococcus aureus in the community: colonization versus infection.  PLoS One. 2009;4(8):e6708.PubMedGoogle ScholarCrossref
52.
Lee  CJ, Sankaran  S, Mukherjee  DV,  et al.  Staphylococcus aureus oropharyngeal carriage in a prison population.  Clin Infect Dis. 2011;52(6):775-778.PubMedGoogle ScholarCrossref
53.
Miko  BA, Uhlemann  AC, Gelman  A,  et al.  High prevalence of colonization with Staphylococcus aureus clone USA300 at multiple body sites among sexually transmitted disease clinic patients: an unrecognized reservoir.  Microbes Infect. 2012;14(12):1040-1043.PubMedGoogle ScholarCrossref
54.
Peters  PJ, Brooks  JT, Limbago  B,  et al.  Methicillin-resistant Staphylococcus aureus colonization in HIV-infected outpatients is common and detection is enhanced by groin culture.  Epidemiol Infect. 2011;139(7):998-1008.PubMedGoogle ScholarCrossref
55.
Eveillard  M, de Lassence  A, Lancien  E, Barnaud  G, Ricard  JD, Joly-Guillou  ML.  Evaluation of a strategy of screening multiple anatomical sites for methicillin-resistant Staphylococcus aureus at admission to a teaching hospital.  Infect Control Hosp Epidemiol. 2006;27(2):181-184.PubMedGoogle ScholarCrossref
56.
Mermel  LA, Cartony  JM, Covington  P, Maxey  G, Morse  D.  Methicillin-resistant Staphylococcus aureus colonization at different body sites: a prospective, quantitative analysis.  J Clin Microbiol. 2011;49(3):1119-1121.PubMedGoogle ScholarCrossref
57.
Lautenbach  E, Nachamkin  I, Hu  B,  et al.  Surveillance cultures for detection of methicillin-resistant Staphylococcus aureus: diagnostic yield of anatomic sites and comparison of provider- and patient-collected samples.  Infect Control Hosp Epidemiol. 2009;30(4):380-382.PubMedGoogle ScholarCrossref
58.
Cluzet  VC, Gerber  JS, Nachamkin  I,  et al.  Duration of colonization and determinants of earlier clearance of colonization with methicillin-resistant Staphylococcus aureus Clin Infect Dis. 2015;60(10):1489-1496.PubMedGoogle Scholar
Original Investigation
June 2016

Association of Environmental Contamination in the Home With the Risk for Recurrent Community-Associated, Methicillin-Resistant Staphylococcus aureus Infection

Author Affiliations
  • 1Division of Infectious Diseases, Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, New York
  • 2Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, New York
  • 3Panna Technologies Inc, New York, New York
  • 4Department of Epidemiology and Community Health, School of Health Sciences and Practice, New York Medical College, New York, New York
  • 5Department of Pathology and Cell Biology, College of Physicians and Surgeons, Columbia University, New York, New York
 

Copyright 2016 American Medical Association. All Rights Reserved. Applicable FARS/DFARS Restrictions Apply to Government Use.

JAMA Intern Med. 2016;176(6):807-815. doi:10.1001/jamainternmed.2016.1500
Abstract

Importance  The role of environmental contamination in recurrent Staphylococcus aureus infections within households and its potential effect on intervention strategies has been debated recently.

Objective  To assess whether household environmental contamination increases the risk for recurrent infection among individuals with a community-associated methicillin-resistant S aureus (MRSA) infection.

Design, Setting, and Participants  This cohort study was conducted from November 1, 2011, to June 30, 2014, in the Columbia University Medical Center catchment area. All patients within 72 hours of presentation with skin or soft-tissue infections and blood, urine, or sputum cultures positive for MRSA were identified. Two hundred sixty-two patients met study inclusion criteria; 83 of these (31.7%) agreed to participate (index patients) with 214 household members. Participants were followed up for 6 months, and 62 of the 83 households (74.7%) completed follow-up. Participants and researchers were blinded to exposure status throughout the study. Follow-up was completed on June 30, 2014, and data were assessed from July 1, 2014, to February 19, 2016.

Exposure  Concordant environmental contamination, defined as having an isolate with the identical staphylococcal protein A and staphylococcal chromosomal cassette mec type or antibiogram type as the index patient’s clinical isolate, present on 1 or more environmental surfaces at the time of a home visit to the index patient after infection.

Main Outcomes and Measures  Index recurrent infection, defined as any self-reported infection among the index patients during follow-up.

Results  One patient did not complete any follow-up. Of the remaining 82 index patients, 53 (64.6%) were female and 59 (72.0%) were Hispanic. The mean age was 30 (SD, 20; range, 1-79) years. Forty-nine of 61 MRSA infections where the clinical isolate could be obtained (80.3%) were due to the epidemic strain USA300. Among the 82 households in which a patient had an index MRSA infection, the clinical isolate was present in the environment in 20 (24.4%) and not found in 62 (75.6%). Thirty-five patients (42.7%) reported a recurrent infection during follow-up, of whom 15 (42.9%) required hospitalization. Thirteen recurrent infections were from the 20 households (65.0%) with and 22 were from the 62 households (35.5%) without environmental contamination (P = .04). Environmental contamination increased the rate of index recurrent infection (incident rate ratio, 2.05; 95% CI, 1.03-4.10; P = .04).

