Spread of Methicillin‐Resistant Staphylococcus aureus (MRSA) Among Household Contacts ofIndividuals with Nosocomially Acquired MRSA • Author(s): David P. Calfee , MD, MS; Lisa J. Durbin , BS, MT; Teresa P. Germanson , MPH,PhD; Denise M. Toney , PhD; Elise B. Smith , MT (ASCP); Barry M. Farr , MD, MScSource: Infection Control and Hospital Epidemiology, Vol. 24, No. 6 (June 2003), pp. 422-426Published by: The University of Chicago Press on behalf of The Society for Healthcare Epidemiologyof AmericaStable URL: http://www.jstor.org/stable/10.1086/502225 .

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422 INFECTION CONTROL AND HOSPITAL EPIDEMIOLOGY June 2003

SPREAD OF METHICILLIN-RESISTANT STAPHYLOCOCCUSAUREUS (MRSA) AMONG HOUSEHOLD CONTACTS OF

INDIVIDUALS WITH NOSOCOMIALLY ACQUIRED MRSA

David P. Calfee, MD, MS; Lisa J. Durbin, BS, MT; Teresa P. Germanson, MPH, PhD; Denise M. Toney, PhD;Elise B. Smith, MT (ASCP); Barry M. Farr, MD, MSc

Although methicillin-resistant Staphylococcusaureus (MRSA) is classically considered a nosocomialpathogen, reports of its acquisition in the communityhave become increasingly common during the pastdecade. The emergence of this organism in that settingcould be the result of either primary acquisition of resis-tance among staphylococci in the community or dissemi-nation of nosocomial strains of MRSA from the health-care setting into the community. Although many havesuggested that the former explanation is most likely,1-5 ithas been recognized for decades that S. aureus is sharedamong household contacts.6 More recently, transmissionof MRSA among family and community contacts has alsobeen described.7-16 This suggests that the spread ofMRSA from patients who become colonized while receiv-ing health care to their contacts within the communitymay play a role in the epidemiology of MRSA in the com-munity. However, the frequency with which this type oftransmission occurs is unknown because investigation ofthe MRSA colonization status of individuals with knowncontact with MRSA-colonized patients usually occursonly in the setting of outbreaks of MRSA infection. Toexplore the epidemiology of MRSA among the personalcontacts of MRSA-colonized individuals, the MRSA colo-nization status of the household and community contacts

of patients undergoing MRSA eradication at a universityhospital was reviewed.

METHODS

At the University of Virginia Health System, con-tact/droplet precautions as defined by the Centers forDisease Control and Prevention (ie, gown, gloves, andmask) have been used during the care of all patientsknown to be colonized or infected with MRSA.17

Eradication of MRSA colonization is not required, but insome circumstances (eg, for the psychological benefit ofthe patient, for prevention of infection, or to facilitatetransfer to a nursing or rehabilitation facility) patients andtheir treating physicians request eradication of the organ-ism. Eradication protocols are individualized for eachpatient based on the extent of colonization, the antimicro-bial susceptibility of the colonizing strain of MRSA, andany coexisting medical conditions that could influence theresponse to eradication attempts or increase the risk ofadverse effects from specific treatments.

In general, MRSA eradication attempts have includ-ed topical use of intranasal mupirocin (if the strain is sus-ceptible), daily chlorhexidine baths, a combination of sys-temic antibacterial agents including rifampin whenrequired because of tissue or mucosal colonization at sites

Drs. Calfee and Farr and Ms. Durbin are from the Department of Internal Medicine, University of Virginia Health System, Charlottesville,Virginia. Dr. Germanson is from Germanson and Associates, LLC, Charlottesville, Virginia. Dr. Toney and Ms. Smith are from the Commonwealthof Virginia Department of General Services, Division of Consolidated Laboratory Services, Richmond, Virginia.

Address reprint requests to David P. Calfee, MD, MS, Box 801337, University of Virginia Health System, Charlottesville, VA 22908.Presented in part at the 11th Annual Scientific Meeting of the Society for Healthcare Epidemiology of America; April 1-3, 2001; Toronto,

Ontario, Canada.

