Association of methicillin-resistant Staphylococcus aureus (MRSA) colonization with high-risk sexual behaviors in persons infected with human immunodeficiency virus (HIV)

Nancy F Crum-Cianflone, Aladdin H Shadyab, Amy Weintrob, Duane R Hospenthal, Tahaniyat Lalani, Gary Collins, Alona Mask, Katrin Mende, Stephanie K Brodine, Brian K Agan, Infectious Disease Clinical Research Program HIV Working Group, Nancy F Crum-Cianflone, Aladdin H Shadyab, Amy Weintrob, Duane R Hospenthal, Tahaniyat Lalani, Gary Collins, Alona Mask, Katrin Mende, Stephanie K Brodine, Brian K Agan, Infectious Disease Clinical Research Program HIV Working Group

Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) infections are an important cause of morbidity, especially among human immunodeficiency virus (HIV)-infected persons. Since an increasing number of MRSA skin and soft tissue infections involve the perigenital areas, some have suggested that these infections may be sexually transmitted. We performed a cross-sectional study among HIV-infected adults from 4 geographically diverse United States military HIV clinics to determine the prevalence of and the factors (including sexual practices) associated with MRSA colonization. Swabs were collected from the nares, throat, axillae, groin area, and perirectal area for S. aureus colonization. Data on sociodemographic characteristics, medical conditions, and sexual history were collected. Multivariate logistic regression models evaluated factors associated with carriage. We studied 550 HIV-infected adults with a median age of 42 years; 93% were male; and race/ethnicity was white for 46%, African American for 35%, and other for 19%. Median CD4 count was 529 cells/mm, 11% had a history of a MRSA infection, and 21% had a sexually transmitted infection within the last year, including 8% with syphilis. One hundred eighty (33%) were colonized with S. aureus and 22 (4%) with MRSA. The most common location for carriage was the nares, followed by the perigenital area (groin or perirectal area). Factors associated with MRSA carriage in the multivariate analyses included a sexually transmitted infection in the last year (odds ratio [OR], 4.2; p<0.01), history of MRSA infection (OR, 9.4; p<0.01), and African American compared with white race/ethnicity (OR, 3.5; p=0.01). In separate multivariate models, syphilis, nongonococcal urethritis, and public bath use were also associated with MRSA carriage (all p<0.01). In conclusion, a history of recent sexually transmitted infections, including syphilis and urethritis, was associated with MRSA carriage. These data suggest that high-risk sexual activities may play a role in MRSA transmission.