Conclusions and Relevance  Household environmental contamination was associated with an increased rate of recurrent infection. Environmental decontamination should be considered as a strategy to prevent future MRSA infections, particularly among households where an infection has occurred.

Introduction

During the last 3 decades, the number of methicillin-resistant Staphylococcus aureus (MRSA) infections in community settings has increased dramatically.1 Most infections involve the skin and soft tissues, but 5% to 10% of these infections have been life threatening.2 Studies have highlighted the household as the primary reservoir for S aureus in the community.3-11 Reports have described how epidemic clones bounce among family members,12,13 resulting in high rates of recurrent infection. The events that follow an initial community-associated (CA)–MRSA infection in a household include an increase in (1) MRSA found among other household members7,14-21; (2) contamination of environmental surfaces3,4,8,21; and (3) the risk for infection among other household members.12,13,21-26

The role of the environment in S aureus transmission and infections has been studied in the health care setting27,28 and in certain high-risk community settings, such as in injection drug–using sites and prisons.29,30 Environmental contamination has been increasingly recognized for its possible role in S aureus transmission and infection within households.3,4,6,8,21,31,32 The potential importance of environmental contamination in S aureus infection is further supported by the mixed success of body-site decolonization interventions designed to prevent recurrent infections within the household, with recurrent infections often occurring despite best efforts.33-36 In the general patient population, the success of MRSA decolonization is highly variable (range, 23%-96%).37 Alternatively, environmental contamination may simply be a surrogate marker of colonization of multiple body sites or more common among households with multiple infections because infected individuals are more likely to shed bacteria into their environment. We conducted a prospective cohort study designed to determine whether environmental contamination of the household increases the risk for recurrent infection among individuals with a CA-MRSA infection while accounting for competing risk factors.

Box Section Ref ID

Key Points

  • Question Does household environmental contamination increase the risk for recurrent infection among individuals with a community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infection?

  • Findings In this prospective cohort study of 82 individuals with CA-MRSA infections, those living in households where environmental items were contaminated with the clinical isolate had twice the risk of developing a recurrent infection compared with those living in households where the clinical isolate was not found in the environment, a significant difference.

  • Meaning Environmental decontamination should be considered when attempting to prevent CA-MRSA infections, particularly among households with multiple infected members.

Methods
Study Population

This prospective cohort study was conducted among patients in the catchment area (defined by surrounding zip codes) of Columbia University Medical Center (CUMC) with a CA-MRSA infection. Data were collected from November 1, 2011, to June 30, 2014. The institutional review board of CUMC approved this study. Written informed consent was obtained from each individual before participation. Parental consent was required for the participation of children younger than 18 years, and pediatric assent was obtained from those capable of providing it.

Study Procedures

Figure 1 summarizes study participant enrollment. Five hundred fifty-four outpatients or inpatients with skin and soft-tissue infections and blood, urine, or sputum cultures positive for MRSA obtained within 72 hours of admission were identified. Patients were ineligible if they were a resident in a long-term care facility, had been hospitalized within the past 6 months, were homeless or living in a shelter, had a chronic illness such as end-stage renal disease, were younger than 1 year, or were a member of a household that already participated in the study. On review of their medical records, 262 patients met the inclusion criteria. We mailed a letter describing the study and attempted to contact these patients by telephone. Of these, 131 (50.0%) could not be reached, 48 (18.3%) refused to participate, and 83 (31.7%) agreed to participate.

Participation involved an initial home visit, during which a structured questionnaire was administered by a trained interviewer (J.K. or J.U.) to the patient with the infection (ie, the index patient) to collect demographic information and assess risk factors for CA-MRSA infection. Potentially sensitive information was obtained using paper-based self-interviewing. All household members who agreed to participate provided the same data as the index patient. After the home visit, monthly follow-up calls were made to the household for 6 months to determine whether any participating household member had an infection in the previous month. One index patient did not complete any follow-up and was excluded from this analysis. The remaining 82 index patients with CA-MRSA infections were included in this analysis; 62 (75.6%) completed follow-up.

The clinical isolates of the index patients were retrieved from the clinical microbiology laboratory at CUMC. At the baseline visit, anterior nares, throat, and inguinal cultures were collected with premoistened swabs (Culturette Systems; Becton Dickinson) from all consenting household members. A standardized list of 11 environmental items were sampled by swabbing the surface area for 30 seconds with premoistened swabs as previously described.3,4 In all households, surfaces sampled included door knobs, the television remote, the living room light switch, toys, the couch, the computer or radio, the house telephone or index cellular phone, the bathroom sink, the toilet seat, the kitchen towel, and kitchen appliance handles.

All swabs were processed as previously described.3,4 Those isolates that were positive for S aureus underwent staphylococcal protein A (spa) sequencing using Ridom StaphType software (Ridom GmbH).38,39 Methicillin resistance was assessed by the presence and type of staphylococcal chromosomal cassette mec (SCCmec) using multiplex polymerase chain reaction analysis.40,41 The S aureus isolates characterized as spa type 8 with or without the presence of SCCmec were categorized as USA300. All study team members with access to participants were unaware of the results of the environmental samples to minimize differential treatment between households with and without concordant environmental contamination.

Measures

The outcome, index recurrent infection, was defined as any self-reported new infection by the index patient during follow-up, but it did not necessarily occur at a different anatomical site. Medical records of all index patients with a reported recurrent infection were reviewed to determine whether they returned to CUMC for treatment of the reported infection.

The primary exposure, concordant environmental contamination, was defined as an isolate with the identical spa and SCCmec types as the index clinical isolate found on an environmental surface. The primary 2 confounders were defined as having an isolate with the identical spa-type and SCCmec type as the index clinical isolate on the index patient or on a nonindex household member (concordant colonization).

Twenty-one of 82 index clinical isolates (25.6%) were unavailable. When a clinical isolate was unavailable for genotyping and MRSA was present in the household from a human or in the environment (n = 10), antibiogram typing was used to assess strain relatedness between the clinical and colonizing isolates, as previously described.42,43 Antibiogram typing has been used for successful screening of MRSA strains in other studies and is performed similarly to spa typing, although it was slightly more discriminatory.44-46 All clinical isolates were analyzed using a PC34 panel (MicroScan; Beckman Coulter) at the time of their initial isolation. The same analyses were run on 1 colonizing MRSA isolate per spa type among cases with a missing clinical isolate and 1 MRSA isolate identified in the household during the home visit. Results were then compared with those obtained from the relevant index clinical isolate. Clinical and household isolates were considered concordant if they had identical results on all biochemical panels (26 tests) and exhibited minimum inhibitory concentration susceptibilities within 1 dilution on all antimicrobial susceptibility panels (12 tests).

To determine whether the clinical isolates unavailable for genotyping (n = 21) were pulsed-field gel electrophoresis type USA300,47 the results of their biochemical panels and antimicrobial susceptibility panels were compared with biochemical and antimicrobial susceptibility panels on all clinical isolates determined to be USA300 through spa typing. Unavailable clinical isolates whose results fell within the range of values obtained for these clinical isolates were considered to be USA300.

Statistical Analysis

Follow-up was completed on June 30, 2014, and data were analyzed from July 1, 2014, to February 19, 2015. Bivariate analyses of index demographics, household characteristics, and clinical characteristics were compared between households with and without concordant environmental contamination; χ2 tests and 2-tailed t tests were used for these comparisons. We drew Kaplan-Meier survival curves to compare the rate of recurrent infection among index patients with concordant environmental contamination with the rate among index patients without concordant environmental contamination. Index patients were censored once they were unavailable for follow-up or the study period ended. Curves were compared using the log-rank statistic. To identify variables that might confound the association between concordant environmental contamination and index recurrent infection, we assessed the bivariate association of potential confounding variables (a complete list is found in the Table) with concordant environmental contamination (yes or no) and with recurrent index infection (yes or no). All associations were nonsignificant (P < .20). Therefore, no covariates were entered in the Poisson regression model used to estimate the increased rate of index recurrent infection. All statistical tests were 2 sided. Data were analyzed using SAS software (version 9.4; SAS Institute Inc).

Results
Study Population Characteristics

Eighty-two index patients were included in the analyses. The mean age of index patients was 30 (SD, 20; range, 1-79) years, and 53 (64.6%) were female. Fifty-nine patients (72.0%) were Hispanic, 26 (31.7%) had completed high school, 35 (42.7%) were employed, and 58 (70.7%) reported a household income of less than $21 000 per year. These characteristics reflected the demographics of Northern Manhattan and the South Bronx. The mean household size (including the index patient) was 4 individuals (SD, 2; median, 4; range, 1-9). Nine index patients (11.0%) lived alone.

Index patients were interviewed a mean of 34 (SD, 16; range, 13-104) days after their infection. Index infections involved a variety of body sites, including the lower extremity (n = 25), trunk (n = 21), head and neck (n = 14), axilla (n = 14), upper extremity (n = 13), vaginal area (n = 5), and urinary tract (n = 1). Some individuals had infections at more than 1 body site. Thirty-two index patients (39.0%) reported having an antecedent infection similar to the one that qualified them for participation in this study. At the time of the interview, 4 index patients (4.9%) reported that their infection had not healed. All 4 of these patients stated that the infection had healed by the first follow-up telephone call. Index patients reported making a mean of 2 (SD, 1; range, 1-10) visits to a physician to have the infection treated. Seventy-eight index patients (95.1%) received antibiotics for their infection.

In the 82 households, 214 of 225 nonindex members (95.1%) participated. The mean age of nonindex household members was 26 (SD, 19; range, 0-76) years. One hundred six nonindex household members (49.5%) were female. The Table presents the distribution of sociodemographic characteristics, clinical characteristics, and presence of clinical isolates in the household among those with and without concordant environmental contamination.

Molecular Characterization of Clinical S aureus Isolates

Isolates consistent with the epidemic strain USA300 (MRSA t008) were the most common clinical isolate (49 of 61 isolates available [80.3%]) (Figure 2). The remaining 12 clinical isolates (19.7%) belonged to 9 different spa types. Among the clinical isolates classified by antibiogram typing, 13 of 21 (61.9%) were determined to be USA300.

Presence of the Clinical Isolate on Environmental Surfaces

Specimens were collected from 884 environmental items among the 82 households, of which 129 (14.6%) were positive for S aureus and 40 isolates were identified as the clinical isolate. Twenty households (24.4%) had the clinical isolate present in the environment. Among these 20 households, 12 had multiple surfaces that were contaminated. The clinical isolate was found on a variety of surfaces (7 bathroom sinks, 6 television remotes, 6 toilet seats, 4 computers, 4 door knobs, 4 kitchen towels, 4 refrigerator handles, 3 couches, and 2 telephones).

Presence of the Clinical Isolate Among Index Patients

The clinical isolate was found to be present in 25 index patients (30.4%) at the time of the interview. Among these 25 index patients, the clinical isolate was identified from 16 nasal cultures, 8 inguinal cultures, and 7 throat cultures; 5 of the 25 (20.0%) had the clinical isolate present at multiple body sites. The presence of the clinical isolate in the index patient was more frequent among households with than without concordant environmental contamination (15 of 20 [75.0%] vs 10 of 62 [16.1%]; P < .001).

Presence of the Clinical Isolate Among Nonindex Household Members

The clinical isolate was found to be present in a nonindex household member in 19 households (23.2%). Among the 19 households, 27 nonindex household members had the clinical isolate, including multiple members in 7 households. Among these 27 nonindex household members, the clinical isolate was identified from 17 nasal cultures, 12 inguinal cultures, and 8 throat cultures; 9 of the 27 nonindex household members (33.3%) had the isolate present at multiple body sites. The presence of the clinical isolate among nonindex household members was more frequent among households with than without concordant environmental contamination (11 of 20 [55.0%] vs 8 of 62 [12.9%]; P < .001).

Recurrent Infection Among Index Patients

Thirty-five index patients (42.7%) reported a recurrent infection during the follow-up period. Index patients reported a recurrent infection at the following proportions and intervals: 10 (12.2%) at baseline to less than 1 month; 9 (11.0%) at 1 to less than 2 months; 3 (3.7%) at 2 to less than 3 months; 5 (6.1%) at 3 to less than 4 months; 10 (12.2%) at 4 to less than 5 months; and 7 (8.5%) at 5 to 6 months (completion of the study). Fifteen of the 35 index patients with a reported recurrent infection (42.9%) were treated for an MRSA-positive infection at CUMC around the time of their report. During a follow-up home visit, we collected specimen data for 23 of the 35 index patients who reported a recurrent infection (65.7%). In 13 of these 23 index patients (56.5%), an isolate with the identical spa type and SCCmec type as the index clinical isolate was present. Four patients (11.4%) had the recurrent infections at the same site as the initial infection, all of which had healed by the initial home visit. Recurrent index infections were more common among households with than without concordant environmental contamination (13 of 20 [65.0%] vs 22 of 62 [35.5%]; P = .04).

Figure 3 shows the occurrence of these recurrent infections, taking into account censoring. Index patients in households with concordant environmental contamination had less mean follow-up time than index patients in households without concordant environmental contamination (127 vs 141 days), although the difference was not statistically significant (P = .36). The incident rate of recurrent infection among index patients in households with concordant environmental contamination was 0.15 infections per month of follow-up compared with 0.08 infections per month of follow-up among index patients in households without concordant environmental contamination, for an incident rate ratio of 2.05 (95% CI, 1.03-4.04; P = .04).

Infections Among Nonindex Household Members

Twenty-seven of 214 nonindex household members (12.6%) from 15 of 82 households (18.3%) reported infections during the follow-up period. Six nonindex household members reported a recurrent infection by 1 month (2.8%); 4, by 2 months (1.9%); 3, by 3 months (1.4%); 1, by 4 months (0.5%); 6, by 5 months (2.8%); and 7, by 6 months (completion of the study) (3.3%). Infections among nonindex household members were not more common among households with than without concordant environmental contamination (5 of 20 [25.0%] vs 10 of 62 [16.1%]; P = .51).

Usa300

We compared the isolates that caused clinical infection between those classified as USA300 (n = 62) and all other strain types (n = 20). During the household visit, USA300 was less likely to be found on the index patient (19 [30.6%] vs 6 [30.0%]; P = .96), on a nonindex household member (16 [25.8%] vs 3 [15.0%]; P = .32), or in the environment (16 [25.8%] vs 2 [10.0%]; P = .46) compared with all other clinical isolates. Index patients with clinical infections caused by USA300 were not significantly more likely to experience a recurrent infection compared with index patients with clinical infections caused by any other strain type (26 of 62 [41.9%] vs 9 of 20 [45.0%]; P = .81).

Discussion

This prospective cohort study found that household environmental contamination was associated with an increased risk for recurrent infection among individuals who experienced a CA-MRSA infection. Index patients living in households where environmental items were contaminated with the clinical isolate developed recurrent infections at twice the rate of index patients living in households where the clinical isolate was not found in the environment. In contrast, body site colonization with the clinical isolate by either the index patient or other household members did not independently increase the risk for recurrent infection. This finding suggests that the contamination of household surfaces plays a role in recurrent CA-MRSA infection.

These findings add to the accumulating evidence demonstrating the contribution of environmental contamination to the transmission of S aureus in community settings by creating a reservoir for infection in the home.3,4,21,32 This study builds on an earlier retrospective household-based investigation3 that found environmental contamination with the clinical isolate to be associated with an increased likelihood of antecedent MRSA infection. A subsequent study showed that environmental contamination with the clinical isolate was also associated with an increased likelihood of S aureus transmission among household members.4 Eells et al8 reported that infection isolates were detected in households 3 months after infection. This finding was associated with body site colonization of household members with the infection isolate. A recent longitudinal study further supported the role of household fomites as a risk for recurrent infections.21

The results of this study demonstrate the high burden of S aureus among households with a recent CA-MRSA infection. Nearly half of the index patients reported a recurrent infection during the 6-month follow-up, a large portion of whom required additional treatment. This rate is similar to what has been observed in other studies.3,21,34-36 Persistence of the clinical infection isolate in the household is also similar to what has been observed in other studies.3,4,7,8,14-21

Strains consistent with the epidemic strain USA300 were responsible for most of the clinical infections and MRSA strains found in households in this study. This trend has been noted in earlier reports.3-5 Conflicting evidence exists regarding whether USA300 is more likely than other CA-MRSA strains to spread or cause recurrent infection among households in the community.3-5,21,48,49 The results of this study do not suggest that USA300 is better able to colonize body sites or survive in the environment compared with other CA-MRSA strains. Patients infected with USA300 were not at a higher risk for experiencing recurrent infection. Further research is needed to more directly weigh the benefits of using strain-targeted interventions to reduce the burden of S aureus in the community.4,49

Our findings suggest the importance of considering environmental contamination when designing interventions aimed at reducing recurrent CA-MRSA infections. In the health care setting, several studies have shown that increased environmental cleaning reduces the amount of MRSA in the environment, although the benefit to the patient remains controversial.27,28 Household-based studies have investigated the efficacy of different interventions to reduce the incidence of recurrent infections. Although these interventions have been partially successful in reducing colonization, recurrent infections have continued.33-36 These studies used decolonization of nonindex household members; however, they have not included environmental decontamination. Further research is needed to determine whether effective decolonization of the household environment of MRSA-infected patients reduces the risk for subsequent infection.

The strengths of this study are that it used a longitudinal cohort design where participants and researchers were blinded to exposure status to answer a directed research question about whether household environmental contamination is an independent predictor of recurrent infection among patients with a CA-MRSA infection. We accounted for numerous other potential risk factors for recurrent infection in our analyses, including body site colonization. To ensure that body site colonization was accurately measured and thus its potential contribution accounted for,50 multiple body sites were sampled.21,32,48,51-58

This study also has limitations. First, the results are representative of a single, predominantly Hispanic community in Northern Manhattan and the South Bronx, where most of the index patients were female and thus may have reduced generalizability. Second, the outcome measure, index recurrent infection, was based on self-report by a consenting household member, not a clinical assessment. However, medical records were reviewed to determine whether the index patients who reported a recurrent infection were treated at CUMC. Third, the study could have been strengthened by including more detailed information on the treatment experience of the patient, including class of antibiotic prescribed, adherence, and decolonization therapy. Fourth, not all of the clinical isolates were available for these analyses. However, the molecular techniques that were used to assess strain relatedness in the absence of having the clinical isolates previously have been used with success.42,43 Whole genome sequencing would further strengthen this study. Fifth, the study could have been improved by reducing the time between infection and the household visit. In addition, owing to limitations of time and enrollment, the targeted sample size (n = 228) was not achieved. Last, most of the clinical infections among our sample were caused by USA300. Therefore, our ability to make comparisons among strain types was limited by this lack of heterogeneity.

Conclusions

Despite limitations, our findings suggest that household environmental contamination increases the risk for recurrent infection among individuals with an index CA-MRSA infection. Environmental decontamination should be considered as a strategy to prevent CA-MRSA infections.

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Article Information

Corresponding Author: Justin Knox, MPH, Division of Infectious Diseases, Department of Medicine, College of Physicians and Surgeons, Columbia University, 630 W 168th St, New York, NY 10032 (jrk2115@cumc.columbia.edu).

Accepted for Publication: February 27, 2016.

Published Online: May 9, 2016. doi:10.1001/jamainternmed.2016.1500.

Author Contributions: Mr Knox and Dr Lowy had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Knox, Sullivan, Miller, Shi, Uhlemann, Lowy.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Knox, Sullivan, Urena, Miller, Uhlemann, Lowy.

Critical revision of the manuscript for important intellectual content: Knox, Miller, Vavagiakis, Shi, Lowy.

Statistical analysis: Knox, Sullivan, Vavagiakis, Shi.

Obtained funding: Miller, Lowy.

Administrative, technical, or material support: Knox, Sullivan, Urena, Vavagiakis, Lowy.

Study supervision: Knox, Uhlemann, Lowy.

Conflict of Interest Disclosures: None reported.

Funding/Support: This study was supported by grants R01 AI077690, R01 AI077690-S1, and R21 AI103562 (Dr Lowy) and K08 AI090013 (Dr Uhlemann) from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, and the Paul A. Marks Scholarship from the Department of Medicine, College of Physicians and Surgeons, Columbia University.

Role of the Funder/Sponsor: The 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; and decision to submit the manuscript for publication.

References
1.
David  MZ, Daum  RS.  Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic.  Clin Microbiol Rev. 2010;23(3):616-687.PubMedGoogle ScholarCrossref
2.
Fridkin  SK, Hageman  JC, Morrison  M,  et al; Active Bacterial Core Surveillance Program of the Emerging Infections Program Network.  Methicillin-resistant Staphylococcus aureus disease in three communities.  N Engl J Med. 2005;352(14):1436-1444.PubMedGoogle ScholarCrossref
3.
Uhlemann  AC, Knox  J, Miller  M,  et al.  The environment as an unrecognized reservoir for community-associated methicillin resistant Staphylococcus aureus USA300: a case-control study.  PLoS One. 2011;6(7):e22407.PubMedGoogle ScholarCrossref
4.
Knox  J, Uhlemann  AC, Miller  M,  et al.  Environmental contamination as a risk factor for intra-household Staphylococcus aureus transmission.  PLoS One. 2012;7(11):e49900.PubMedGoogle ScholarCrossref
5.
Uhlemann  AC, Dordel  J, Knox  JR,  et al.  Molecular tracing of the emergence, diversification, and transmission of S aureus sequence type 8 in a New York community.  Proc Natl Acad Sci U S A. 2014;111(18):6738-6743.PubMedGoogle ScholarCrossref
6.
Davis  MF, Iverson  SA, Baron  P,  et al.  Household transmission of methicillin-resistant Staphylococcus aureus and other staphylococci.  Lancet Infect Dis. 2012;12(9):703-716.PubMedGoogle ScholarCrossref
7.
Lautenbach  E, Tolomeo  P, Nachamkin  I, Hu  B, Zaoutis  TE.  The impact of household transmission on duration of outpatient colonization with methicillin-resistant Staphylococcus aureus.  Epidemiol Infect. 2010;138(5):683-685.PubMedGoogle ScholarCrossref
8.
Eells  SJ, David  MZ, Taylor  A,  et al.  Persistent environmental contamination with USA300 methicillin-resistant Staphylococcus aureus and other pathogenic strain types in households with S aureus skin infections.  Infect Control Hosp Epidemiol. 2014;35(11):1373-1382.PubMedGoogle ScholarCrossref
9.
Knox  J, Uhlemann  AC, Lowy  FD.  Staphylococcus aureus infections: transmission within households and the community.  Trends Microbiol. 2015;23(7):437-444.PubMedGoogle ScholarCrossref
10.
Macal  CM, North  MJ, Collier  N,  et al.  Modeling the transmission of community-associated methicillin-resistant Staphylococcus aureus: a dynamic agent-based simulation.  J Transl Med. 2014;12:124.PubMedGoogle ScholarCrossref
11.
Alam  MT, Read  TD, Petit  RA  III,  et al.  Transmission and microevolution of USA300 MRSA in US households: evidence from whole-genome sequencing.  MBio. 2015;6(2):e00054.PubMedGoogle ScholarCrossref
12.
Jones  TF, Creech  CB, Erwin  P, Baird  SG, Woron  AM, Schaffner  W.  Family outbreaks of invasive community-associated methicillin-resistant Staphylococcus aureus infection.  Clin Infect Dis. 2006;42(9):e76-e78.PubMedGoogle ScholarCrossref
13.
Cook  HA, Furuya  EY, Larson  E, Vasquez  G, Lowy  FD.  Heterosexual transmission of community-associated methicillin-resistant Staphylococcus aureus.  Clin Infect Dis. 2007;44(3):410-413.PubMedGoogle ScholarCrossref
14.
Zafar  U, Johnson  LB, Hanna  M,  et al.  Prevalence of nasal colonization among patients with community-associated methicillin-resistant Staphylococcus aureus infection and their household contacts.  Infect Control Hosp Epidemiol. 2007;28(8):966-969.PubMedGoogle Scholar
15.
Johansson  PJ, Gustafsson  EB, Ringberg  H.  High prevalence of MRSA in household contacts.  Scand J Infect Dis. 2007;39(9):764-768.PubMedGoogle ScholarCrossref
16.
Ho  PL, Cheung  C, Mak  GC,  et al.  Molecular epidemiology and household transmission of community-associated methicillin-resistant Staphylococcus aureus in Hong Kong.  Diagn Microbiol Infect Dis. 2007;57(2):145-151.PubMedGoogle ScholarCrossref
17.
Stone  A, Quittell  L, Zhou  J,  et al.  Staphylococcus aureus nasal colonization among pediatric cystic fibrosis patients and their household contacts.  Pediatr Infect Dis J. 2009;28(10):895-899.PubMedGoogle ScholarCrossref
18.
Huang  YC, Ho  CF, Chen  CJ, Su  LH, Lin  TY.  Nasal carriage of methicillin-resistant Staphylococcus aureus in household contacts of children with community-acquired diseases in Taiwan.  Pediatr Infect Dis J. 2007;26(11):1066-1068.PubMedGoogle ScholarCrossref
19.
Busato  CR, Carneiro Leão  MT, Gabardo  J.  Staphylococcus aureus nasopharyngeal carriage rates and antimicrobial susceptibility patterns among health care workers and their household contacts.  Braz J Infect Dis. 1998;2(2):78-84.PubMedGoogle Scholar
20.
Wagenvoort  JH, Toenbreker  HM, Nurmohamed  A, Davies  BI.  Transmission of methicillin-resistant Staphylococcus aureus within a household.  Eur J Clin Microbiol Infect Dis. 1997;16(5):399-400.PubMedGoogle ScholarCrossref
21.
Miller  LG, Eells  SJ, David  MZ,  et al.  Staphylococcus aureus skin infection recurrences among household members: an examination of host, behavioral, and pathogen-level predictors.  Clin Infect Dis. 2015;60(5):753-763.PubMedGoogle ScholarCrossref
22.
Huijsdens  XW, van Santen-Verheuvel  MG, Spalburg  E,  et al.  Multiple cases of familial transmission of community-acquired methicillin-resistant Staphylococcus aureus.  J Clin Microbiol. 2006;44(8):2994-2996.PubMedGoogle ScholarCrossref
23.
L’Hériteau  F, Lucet  JC, Scanvic  A, Bouvet  E.  Community-acquired methicillin-resistant Staphylococcus aureus and familial transmission.  JAMA. 1999;282(11):1038-1039.PubMedGoogle ScholarCrossref
24.
Yamamoto  T, Takano  T, Yabe  S,  et al.  Super-sticky familial infections caused by Panton-Valentine leukocidin-positive ST22 community-acquired methicillin-resistant Staphylococcus aureus in Japan.  J Infect Chemother. 2012;18(2):187-198.PubMedGoogle ScholarCrossref
25.
Yabe  S, Takano  T, Higuchi  W, Mimura  S, Kurosawa  Y, Yamamoto  T.  Spread of the community-acquired methicillin-resistant Staphylococcus aureus USA300 clone among family members in Japan.  J Infect Chemother. 2010;16(5):372-374.PubMedGoogle ScholarCrossref
26.
Amir  NH, Rossney  AS, Veale  J, O’Connor  M, Fitzpatrick  F, Humphreys  H.  Spread of community-acquired meticillin-resistant Staphylococcus aureus skin and soft-tissue infection within a family: implications for antibiotic therapy and prevention.  J Med Microbiol. 2010;59(pt 4):489-492.PubMedGoogle ScholarCrossref
27.
Dancer  SJ.  The role of environmental cleaning in the control of hospital-acquired infection.  J Hosp Infect. 2009;73(4):378-385.PubMedGoogle ScholarCrossref
28.
Dancer  SJ.  Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning.  Lancet Infect Dis. 2008;8(2):101-113.PubMedGoogle ScholarCrossref
29.
Gwizdala  RA, Miller  M, Bhat  M,  et al.  Staphylococcus aureus colonization and infection among drug users: identification of hidden networks.  Am J Public Health. 2011;101(7):1268-1276.PubMedGoogle ScholarCrossref
30.
Miko  BA, Herzig  CT, Mukherjee  DV,  et al.  Is environmental contamination associated with Staphylococcus aureus clinical infection in maximum security prisons?  Infect Control Hosp Epidemiol. 2013;34(5):540-542.PubMedGoogle ScholarCrossref
31.
Fritz  SA, Hogan  PG, Singh  LN,  et al.  Contamination of environmental surfaces with Staphylococcus aureus in households with children infected with methicillin-resistant S aureus.  JAMA Pediatr. 2014;168(11):1030-1038.PubMedGoogle ScholarCrossref
32.
Miller  LG, Diep  BA.  Clinical practice: colonization, fomites, and virulence: rethinking the pathogenesis of community-associated methicillin-resistant Staphylococcus aureus infection.  Clin Infect Dis. 2008;46(5):752-760.PubMedGoogle ScholarCrossref
33.
Miller  LG, Tan  J, Eells  SJ, Benitez  E, Radner  AB.  Prospective investigation of nasal mupirocin, hexachlorophene body wash, and systemic antibiotics for prevention of recurrent community-associated methicillin-resistant Staphylococcus aureus infections.  Antimicrob Agents Chemother. 2012;56(2):1084-1086.PubMedGoogle ScholarCrossref
34.
Fritz  SA, Hogan  PG, Hayek  G,  et al.  Household versus individual approaches to eradication of community-associated Staphylococcus aureus in children: a randomized trial.  Clin Infect Dis. 2012;54(6):743-751.PubMedGoogle ScholarCrossref
35.
Fritz  SA, Hogan  PG, Camins  BC,  et al.  Mupirocin and chlorhexidine resistance in Staphylococcus aureus in patients with community-onset skin and soft tissue infections.  Antimicrob Agents Chemother. 2013;57(1):559-568.PubMedGoogle ScholarCrossref
36.
Kaplan  SL, Forbes  A, Hammerman  WA,  et al.  Randomized trial of “bleach baths” plus routine hygienic measures vs routine hygienic measures alone for prevention of recurrent infections.  Clin Infect Dis. 2014;58(5):679-682.PubMedGoogle ScholarCrossref
37.
Kohler  P, Bregenzer-Witteck  A, Rettenmund  G, Otterbech  S, Schlegel  M.  MRSA decolonization: success rate, risk factors for failure and optimal duration of follow-up.  Infection. 2013;41(1):33-40.PubMedGoogle ScholarCrossref
38.
Shopsin  B, Gomez  M, Montgomery  SO,  et al.  Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains.  J Clin Microbiol. 1999;37(11):3556-3563.PubMedGoogle Scholar
39.
Harmsen  D, Claus  H, Witte  W,  et al.  Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management.  J Clin Microbiol. 2003;41(12):5442-5448.PubMedGoogle ScholarCrossref
40.
Milheiriço  C, Oliveira  DC, de Lencastre  H.  Update to the multiplex PCR strategy for assignment of mec element types in Staphylococcus aureus.  Antimicrob Agents Chemother. 2007;51(9):3374-3377.PubMedGoogle ScholarCrossref
41.
Milheiriço  C, Oliveira  DC, de Lencastre  H.  Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: “SCCmec IV multiplex”.  J Antimicrob Chemother. 2007;60(1):42-48.PubMedGoogle ScholarCrossref
42.
Blanc  DS, Petignat  C, Moreillon  P, Wenger  A, Bille  J, Francioli  P.  Quantitative antibiogram as a typing method for the prospective epidemiological surveillance and control of MRSA: comparison with molecular typing.  Infect Control Hosp Epidemiol. 1996;17(10):654-659.PubMedGoogle ScholarCrossref
43.
Younger  JJ, Christensen  GD, Bartley  DL, Simmons  JC, Barrett  FF.  Coagulase-negative staphylococci isolated from cerebrospinal fluid shunts: importance of slime production, species identification, and shunt removal to clinical outcome.  J Infect Dis. 1987;156(4):548-554.PubMedGoogle ScholarCrossref
44.
Montesinos  I, Salido  E, Delgado  T, Cuervo  M, Sierra  A.  Epidemiologic genotyping of methicillin-resistant Staphylococcus aureus by pulsed-field gel electrophoresis at a university hospital and comparison with antibiotyping and protein A and coagulase gene polymorphisms.  J Clin Microbiol. 2002;40(6):2119-2125.PubMedGoogle ScholarCrossref
45.
Omar  NY, Ali  HA, Harfoush  RA, El Khayat  EH.  Molecular typing of methicillin resistant Staphylococcus aureus clinical isolates on the basis of protein A and coagulase gene polymorphisms.  Int J Microbiol. 2014;2014:650328.PubMedGoogle ScholarCrossref
46.
Mehndiratta  PL, Bhalla  P.  Typing of methicillin resistant Staphylococcus aureus: a technical review.  Indian J Med Microbiol. 2012;30(1):16-23.PubMedGoogle ScholarCrossref
47.
McDougal  LK, Steward  CD, Killgore  GE, Chaitram  JM, McAllister  SK, Tenover  FC.  Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database.  J Clin Microbiol. 2003;41(11):5113-5120.PubMedGoogle ScholarCrossref
48.
Miller  LG, Eells  SJ, Taylor  AR,  et al.  Staphylococcus aureus colonization among household contacts of patients with skin infections: risk factors, strain discordance, and complex ecology.  Clin Infect Dis. 2012;54(11):1523-1535.PubMedGoogle ScholarCrossref
49.
Knox  J, Van Rijen  M, Uhlemann  AC,  et al.  Community-associated methicillin-resistant Staphylococcus aureus transmission in households of infected cases: a pooled analysis of primary data from three studies across international settings.  Epidemiol Infect. 2015;143(2):354-365.PubMedGoogle ScholarCrossref
50.
Harbarth  S, Liassine  N, Dharan  S, Herrault  P, Auckenthaler  R, Pittet  D.  Risk factors for persistent carriage of methicillin-resistant Staphylococcus aureus.  Clin Infect Dis. 2000;31(6):1380-1385.PubMedGoogle ScholarCrossref
51.
Miller  M, Cook  HA, Furuya  EY,  et al.  Staphylococcus aureus in the community: colonization versus infection.  PLoS One. 2009;4(8):e6708.PubMedGoogle ScholarCrossref
52.
Lee  CJ, Sankaran  S, Mukherjee  DV,  et al.  Staphylococcus aureus oropharyngeal carriage in a prison population.  Clin Infect Dis. 2011;52(6):775-778.PubMedGoogle ScholarCrossref
53.
Miko  BA, Uhlemann  AC, Gelman  A,  et al.  High prevalence of colonization with Staphylococcus aureus clone USA300 at multiple body sites among sexually transmitted disease clinic patients: an unrecognized reservoir.  Microbes Infect. 2012;14(12):1040-1043.PubMedGoogle ScholarCrossref
54.
Peters  PJ, Brooks  JT, Limbago  B,  et al.  Methicillin-resistant Staphylococcus aureus colonization in HIV-infected outpatients is common and detection is enhanced by groin culture.  Epidemiol Infect. 2011;139(7):998-1008.PubMedGoogle ScholarCrossref
55.
Eveillard  M, de Lassence  A, Lancien  E, Barnaud  G, Ricard  JD, Joly-Guillou  ML.  Evaluation of a strategy of screening multiple anatomical sites for methicillin-resistant Staphylococcus aureus at admission to a teaching hospital.  Infect Control Hosp Epidemiol. 2006;27(2):181-184.PubMedGoogle ScholarCrossref
56.
Mermel  LA, Cartony  JM, Covington  P, Maxey  G, Morse  D.  Methicillin-resistant Staphylococcus aureus colonization at different body sites: a prospective, quantitative analysis.  J Clin Microbiol. 2011;49(3):1119-1121.PubMedGoogle ScholarCrossref
57.
Lautenbach  E, Nachamkin  I, Hu  B,  et al.  Surveillance cultures for detection of methicillin-resistant Staphylococcus aureus: diagnostic yield of anatomic sites and comparison of provider- and patient-collected samples.  Infect Control Hosp Epidemiol. 2009;30(4):380-382.PubMedGoogle ScholarCrossref
58.
Cluzet  VC, Gerber  JS, Nachamkin  I,  et al.  Duration of colonization and determinants of earlier clearance of colonization with methicillin-resistant Staphylococcus aureus Clin Infect Dis. 2015;60(10):1489-1496.PubMedGoogle Scholar
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