OBJECTIVE: To determine the frequency with whichmethicillin-resistant Staphylococcus aureus (MRSA) is spreadfrom colonized or infected patients to their household and com-munity contacts.

DESIGN: Retrospective cohort study.SETTING: University hospital.PARTICIPANTS: Household and community contacts of

MRSA-colonized or -infected patients for whom MRSA screeningcultures were performed.

RESULTS: MRSA was isolated from 25 (14.5%) of 172individuals. Among the contacts of index patients who had at

least one MRSA-colonized contact, those with close contact to theindex patient were 7.5 times more likely to be colonized (53% vs7%; 95% confidence interval, 1.1 to 50.3; P = .002). An analysis ofantimicrobial susceptibility and DNA fingerprint patterns sug-gested person-to-person spread.

CONCLUSIONS: MRSA colonization occurs frequentlyamong household and community contacts of patients with noso-comially acquired MRSA, suggesting that transmission of noso-comially acquired MRSA outside of the healthcare setting may bea substantial source of MRSA colonization and infection in thecommunity (Infect Control Hosp Epidemiol 2003;24:422-426).

ABSTRACT

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Vol. 24 No. 6 MRSA IN HOUSEHOLD CONTACTS 423

other than the nose (if the strain is susceptible), disinfec-tion of fomites, exchange of foreign bodies if present andif possible, and screening cultures of close contacts. Thepatient or the treating physician identifies individuals whoare considered to be “close contacts.” Typically theseinclude members of the patient’s household and otherindividuals who are thought to have substantial contactwith the patient. Screening cultures are performed so thatcolonized contacts can undergo simultaneous eradicationtherapy to reduce the possibility of either apparent failureof eradication or relapse of MRSA colonization in theindex patient following successful eradication (ie, due totransmission of the organism back to the patient from thecolonized household contact).

Specimens for screening cultures were routinelyobtained from the anterior nares of household contacts.The groin, axillae, perirectal area, and sites of non-intactskin were additional sites that were frequently cultured.Specimens were obtained using dry, sterile, cotton-tippedswabs. The swabs were directly plated onto trypticase soyagar with 5% sheep blood and mannitol salt agar (BBL,Cockeysville, MD). Colonies of S. aureus were identifiedby standard microbiologic methods.18 The presence orabsence of resistance to methicillin was determined usingthe disk-diffusion method according to standards setforth by the National Committee for Clinical LaboratoryStandards.19 Oxacillin salt agar screening plates were alsoused in the identification of MRSA.20 All MRSA isolateswere also tested for susceptibility to vancomycin,rifampin, mupirocin, trimethoprim/sulfamethoxazole,tetracycline, ciprofloxacin, clindamycin, and ery-thromycin using the disk-diffusion method.19 All screen-ing cultures were performed and all documentation wasmaintained in the epidemiology laboratory of the hospital.

The results of screening cultures performed forcontacts of MRSA-colonized patients undergoing eradica-tion therapy between June 1992 and November 2000 werereviewed. The number of cultures performed, the sitefrom which each specimen for culture was obtained, andthe results of all cultures were noted. The type of rela-tionship between the contact and the index patient wasnoted for all contact–index patient pairs. Individualswhose relationship with the index patient was classified asspouse, parent, child, or “caregiver” were considered tohave close contact with the index patient. Other individu-als (eg, roommates, siblings, and friends) were consid-ered to have casual contact with the index patient. Strainrelatedness between each index patient and his or herMRSA-colonized contacts was initially evaluated by com-paring the qualitative antimicrobial susceptibility patternsof the MRSA isolates.

Further evaluation of strain relatedness was per-formed using pulsed-field gel electrophoresis (PFGE).The protocol for preparation of chromosomal DNA wasmodified from that described by Bannerman et al.21

Cultures grown in brain–heart infusion broth at 37°Cwere treated with 4 µg of recombinant lysostaphin dis-solved in 20 mM of sodium acetate (pH 4.5) (Sigma, St.