References

    1. Acton DS, Plat-Sinnige MJ, van Wamel W, de Groot N, van Belkum A. Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact? Eur J Clin Microbiol Infect Dis. 2009;28:115-127.
    1. Antoniou T, Devlin R, Gough K, Mulvey M, Katz KC, Zehtabchi M, Polsky J, Tilley D, Brunetta J, Arbess G, Guiang C, Chang B, Kovacs C, Ghavam-Rassoul A, Cavacuiti C, Corneslon B, Berger P, Loutfy MR. Prevalence of community-associated methicillin-resistant Staphylococcus aureus colonization in men who have sex with men. Int J STD AIDS. 2009;20:180-183.
    1. Brown DF, Edwards DI, Hawkey PM, Morrison D, Ridgway GL, Towner KJ, Wren MW. Joint Working Party of the British Society for Antimicrobial Chemotherapy; Hospital Infection Society; Infection Control Nurses Association. Guidelines for the laboratory diagnosis and susceptibility testing of methicillin-resistant Staphylococcus aureus (MRSA). J Antimicrob Chemother. 2005;56:1000-1018.
    1. Cenizal MJ, Hardy RD, Anderson M, Katz K, Skiest DJ. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization in HIV-infected ambulatory patients. J Acquir Immune Defic Syndr. 2008;48:567-571.
    1. Centers for Disease Control and Prevention. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR Recomm Rep. 1992;41:1-19.
    1. Centers for Disease Control and Prevention. Public health dispatch: outbreaks of community-associated methicillin-resistant Staphylococcus aureus skin infections-Los Angeles County, California, 2002-2003. JAMA. 2003;289:1377.
    1. Chacko J, Kuruvila M, Bhat GK. Factors affecting the nasal carriage of methicillin-resistant Staphylococcus aureus in human immunodeficiency virus-infected patients. Indian J Med Microbiol. 2009;27:146-148.
    1. Cook HA, Furuya Y, Larson E, Vasquez G, Lowy FD. Heterosexual transmission of community-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 2007;44:410-413.
    1. Crum-Cianflone NF, Burgi AA, Hale BR. Increasing rates of community-acquired methicillin-resistant Staphylococcus aureus infections among HIV-infected persons. Int J STD AIDS. 2007;18:521-526.
    1. Crum-Cianflone N, Weekes J, Bavaro M. Recurrent community-associated methicillin-resistant Staphylococcus aureus infections among HIV-infected persons: incidence and risk factors. AIDS Patient Care STDs. 2009;23:499-502.
    1. Davis KA, Stewart JJ, Crouch HK, Florez CE, Hospenthal DR. Methicillin-resistant Staphylococcus aureus (MRSA) nares colonization at hospital admission and its effect on subsequent MRSA infection. Clin Infect Dis. 2004;39:776-782.
    1. Diep BA, Chambers HF, Graber CJ, Szumowski JD, Miller LG, Han LL, Chen JH, Lin F, Lin J, Phan TH, Carleton HA, McDougal LK, Tenover FC, Cohen DE, Mayer KH, Sensabaugh GF, Perdreau-Remington F. Emergence of multidrug-resistant, community-associated, methicillin-resistant Staphylococcus aureus clone USA300 in men who have sex with men. Ann Intern Med. 2008;148:249-257.
    1. Ellis MW, Hospenthal DR, Dooley DP, Gray PJ, Murray CK. Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiers. Clin Infect Dis. 2004;39:971-979.
    1. Freitas EA, Harris RM, Blake RK, Salgado CD. Prevalence of USA300 strain type of methicillin-resistant Staphylococcus aureus among patients with nasal colonization identified with active surveillance. Infect Control Hosp Epidemiol. 2010;31:469-475.
    1. Ganesh R, Castle D, McGibbon D, Phillips I, Bradbeer C. Staphylococcal carriage and HIV infection. Lancet. 1989;2:558.
    1. Giuliani M, Longo B, Latini A, Prignano G, Monaco M, De Santis A, Impara G, Palamara G, Pantosti A. No evidence of colonization with community-acquired methicillin-resistant Staphylococcus aureus in HIV-1-infected men who have sex with men. Epidemiol Infect. 2010;138:738-742.
    1. Gordon RJ, Chez N, Jia H, Zeller B, Sobieszczyk M, Brennan C, Hisert KB, Lee MH, Vavagiakis P, Lowy FD. The NARES study (Nasal Ointment for Staphylococcus aureus Eradication): a randomized controlled trial of monthly mupirocin in HIV-infected individuals. J Acquir Immune Defic Syndr. 2010;55:466-472.
    1. Graber CJ, Jacobson MA, Perdreau-Remington F, Chambers HF, Diep BA. Recurrence of skin and soft tissue infection caused by methicillin-resistant Staphylococcus aureus in a HIV primary care clinic. J Acquir Immune Defic Syndr. 2008;49:231-233.
    1. Graham PL, Lin SX, Larson EL. A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med. 2006;144:318-325.
    1. Hidron AI, Kourbatova EV, Halvosa JS, Terrell BJ, McDougal LK, Tenover FC, Blumberg HM, King MD. Risk factors for colonization with methicillin-resistant Staphylococcus aureus (MRSA) in patients admitted to an urban hospital: emergence of community-associated MRSA nasal carriage. Clin Infect Dis. 2005;41:159-166.
    1. Holbrook KA, Klein RS, Hartel D, Elliot DA, Barsky TB, Rothschild LH, Lowy FD. Staphylococcus aureus nasal colonization in HIV-seropositive and HIV-seronegative drug users. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;16:301-306.
    1. Honda H, Krauss MJ, Coopersmith CM, Kollef MH, Richmond AM, Fraser VJ, Warren DK. Staphylococcus aureus nasal colonization and subsequent infection in intensive care unit patients: does methicillin resistance matter? Infect Control Hosp Epidemiol. 2010;31:584-591.
    1. King MD, Humphrey BJ, Wang YF, Kourbatova EV, Ray SM, Blumberg HM. Emergence of community-acquired methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann Intern Med. 2006;144:309-317.
    1. Klein PA, Greene WH, Fuhrer J, Clark RA. Prevalence of methicillin-resistant Staphylococcus aureus in outpatients with psoriasis, atopic dermatitis, or HIV infection. Arch Dermatol. 1997;133:1463-1465.