Louis, MO). The lysostaphin–cell suspension mixture wascombined with 1.8% Seakem Gold Agarose (BioWhittaker,Rockland, ME) and dispensed into plug molds to solidify.Plugs were treated with cell lysis buffer for 4 to 5 hours at37°C without agitation followed by SmaI (30 U) restric-tion enzyme digestion. Electrophoresis was performedfor 18 hours at 14°C in a CHEF Mapper (Bio-Rad,Hercules, CA) using switch times of 5 and 40 seconds.Gels were stained with ethidium bromide and images cap-tured using Multi-Analyst software (Bio-Rad). Fingerprintpatterns were analyzed using GelCompar software (ver-sion 4.2; Applied Maths, Kortrijk, Belgium).Interpretation of PFGE patterns was performed asdescribed by Tenover et al.22

A retrospective review of the medical records ofeach of the index patients was performed to allow charac-terization of these individuals. Data related to underlyingmedical conditions, performance status, frequency andduration of hospitalization at the study hospital during the12 months prior to the date on which contacts underwentculture, and the location of each index patient at the timeeradication was attempted were extracted from the med-ical record. Performance status was assessed using theKarnofsky performance status scale.23

All data were entered into an electronic database(Microsoft Access 97; Microsoft, Redmond, WA). The pro-portion of contacts colonized with MRSA was calculatedfor all contacts, close contacts, and casual contacts.Continuous variables were compared using the Wilcoxonrank sum test. Proportions were compared using the chi-square test or Fisher’s exact test, if expected cell sizeswere small. P values of .05 or less were considered statis-tically significant. Statistical analyses were performedusing Epi-Info (Centers for Disease Control andPrevention, Atlanta, GA) and S-Plus 2000 (Mathsoft,Seattle, WA) software. The study protocol was reviewedand approved by the University of Virginia HumanInvestigation Committee.

RESULTS

Between June 1992 and November 2000, screeningcultures for MRSA were performed for 172 personal con-tacts of 88 index patients colonized with MRSA.Characteristics of the 88 index patients are presented inthe table. MRSA was initially isolated from a clinical spec-imen in 58 (66%) of the cases and from a surveillanceculture in 26 (30%) of the cases. Four cases had been iden-tified as colonized with MRSA at another healthcare facil-ity. The median time between detection of MRSA colo-nization and acquisition of specimens for surveillancecultures from contacts was 37.5 days (range, 3 to 930days). Sixty (68%) of the index patients had returnedhome before cultures were performed for their contacts.Fifty-three (60%) of the index patients were living at homeat the time their contacts underwent culture.

Twenty-one (24%) of the index patients had at leastone MRSA-colonized contact. A comparison of indexpatients with MRSA-colonized contacts with index

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424 INFECTION CONTROL AND HOSPITAL EPIDEMIOLOGY June 2003

patients without MRSA-colonized contacts is presented inthe table. MRSA was isolated from 25 (14.5%) of the 172personal contacts: 24 (18.5%) of 130 of those with closecontact versus 1 (2.4%) of 42 of those with only casual con-tact. Among the household contacts of the 21 indexpatients with at least one MRSA-colonized contact, 24(53%) of 45 with close contact as compared with 1 (7%) of14 with casual contact were colonized with MRSA (rela-tive risk, 7.5; 95% confidence interval, 1.1 to 50.3; P =.002). No clinical data from household contacts were avail-able. Among the 60 index patients who had returned totheir homes while known to be colonized with MRSA, 19(32%) had MRSA-colonized contacts as compared withonly 2 (7%) of the 28 who had not returned to their homes(relative risk, 4.43; 95% confidence interval, 1.11 to 17.7;P = .012). Patients with contacts who were colonized were6 times more likely to have returned home prior to thetime when cultures were performed for their identifiedcontacts. These case-patients also had significantly fewerdays of hospitalization in the year preceding the eradica-tion attempt.

Among the 25 MRSA-colonized contacts, the quali-tative antimicrobial susceptibility patterns of 19 (76%)were identical to that of the index patient to whom eachcontact had been exposed. The antimicrobial susceptibili-ty patterns from six MRSA-colonized contacts were notidentical to that of the index patient. The antibiotic sus-ceptibility patterns differed by one drug in five instancesand by two drugs in a single instance. Four index patientshad two MRSA-colonized contacts and in all instances theMRSA isolates from the two contacts had the same antimi-crobial susceptibility pattern as that of the index patient.Assuming a binomial distribution, we calculated the prob-ability that at least 19 (76%) of 25 household contacts’MRSA antibiograms would have matched their respectiveindex patient’s antibiogram exactly by chance alone.Because 19 different antibiograms occurred among the 21index patients and their 25 contacts, we assumed that theprobability of one household contact’s antibiogram hap-pening by chance alone to match the respective indexpatient’s antibiogram would be 1 in 19. The probability offinding by chance alone that 19 of 25 contacts’ antibi-ograms exactly matched that of the index patient in theirhousehold was calculated to be less than 10-15.

MRSA isolates from 9 index patients and their 11MRSA-colonized contacts were available for additionalanalysis by PFGE. Qualitative antibiograms were identicalin each of these case–contact groups. One index patientappeared to have two different strains of MRSA based onqualitative antibiogram and morphologic appearance. Thetwo isolates were available for testing. Thus, 21 isolateswere evaluated by PFGE. A total of eight unique DNA fin-gerprint patterns were identified. There were two otherpatterns identified: one varied by a single band from oneof the eight unique patterns and one differed from a sec-ond unique pattern by two bands.

The MRSA isolates from the contacts of eight ofnine index patients had DNA fingerprint patterns identical

TABLECHARACTERISTICS OF INDEX PATIENTS COLONIZED WITH

METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS

Patients With Patients WithoutColonized Colonized

Characteristic Contacts (n = 21) Contacts (n = 67) P

Male 12 (57%) 35 (52%) .70Age, y

Median (range) 42 (3–98) 51 (1–86) .89Mean 49.8 49.1

Performance statusMedian (range) 70 (40–90) 60 (20–100) .31Mean 67.1 60.7

No. of hospitalizationsMedian (range) 1 (0–3) 1 (0–6) .32Mean 1.1 1.6

No. of hospital daysMedian (range) 10 (0–104) 25 (0–185) .02Mean 16.3 33.4

Location at time ofcontact cultureHome 19 (90%) 34 (51%) .001Hospital 0 20 (30%)Nursing facility 0 2 (3%)Rehabilitation facility 2 (10%) 11 (16%)

Known admission to 8 (38%) 31 (46%) .51another health-care facility

History of MRSA 13 (62%) 31 (46%) .21infection

Lived at home while 19 (90%) 41 (61%) .01known to be MRSAcolonized

Diabetes mellitus 3 (14%) 12 (18%) .7Requiring insulin 1 (5%) 6 (9%)

Chronic renal disease 3 (14%) 10 (15%) .94Dialysis dependent 2 (10%) 5 (7%)

Coronary artery disease 4 (19%) 15 (22%) .74Congestive heart failure 3 (14%) 7 (10%) .63Hypertension 10 (48%) 23 (34%) .27Peripheral vascular 2 (10%) 9 (13%) .64

diseaseChronic lung disease 1 (5%) 10 (15%) .22Chronic skin disease 6 (29%) 16 (24%) .66

or ulcersParalysis 5 (24%) 22 (33%) .43Dementia 3 (14%) 8 (12%) .78Solid organ malignancy 2 (10%) 3 (4%) .38Hematologic malignancy 0 (0) 1 (1%) .57Solid organ transplant 0 (0) 4 (6%) .25Stem cell transplant 0 (0) 1 (1%) .57Indwelling bladder 3 (14%) 5 (7%) .34

catheterFeeding tube 6 (29%) 15 (22%) .56

MRSA = methicillin-resistant Staphylococcus aureus.

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Vol. 24 No. 6 MRSA IN HOUSEHOLD CONTACTS 425

to those of the MRSA isolated from the index patient towhom each had been exposed (Figure). The PFGE pat-terns of the MRSA isolates from the final case–contactpair, which had been collected 2 months apart, differed byonly two bands, suggesting that these were also closelyrelated. The two isolates submitted from a single indexpatient had unique DNA fingerprint patterns. The MRSAstrains isolated from the colonized contacts of this patientwere identical to one of the index patient’s strains.

DISCUSSION

This review identified MRSA colonization among asubstantial proportion of household and community con-tacts of patients with healthcare-associated MRSA.Although molecular typing methods could not be per-formed to determine the strain relatedness of MRSA with-in all of the index case–contact groups in this study, PFGEanalysis of 9 (43%) of the case–contact groups found thatthe MRSA isolated from the contact was either identical to(8) or closely related to (1) that of the index patient. Thisstrongly supports the hypothesis that cross-transmissionof a single strain between the index patient and his or herhousehold contact(s) had occurred in each instance.

There are several limitations to this study. First,molecular typing could not be performed for all case–con-tact pairs because not all specimens had been saved.Second, it was assumed that the MRSA-colonized house-hold contacts acquired the organism from the “indexpatient.” However, the possibility that one or more of theindex patients acquired MRSA from a household contactexists. Nevertheless, the results of this study indicate thatMRSA transmission among household contacts occurs.Third, because this was a retrospective review of clinicaldata, the index patients were not a randomly selectedsample of patients colonized or infected with MRSA, con-tacts were not identified using specific criteria, and littledata regarding the household contacts were available.Future prospective studies in this area would be of valuein determining whether these results can be generalizedto other populations.

The prevalence of MRSA among members of thecommunity has been evaluated. In one study of 3,525 indi-viduals without healthcare contacts or known exposure toMRSA-colonized individuals, the prevalence of MRSA col-onization was only 0.2%.24 This finding has been corrobo-rated by several other studies including a study that eval-uated the prevalence of MRSA among healthy childrenand their guardians attending outpatient clinics in NewYork25 and a community-based study of the urban poor inSan Francisco, California.26 Although differences in studymethods prevent direct comparison of those results withthe results of the current study, it appears that householdcontact with a MRSA-colonized hospital patient who hasbeen discharged home is an important risk factor forMRSA colonization among healthy members of the com-munity. Additional studies to further investigate the fac-tors associated with and the outcomes related to trans-mission of MRSA within such households are needed.

Identification of MRSA colonization in almost 15% ofthe household contacts of MRSA-colonized patients evalu-ated in this study would appear to have at least two impor-tant implications. First, in terms of the index patient, failureto identify colonization of household contacts may beresponsible for persistent colonization or for apparent pri-mary “failure” of or “relapse” following eradication therapydue to “ping-pong transmission” from a colonized house-hold contact back to the index patient. Most publishedstudies of eradication of S. aureus colonization have neitherassessed nor dealt with colonization of family members.

The second possible implication is of importance ona much larger scale. This relates to the issue of commu-nity acquisition of MRSA. Several studies have describedbeta-lactam monoresistance among MRSA strains origi-nating within the community.4,8,27-29 This difference inantimicrobial susceptibility patterns, as compared withthe typical multidrug-resistant patterns of healthcare-associated strains, has been explained by the presence ofa novel (ie, type IV) staphylococcal cassette chromosomemec (SCCmec) that, unlike SCCmec types I to III found inmost healthcare-associated MRSA strains, does not con-tain genes that confer resistance to other classes ofantimicrobials.30,31 Large, population-based studies havenot yet been performed to determine the proportion of“community-acquired” MRSA strains that contain thisgenetic element (ie, type IV SCCmec) and most studies ofcommunity-acquired MRSA have not reported antibioticsusceptibility profiles for these organisms.

The results of the current study suggest that trans-mission of MRSA to household contacts of patients withnosocomially acquired MRSA is another way in which indi-viduals without typical healthcare-associated risk factorscan acquire MRSA. These results imply that failure to con-trol MRSA within the healthcare system is likely to lead tofurther dissemination of MRSA into the community.

FIGURE. Pulsed-field gel electrophoresis analysis of methicillin-resistantStaphylococcus aureus (MRSA) strains isolated from individuals with noso-comially acquired MRSA and their household contacts. Identical elec-trophoresis patterns can be seen for three case–contact pairs (lanes 3 and4, 5 and 6, and 9 and 10). Lane 11 contains the isolate from a fourthindex patient, which was identical to those of the case–contact pair inlanes 3 and 4. All other lanes contain S. aureus control strains used asmarkers used for pattern analysis.

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426 INFECTION CONTROL AND HOSPITAL EPIDEMIOLOGY June 2003

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