    1. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK. Active Bacterial Core surveillance (ABCs) MRSA Investigators. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA. 2007;298:1763-1771.
    1. Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10:505-520.
    1. Lee NE, Taylor MM, Bancroft E, Ruane PJ, Morgan M, McCoy L, Simon PA. Risk factors for community-associated methicillin-resistant Staphylococcus aureus skin infections among HIV-positive men who have sex with men. Clin Infect Dis. 2005;40:1529-1534.
    1. Madariaga MG, Ullrich F, Swindells S. Low prevalence of community-acquired methicillin-resistant Staphylococcus aureus colonization and apparent lack of correlation with sexual behavior among HIV-infected patients in Nebraska. Clin Infect Dis. 2009;48:1485-1487.
    1. Mathews WC, Caperna JC, Barber RE, Torriani FJ, Miller LG, May S, McCutchan JA. Incidence of and risk factors for clinically significant methicillin-resistant Staphylococcus aureus infection in a cohort of HIV-infected adults. J Acquir Immune Defic Syndr. 2005;40:155-160.
    1. McDonald LC, Lauderdale TL, Lo HJ, Tsai JJ, Hung CC. Colonization of HIV-infected outpatients in Taiwan with methicillin-resistant and methicillin-susceptible Staphylococcus aureus. Int J STD AIDS. 2003;14:473-477.
    1. Melles DC, Pauw E, van den Boogaard L, Boelens HA, Peters J, Peeters JK, Witsenboer H, van Leeuwen WB, Verbrugh HA, van Belkum A, Nouwen JL. Host-microbe interplay in persistent Staphylococcus aureus nasal carriage in HIV patients. Microbes Infect. 2008;10:151-158.
    1. Mermel LA, Eells SJ, Acharya MK, Cartony JM, Dacus D, Fadem S, Gay EA, Gordon S, Lonks JR, Perl TM, McDougal LK, McGowan JE, Maxey G, Morse D, Tenover FC. Quantitative analysis and molecular fingerprinting of methicillin-resistant Staphylococcus aureus nasal colonization in different patient populations: a prospective, multicenter study. Infect Control Hosp Epidemiol. 2010;31:592-597.
    1. Mertz D, Frei R, Periat N, Zimmerli M, Battegay M, Fluckiger U, Widmer AF. Exclusive Staphylococcus aureus throat carriage: at-risk populations. Arch Intern Med. 2009;169:172-178.
    1. Miller M, Cespedes C, Vavagiakis P, Klein RS, Lowy FD. Staphylococcus aureus colonization in a community sample of HIV-infected and HIV-uninfected drug users. Eur J Clin Microbiol Infect Dis. 2003;22:463-469.
    1. Milstone AM, Carroll KC, Ross T, Shangraw KA, Perl TM. Community-associated methicillin-resistant Staphylococcus aureus strains in pediatric intensive care unit. Emerg Infect Dis. 2010;16:647-655.
    1. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB, Talan DA. EMERGEncy ID Net Study Group. Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med. 2006;355:666-674.
    1. Nguyen MH, Kauffman CA, Goodman RP, Squier C, Arbeit RD, Singh N, Wagener MM, Yu VL. Nasal carriage of and infection with Staphylococcus aureus in HIV-infected patients. Ann Intern Med. 1999;130:221-225.
    1. Onorato M, Borucki MJ, Baillargeon G, Paar DP, Freeman DH, Cole CP, Mayhall CG. Risk factors for colonization or infection due to methicillin-resistant Staphylococcus aureus in HIV-positive patients: a retrospective case-control study. Infect Control Hosp Epidemiol. 1999:20:26-30.
    1. Ramsetty SK, Stuart LL, Blake RT, Parsons CH, Salgado CD. Risks for methicillin-resistant Staphylococcus aureus colonization or infection among patients with HIV infection. HIV Med. 2010;11:389-394.
    1. Raviglione MC, Mariuz P, Pablos-Mendez A, Battan R, Ottuso P, Taranta A. High Staphylococcus aureus nasal carriage rate in patients with acquired-immunodeficiency syndrome or AIDS-related complex. Am J Infect Control. 1990;18:64-69.
    1. Seybold U, Supthut-Schroder B, Draenert R, Hogardt M, Bogner JR. Prevalence and risk factors of nasal colonization with Staphylococcus aureus-association with HIV infection in older patients. Scand J Infect Dis. 2009;41:63-66.
    1. Shet A, Mathema B, Mediavilla JR, Kishii K, Mehandru S, Jeane-Pierre P, Laroche M, Willey BM, Kreiswirth N, Markowitz M, Kreiswirth BN. Colonization and subsequent skin and soft tissue infection due to methicillin-resistant Staphylococcus aureus in a cohort of otherwise healthy adults infected with HIV type 1. J Infect Dis. 2009;200:88-93.
    1. Sissolak D, Geusau A, Heinze G, Witte W, Rotter ML. Risk factors for nasal carriage of Staphylococcus aureus in infectious disease patients, including patients infected with HIV, and molecular typing of colonizing strains. Eur J Clin Microbiol Infect Dis. 2002;21:88-96.
    1. Skiest DJ, Brown K, Cooper TW, Hoffman-Roberts H, Mussa HR, Elliott AC. Prospective comparison of methicillin-susceptible and methicillin-resistant community-associated Staphylococcus aureus infections in hospitalized patients. J Infect. 2007;54:427-434.
    1. Szumowski JD, Wener KM, Gold HS, Wong M, Venkataraman L, Runde CA, Cohen DE, Mayer KH, Wright SB. Methicillin-resistant Staphylococcus aureus colonization, behavioral risk factors, and skin and soft-tissue infection at an ambulatory clinic serving a large population of HIV-infected men who have sex with men. Clin Infect Dis. 2009;49:118-121.
    1. Villacian JS, Barkham T, Earnest A, Paton NI. Prevalence of and risk factors for nasal colonization with Staphylococcus aureus among human immunodeficiency virus-positive outpatients in Singapore. Infect Control Hosp Epidemiol. 2004;25:438-440.
    1. Weinke T, Schiller R, Fehrenbach FJ, Pohle HD. Association between Staphylococcus aureus nasopharyngeal colonization and septicemia in patients infected with the human immunodeficiency virus. Eur J Clin Microbiol Infect Dis. 1992;11:985-989.
    1. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5:751-762.

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner