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Review

Epidemiology and clinical relevance of Staphylococcus aureus intestinal carriage: a systematic review and meta-analysis

, , , , , , & show all
Pages 767-785 | Received 07 Apr 2017, Accepted 19 Jul 2017, Published online: 27 Jul 2017

References

  • Verhoeven PO, Gagnaire J, Botelho-Nevers E, et al. Detection and clinical relevance of Staphylococcus aureus nasal carriage: an update. Expert Rev Anti Infect Ther. 2014;12:75–89.
  • Wertheim HFL, Verveer J, Boelens HAM, et al. Effect of mupirocin treatment on nasal, pharyngeal, and perineal carriage of Staphylococcus aureus in healthy adults. Antimicrob Agents Chemother. 2005;49:1465–1467.
  • Mertz D, Frei R, Periat N, et al. Exclusive Staphylococcus aureus throat carriage: at-risk populations. Arch Intern Med. 2009;169:172–178.
  • Verhoeven PO, Haddar CH, Grattard F, et al. Does pharyngeal sampling improve the detection of nasopharyngeal persistent carriers of Staphylococcus aureus?. J Hosp Infect 2015;70:549-552.
  • Acton DS, Plat-Sinnige MJT, van Wamel W, et al. 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 Off Publ Eur Soc Clin Microbiol. 2009;28:115–127.
  • Claassen-Weitz S, Shittu AO, Ngwarai MR, et al. Fecal carriage of Staphylococcus aureus in the hospital and community setting: a systematic review. Front Microbiol. 2016;7:449.
  • Lemmens N, van Wamel W, Snijders S, et al. Genomic comparisons of USA300 Staphylococcus aureus colonizating the nose and rectum of children with skin abscesses. Microb Pathog. 2011;50:192–199.
  • Tong SYC, Davis JS, Eichenberger E, et al. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015;28:603–661.
  • Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62:1006–1012.
  • Higgins JPT, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–560.
  • Aubry-Damon H, Grenet K, Sall-Ndiaye P, et al. Antimicrobial resistance in commensal flora of pig farmers. Emerg Infect Dis. 2004;10:873–879.
  • Lindberg E, Adlerberth I, Hesselmar B, et al. High rate of transfer of Staphylococcus aureus from parental skin to infant gut flora. J Clin Microbiol. 2004;42:530–534.
  • Chen KT, Huard RC, Della-Latta P, et al. Prevalence of methicillin-sensitive and methicillin-resistant Staphylococcus aureus in pregnant women. Obstet Gynecol. 2006;108:482–487.
  • Szakacs TA, Toye B, Turnbull JM, et al. Prevalence of methicillin-resistant Staphylococcus aureus in a Canadian inner-city shelter. Can J Infect Dis Med Microbiol J Can Mal Infect Microbiol Medicale. 2007;18:249–252.
  • Harrison LM, Morris JA, Lauder RM, et al. The effect of Staphylococcus aureus carriage in late pregnancy on antibody levels to staphylococcal toxins in cord blood and breast milk. FEMS Immunol Med Microbiol. 2008;54:137–143.
  • Andrews JI, Fleener DK, Messer SA, et al. Screening for Staphylococcus aureus carriage in pregnancy: usefulness of novel sampling and culture strategies. Am J Obstet Gynecol. 2009;201:396.e1-5.
  • Thyagarajan D, Sunderamoorthy D, Haridas S, et al. MRSA colonisation in patients admitted with hip fracture: implications for prevention of surgical site infection. Acta Orthop Belg. 2009;75:252–257.
  • Creech CB, Litzner B, Talbot TR, et al. Frequency of detection of methicillin-resistant Staphylococcus aureus from rectovaginal swabs in pregnant women. Am J Infect Control. 2010;38:72–74.
  • Top KA, Huard RC, Fox Z, et al. Trends in methicillin-resistant Staphylococcus aureus anovaginal colonization in pregnant women in 2005 versus 2009. J Clin Microbiol. 2010;48:3675–3680.
  • Onanuga A, Temedie TC. Multidrug-resistant intestinal Staphylococcus aureus among self-medicated healthy adults in Amassoma, South-South, Nigeria. J Health Popul Nutr. 2011;29:446–453.
  • Tomlinson MW, Schmidt NM, Rourke JW, et al. Rectovaginal Staphylococcus aureus colonization: is it a neonatal threat? Am J Perinatol. 2011;28:673–676.
  • Cursino MA, Garcia CP, Lobo RD, et al. Performance of surveillance cultures at different body sites to identify asymptomatic Staphylococcus aureus carriers. Diagn Microbiol Infect Dis. 2012;74:343–348.
  • Benito D, Lozano C, Gómez-Sanz E, et al. Detection of methicillin-susceptible Staphylococcus aureus ST398 and ST133 strains in gut microbiota of healthy humans in Spain. Microb Ecol. 2013;66:105–111.
  • Chan GJ, Modak JK, Mahmud AA, et al. Maternal and neonatal colonization in Bangladesh: prevalences, etiologies and risk factors. J Perinatol Off J Calif Perinat Assoc. 2013;33:971–976.
  • Gurnee EA, Ndao IM, McGhee JE, et al. Fecal carriage of methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus in healthy children. Antimicrob Agents Chemother. 2014;58:1261–1262.
  • Albrecht VS, Limbago BM, Moran GJ, et al. Staphylococcus aureus colonization and strain type at various body sites among patients with a closed abscess and uninfected controls at U.S. emergency departments. J Clin Microbiol. 2015;53:3478–3484.
  • Kumar N, David MZ, Boyle-Vavra S, et al. High Staphylococcus aureus colonization prevalence among patients with skin and soft tissue infections and controls in an urban emergency department. J Clin Microbiol. 2015;53:810–815.
  • Frickmann H, Wiemer D, Frey C, et al. Low enteric colonization with multidrug-resistant pathogens in soldiers returning from deployments - experience from the years 2007-2015. PloS One. 2016;11:e0162129.
  • Singh J, Johnson RC, Schlett CD, et al. Multi-body-site microbiome and culture profiling of military trainees suffering from skin and soft tissue infections at Fort Benning, Georgia. mSphere. 2016;1(5). pii: e00232-16.
  • Soysal A, Sahin H, Yagci A, et al. The low rate of methicillin-resistant Staphylococcus aureus in Turkish children. Jpn J Infect Dis. 2006;59:195–196.
  • Adlerberth I, Strachan DP, Matricardi PM, et al. Gut microbiota and development of atopic eczema in 3 European birth cohorts. J Allergy Clin Immunol. 2007;120:343–350.
  • Gustafsson EB, Ringberg H, Johansson PJH. MRSA in children from foreign countries adopted to Swedish families. Acta Paediatr Oslo Nor 1992. 2007;96:105–108.
  • Harrison LM, Morris JA, Lauder RM, et al. Staphylococcal pyrogenic toxins in infant urine samples: a possible marker of transient bacteraemia. J Clin Pathol. 2009;62:735–738.
  • Skov L, Halkjaer LB, Agner T, et al. Neonatal colonization with Staphylococcus aureus is not associated with development of atopic dermatitis. Br J Dermatol. 2009;160:1286–1291.
  • Faden H, Lesse AJ, Trask J, et al. Importance of colonization site in the current epidemic of staphylococcal skin abscesses. Pediatrics. 2010;125:e618–624.
  • Hewlett AL, Falk PS, Hughes KS, et al. Epidemiology of methicillin-susceptible Staphylococcus aureus in a university medical center day care facility. Pediatr Infect Dis J. 2010;29:145–147.
  • Lindberg E, Adlerberth I, Matricardi P, et al. Effect of lifestyle factors on Staphylococcus aureus gut colonization in Swedish and Italian infants. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2011;17:1209–1215.
  • Akinkunmi EO, Lamikanra A. A study of the intestinal carriage of antibiotic resistant Staphylococcus aureus by Nigerian children. Afr Health Sci. 2012;12:381–387.
  • Sánchez E, Ribes-Koninckx C, Calabuig M, et al. Intestinal Staphylococcus spp. and virulent features associated with coeliac disease. J Clin Pathol. 2012;65:830–834.
  • González R, Maldonado A, Martín V, et al. Breast milk and gut microbiota in African mothers and infants from an area of high HIV prevalence. PloS One. 2013;8:e80299.
  • Stokholm J, Thorsen J, Chawes BL, et al. Cesarean section changes neonatal gut colonization. J Allergy Clin Immunol. 2016;138:881–889.e2.
  • Lundell A-C, Adlerberth I, Lindberg E, et al. Increased levels of circulating soluble CD14 but not CD83 in infants are associated with early intestinal colonization with Staphylococcus aureus. Clin Exp Allergy J Br Soc Allergy Clin Immunol. 2007;37:62–71.
  • Gries DM, Zemzars TF, Gibson KA, et al. A pilot study to assess frequency of carriage and routes of acquisition of Staphylococcus aureus by healthy infants. Am J Infect Control. 2009;37:598–600.
  • Highet AR, Berry AM, Bettelheim KA, et al. Gut microbiome in sudden infant death syndrome (SIDS) differs from that in healthy comparison babies and offers an explanation for the risk factor of prone position. Int J Med Microbiol IJMM. 2014;304:735–741.
  • Benito D, Lozano C, Jiménez E, et al. Characterization of Staphylococcus aureus strains isolated from faeces of healthy neonates and potential mother-to-infant microbial transmission through breastfeeding. FEMS Microbiol Ecol. 2015;91(3). pii: fiv007.
  • El-Kersh TA, Marie MA, Al-Sheikh YA, et al. Prevalence and risk factors of early fecal carriage of Enterococcus faecalis and Staphylococcus spp and their antimicrobial resistant patterns among healthy neonates born in a hospital setting in central Saudi Arabia. Saudi Med J. 2016;37:280–287.
  • Kigbu A, Orimadegun AE, Tongo OO, et al. Intestinal bacterial colonization in the first 2 weeks of life of Nigerian neonates using standard culture methods. Front Pediatr. 2016;4:139.
  • Dupeyron C, Campillo B, Bordes M, et al. A clinical trial of mupirocin in the eradication of methicillin-resistant Staphylococcus aureus nasal carriage in a digestive disease unit. J Hosp Infect. 2002;52:281–287.
  • Manian FA, Senkel D, Zack J, et al. Routine screening for methicillin-resistant Staphylococcus aureus among patients newly admitted to an acute rehabilitation unit. Infect Control Hosp Epidemiol. 2002;23:516–519.
  • Squier C, Rihs JD, Risa KJ, et al. Staphylococcus aureus rectal carriage and its association with infections in patients in a surgical intensive care unit and a liver transplant unit. Infect Control Hosp Epidemiol. 2002;23:495–501.
  • Esposito S, Capuano A, Noviello S, et al. Modification of patients’ endogenous bacterial flora during hospitalization in a large teaching hospital in Naples. J Chemother Florence Italy. 2003;15:568–573.
  • Gnanalingham KK, Elsaghier A, Kibbler C, et al. The impact of methicillin-resistant Staphylococcus aureus in a neurosurgical unit: a growing problem. J Neurosurg. 2003;98:8–13.
  • Ho P-L, Hong Kong intensive care unit antimicrobial resistance study (HK-ICARE) Group. Carriage of methicillin-resistant Staphylococcus aureus, ceftazidime-resistant Gram-negative bacilli, and vancomycin-resistant enterococci before and after intensive care unit admission. Crit Care Med. 2003;31:1175–1182.
  • Boyce JM, Havill NL, Maria B. Frequency and possible infection control implications of gastrointestinal colonization with methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43:5992–5995.
  • Cavalcanti SMM, França ERD, Cabral C, et al. Prevalence of Staphylococcus aureus introduced into intensive care units of a University Hospital. Braz J Infect Dis Off Publ Braz Soc Infect Dis. 2005;9:56–63.
  • Grmek-Kosnik I, Ihan A, Dermota U, et al. Evaluation of separate vs pooled swab cultures, different media, broth enrichment and anatomical sites of screening for the detection of methicillin-resistant Staphylococcus aureus from clinical specimens. J Hosp Infect. 2005;61:155–161.
  • Marchaim D, Lazarovitch Z, Efrati S, et al. Serious consequences to the use of cephalosporins as the first line of antimicrobial therapy administered in hemodialysis units. Nephron Clin Pract. 2005;101:c58–64.
  • Eveillard M, de Lassence A, Lancien E, et al. 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;27:181–184.
  • Singh N, Squier C, Wannstedt C, et al. Impact of an aggressive infection control strategy on endemic Staphylococcus aureus infection in liver transplant recipients. Infect Control Hosp Epidemiol. 2006;27:122–126.
  • Bhalla A, Aron DC, Donskey CJ. Staphylococcus aureus intestinal colonization is associated with increased frequency of S. aureus on skin of hospitalized patients. BMC Infect Dis. 2007;7:105.
  • Zhang SX, Drews SJ, Tomassi J, et al. Comparison of two versions of the IDI-MRSA assay using charcoal swabs for prospective nasal and nonnasal surveillance samples. J Clin Microbiol. 2007;45:2278–2280.
  • Batra R, Eziefula AC, Wyncoll D, et al. Throat and rectal swabs may have an important role in MRSA screening of critically ill patients. Intensive Care Med. 2008;34:1703–1706.
  • Currie A, Davis L, Odrobina E, et al. Sensitivities of nasal and rectal swabs for detection of methicillin-resistant Staphylococcus aureus colonization in an active surveillance program. J Clin Microbiol. 2008;46:3101–3103.
  • Furuno JP, Hebden JN, Standiford HC, et al. Prevalence of methicillin-resistant Staphylococcus aureus and Acinetobacter baumannii in a long-term acute care facility. Am J Infect Control. 2008;36:468–471.
  • Reyes RC, Stoakes L, Milburn S, et al. Evaluation of a new chromogenic medium for the detection of methicillin-resistant Staphylococcus aureus carriage on nasal and perianal specimens. Diagn Microbiol Infect Dis. 2008;60:225–227.
  • Ide L, Lootens J, Thibo P, et al. The nose is not the only relevant MRSA screening site. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2009;15:1192–1193.
  • Nishikawa M, Tanaka T, Nakashima K, et al. Screening for methicillin-resistant Staphylococcus aureus (MRSA) carriage on admission to a geriatric hospital. Arch Gerontol Geriatr. 2009;49:242–245.
  • Baker SE, Brecher SM, Robillard E, et al. Extranasal methicillin-resistant Staphylococcus aureus colonization at admission to an acute care Veterans Affairs hospital. Infect Control Hosp Epidemiol. 2010;31:42–46.
  • Bitterman Y, Laor A, Itzhaki S, et al. Characterization of the best anatomical sites in screening for methicillin-resistant Staphylococcus aureus colonization. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2010;29:391–397.
  • Lauderdale T-LY, Wang J-T, Lee W-S, et al. Carriage rates of methicillin-resistant Staphylococcus aureus (MRSA) depend on anatomic location, the number of sites cultured, culture methods, and the distribution of clonotypes. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. 2010;29:1553–1559.
  • Collins J, Raza M, Ford M, et al. Review of a three-year methicillin-resistant Staphylococcus aureus screening programme. J Hosp Infect. 2011;78:81–85.
  • Maillet J-M, Oghina G, Le Besnerais P, et al. Preoperative carriage and postoperative same-species sternal wound infection after cardiac surgery. Interact Cardiovasc Thorac Surg. 2011;13:381–385.
  • Schechter-Perkins EM, Mitchell PM, Murray KA, et al. Prevalence and predictors of nasal and extranasal staphylococcal colonization in patients presenting to the emergency department. Ann Emerg Med. 2011;57:492–499.
  • Chow A, Win M-K, Wong C-S, et al. Universal methicillin-resistant Staphylococcus aureus (MRSA) screening: comparison of anatomic screening sites for patients with high and low prevalence of MRSA carriage. Infect Control Hosp Epidemiol. 2012;33:315–317.
  • Fiolic Z, Bosnjak Z, Snajdar I, et al. The screening of methicillin-resistant Staphylococcus aureus in vascular surgery patients: a comparison of molecular testing and broth-enriched culture. Chemotherapy. 2012;58:330–336.
  • Matheson A, Christie P, Stari T, et al. Nasal swab screening for methicillin-resistant Staphylococcus aureus–how well does it perform? A cross-sectional study. Infect Control Hosp Epidemiol. 2012;33:803–808.
  • Ng W, George K, Muhammed N, et al. Too close for comfort: screening strategy to detect methicillin-resistant Staphylococcus aureus conversion in exposed roommates. Am J Infect Control. 2012;40:883–885.
  • Datta P, Vasdeva HR, Chander J. Optimization of multiple muco-cutaneous site sampling method for screening MRSA colonization in ICU. Indian J Crit Care Med Peer-Rev Off Publ Indian Soc Crit Care Med. 2013;17:243–245.
  • El-Bouri K, El-Bouri W. Screening cultures for detection of methicillin-resistant Staphylococcus aureus in a population at high risk for MRSA colonisation: identification of optimal combinations of anatomical sites. Libyan J Med. 2013;8:22755.
  • Popovich KJ, Hota B, Aroutcheva A, et al. Community-associated methicillin-resistant Staphylococcus aureus colonization burden in HIV-infected patients. Clin Infect Dis Off Publ Infect Dis Soc Am. 2013;56:1067–1074.
  • Dokter J, Brusselaers N, Hendriks WDH, et al. Bacteriological cultures on admission of the burn patient: to do or not to do, that’s the question. Burns J Int Soc Burn Inj. 2016;42:421–427.
  • Dahlman D, Jalalvand F, Blomé MA, et al. High perineal and overall frequency of Staphylococcus aureus in people who inject drugs, compared to non-injectors. Curr Microbiol. 2017;74:159–167.
  • Thorburn K, Taylor N, Saladi SM, et al. Use of surveillance cultures and enteral vancomycin to control methicillin-resistant Staphylococcus aureus in a paediatric intensive care unit. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2006;12:35–42.
  • Ohno K, Nakamura T, Azuma T, et al. Surveillance of bacteriological examinations at hospitalization in a pediatric surgical ward. J Pediatr Surg. 2008;43:1507–1510.
  • Srinivasan A, Seifried SE, Zhu L, et al. Increasing prevalence of nasal and rectal colonization with methicillin-resistant Staphylococcus aureus in children with cancer. Pediatr Blood Cancer. 2010;55:1317–1322.
  • Shehabi AA, Abu-Yousef R, Badran E, et al. Major characteristics of Staphylococcus aureus colonizing Jordanian infants. Pediatr Int Off J Jpn Pediatr Soc. 2013;55:300–304.
  • Nitsch-Osuch A, Choroszy-Król I, Kuchar E, et al. Microbiological spectrum and susceptibility pattern of clinical isolates from the neonatal unit in a single medical center. Adv Clin Exp Med Off Organ Wroclaw Med Univ. 2015;24:15–22.
  • Gómez M, Moles L, Melgar A, et al. Early gut colonization of preterm infants: effect of enteral feeding tubes. J Pediatr Gastroenterol Nutr. 2016;62:893–900.
  • Waites KB, Canupp KC, DeVivo MJ. Microbiology of the urethra and perineum and its relationship to bacteriuria in community-residing men with spinal cord injury. J Spinal Cord Med. 2004;27:448–452.
  • Roghmann M-C, Gorman PH, Wallin MT, et al. Staphylococcus aureus colonization in community-dwelling people with spinal cord dysfunction. Arch Phys Med Rehabil. 2007;88:979–983.
  • Mody L, Kauffman CA, Donabedian S, et al. Epidemiology of Staphylococcus aureus colonization in nursing home residents. Clin Infect Dis Off Publ Infect Dis Soc Am. 2008;46:1368–1373.
  • Antoniou T, Devlin R, Gough K, et al. Prevalence of community-associated methicillin-resistant Staphylococcus aureus colonization in men who have sex with men. Int J STD AIDS. 2009;20:180–183.
  • O’Fallon E, Schreiber R, Kandel R, et al. Multidrug-resistant gram-negative bacteria at a long-term care facility: assessment of residents, healthcare workers, and inanimate surfaces. Infect Control Hosp Epidemiol. 2009;30:1172–1179.
  • Szumowski JD, Wener KM, Gold HS, et al. 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 Off Publ Infect Dis Soc Am. 2009;49:118–121.
  • March A, Aschbacher R, Dhanji H, et al. Colonization of residents and staff of a long-term-care facility and adjacent acute-care hospital geriatric unit by multiresistant bacteria. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2010;16:934–944.
  • Fouéré S, Dion P-L, Casin I, et al. Absence of community-acquired methicillin-resistant Staphylococcus aureus carriage or infection in a cohort of 300 men who have sex with men attending an inner-city sexually transmitted disease clinic in Paris, France. Dermatol Basel Switz. 2012;224:257–261.
  • Miko BA, Uhlemann A-C, 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;14:1040–1043.
  • Dodiuk-Gad R, Cohen-Barak E, Ziv M, et al. Bacteriological aspects of Darier’s disease. J Eur Acad Dermatol Venereol JEADV. 2013;27:1405–1409.
  • Joore IKCW, van Rooijen MS, Schim van der Loeff MF, et al. Low prevalence of methicillin-resistant Staphylococcus aureus among men who have sex with men attending an STI clinic in Amsterdam: a cross-sectional study. BMJ Open. 2013;3.
  • Gibson KE, McNamara SE, Cassone M, et al. Methicillin-resistant Staphylococcus aureus: site of acquisition and strain variation in high-risk nursing home residents with indwelling devices. Infect Control Hosp Epidemiol. 2014;35:1458–1465.
  • Lemma MT, Zenebe Y, Tulu B, et al. Methicillin resistant Staphylococcus aureus among HIV infected pediatric patients in Northwest Ethiopia: carriage rates and antibiotic co-resistance profiles. Plos One. 2015;10.
  • Roghmann M-C, Johnson JK, Sorkin JD, et al. Transmission of methicillin-resistant Staphylococcus aureus (MRSA) to healthcare worker gowns and gloves during care of nursing home residents. Infect Control Hosp Epidemiol. 2015;36:1050–1057.
  • Alsterholm M, Strömbeck L, Ljung A, et al. Variation in Staphylococcus aureus colonization in relation to disease severity in adults with atopic dermatitis during a five-month follow-up. Acta Derm Venereol. 2017;97:802–807.
  • Lee C-M, Lai -C-C, Chiang H-T, et al. Presence of multidrug-resistant organisms in the residents and environments of long-term care facilities in Taiwan. J Microbiol Immunol Infect Wei Mian Yu Gan Ran Za Zhi. 2017;50:133–144.
  • Marshall C, McBryde E. The role of Staphylococcus aureus carriage in the pathogenesis of bloodstream infection. BMC Res Notes. 2014;7:428.
  • Buehlmann M, Frei R, Fenner L, et al. Highly effective regimen for decolonization of methicillin-resistant Staphylococcus aureus carriers. Infect Control Hosp Epidemiol. 2008;29:510–516.
  • Drews SJ, Willey BM, Kreiswirth N, et al. Verification of the IDI-MRSA assay for detecting methicillin-resistant Staphylococcus aureus in diverse specimen types in a core clinical laboratory setting. J Clin Microbiol. 2006;44:3794–3796.
  • Lee DC, Barlas D, Ryan JG, et al. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci: prevalence and predictors of colonization in patients presenting to the emergency department from nursing homes. J Am Geriatr Soc. 2002;50:1463–1465.
  • Meurman O, Routamaa M, Peltonen R. Screening for methicillin-resistant Staphylococcus aureus: which anatomical sites to culture? J. Hosp Infect. 2005;61:351–353.
  • Crossley K, Solliday J. Comparison of rectal swabs and stool cultures for the detection of gastrointestinal carriage of Staphylococcus aureus. J Clin Microbiol. 1980;11:433–434.
  • Regev-Yochay G, Dagan R, Raz M, et al. Association between carriage of Streptococcus pneumoniae and Staphylococcus aureus in children. JAMA. 2004;292:716–720.
  • Lebon A, Labout JAM, Verbrugh HA, et al. Dynamics and determinants of Staphylococcus aureus carriage in infancy: the generation R study. J Clin Microbiol. 2008;46:3517–3521.
  • Nakao A, Ito T, Han X, et al. Intestinal carriage of methicillin-resistant Staphylococcus aureus in nasal MRSA carriers hospitalized in the neonatal intensive care unit. Antimicrob Resist Infect Control. 2014;3:14.
  • Mongkolrattanothai K, Gray BM, Mankin P, et al. Simultaneous carriage of multiple genotypes of Staphylococcus aureus in children. J Med Microbiol. 2011;60:317–322.
  • Popovich KJ, Aroutcheva A, Hota B, et al. Anatomic sites of colonization with community-associated methicillin-resistant Staphylococcus aureus. Infect Control Hosp Epidemiol. 2014;35:1192–1194.
  • Senn L, Clerc O, Zanetti G, et al. The Stealthy superbug: the role of asymptomatic enteric carriage in maintaining a long-term hospital outbreak of ST228 methicillin-resistant Staphylococcus aureus. mBio. 2016;7:e02039–02015.
  • McKinnell JA, Huang SS, Eells SJ, et al. Quantifying the impact of extranasal testing of body sites for methicillin-resistant Staphylococcus aureus colonization at the time of hospital or intensive care unit admission. Infect Control Hosp Epidemiol. 2013;34:161–170.
  • Chipolombwe J, Török ME, Mbelle N, et al. Methicillin-resistant Staphylococcus aureus multiple sites surveillance: a systemic review of the literature. Infect Drug Resist. 2016;9:35–42.
  • Thwaites GE, Gant V. Are bloodstream leukocytes Trojan horses for the metastasis of Staphylococcus aureus? Nat Rev Microbiol. 2011;9:215–222.
  • Krezalek MA, Hyoju S, Zaborin A, et al. Can methicillin-resistant Staphylococcus aureus silently travel from the gut to the wound and cause postoperative infection? Modeling the “Trojan Horse Hypothesis.”. Ann Surg. 2017. doi: 10.1097/SLA.0000000000002173. Epub ahead of print.
  • Yang ES, Tan J, Eells S, et al. Body site colonization in patients with community-associated methicillin-resistant Staphylococcus aureus and other types of S. aureus skin infections. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2010;16:425–431.
  • Wertheim HFL, Melles DC, Vos MC, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5:751–762.
  • McCullough AC, Seifried M, Zhao X, et al. Higher incidence of perineal community acquired MRSA infections among toddlers. BMC Pediatr. 2011;11:96.
  • Begier EM, Frenette K, Barrett NL, et al. A high-morbidity outbreak of methicillin-resistant Staphylococcus aureus among players on a college football team, facilitated by cosmetic body shaving and turf burns. Clin Infect Dis Off Publ Infect Dis Soc Am. 2004;39:1446–1453.
  • Kazakova SV, Hageman JC, Matava M, et al. A clone of methicillin-resistant Staphylococcus aureus among professional football players. N Engl J Med. 2005;352:468–475.
  • Miller LG, Diep BA. Clinical practice: colonization, fomites, and virulence: rethinking the pathogenesis of community-associated methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis Off Publ Infect Dis Soc Am. 2008;46:752–760.
  • Bode LGM, Kluytmans JAJW, Wertheim HFL, et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Engl J Med. 2010;362:9–17.
  • Allegranzi B, Zayed B, Bischoff P, et al. New WHO recommendations on intraoperative and postoperative measures for surgical site infection prevention: an evidence-based global perspective. Lancet Infect Dis. 2016;16:e288–e303.
  • Septimus EJ, Schweizer ML. Decolonization in prevention of health care-associated infections. Clin Microbiol Rev. 2016;29:201–222.
  • Harbarth S, Dharan S, Liassine N, et al. Randomized, placebo-controlled, double-blind trial to evaluate the efficacy of mupirocin for eradicating carriage of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 1999;43:1412–1416.
  • Oie S, Suenaga S, Sawa A, et al. Association between isolation sites of methicillin-resistant Staphylococcus aureus (MRSA) in patients with MRSA-positive body sites and MRSA contamination in their surrounding environmental surfaces. Jpn J Infect Dis. 2007;60:367–369.
  • Hayden MK, Lin MY, Lolans K, et al. Prevention of colonization and infection by Klebsiella pneumoniae carbapenemase-producing enterobacteriaceae in long-term acute-care hospitals. Clin Infect Dis Off Publ Infect Dis Soc Am. 2015;60:1153–1161.
  • Climo MW, Sepkowitz KA, Zuccotti G, et al. The effect of daily bathing with chlorhexidine on the acquisition of methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus, and healthcare-associated bloodstream infections: results of a quasi-experimental multicenter trial. Crit Care Med. 2009;37:1858–1865.
  • Vernon MO, Hayden MK, Trick WE, et al. Chlorhexidine gluconate to cleanse patients in a medical intensive care unit: the effectiveness of source control to reduce the bioburden of vancomycin-resistant enterococci. Arch Intern Med. 2006;166:306–312.
  • Frost SA, Alogso M-C, Metcalfe L, et al. Chlorhexidine bathing and health care-associated infections among adult intensive care patients: a systematic review and meta-analysis. Crit Care Lond Engl. 2016;20:379.
  • Falagas ME, Bliziotis IA, Fragoulis KN. Oral rifampin for eradication of Staphylococcus aureus carriage from healthy and sick populations: a systematic review of the evidence from comparative trials. Am J Infect Control. 2007;35:106–114.
  • Simor AE, Phillips E, McGeer A, et al. Randomized controlled trial of chlorhexidine gluconate for washing, intranasal mupirocin, and rifampin and doxycycline versus no treatment for the eradication of methicillin-resistant Staphylococcus aureus colonization. Clin Infect Dis Off Publ Infect Dis Soc Am. 2007;44:178–185.
  • Walsh TJ, Standiford HC, Reboli AC, et al. Randomized double-blinded trial of rifampin with either novobiocin or trimethoprim-sulfamethoxazole against methicillin-resistant Staphylococcus aureus colonization: prevention of antimicrobial resistance and effect of host factors on outcome. Antimicrob Agents Chemother. 1993;37:1334–1342.
  • de la Cal MA, Cerdá E, van Saene HKF, et al. Effectiveness and safety of enteral vancomycin to control endemicity of methicillin-resistant Staphylococcus aureus in a medical/surgical intensive care unit. J Hosp Infect. 2004;56:175–183.
  • Furuno JP, Perencevich EN, Johnson JA, et al. Methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococci co-colonization. Emerg Infect Dis. 2005;11:1539–1544.
  • de Smet AMGA, Kluytmans JAJW, Cooper BS, et al. Decontamination of the digestive tract and oropharynx in ICU patients. N Engl J Med. 2009;360:20–31.
  • Price R, MacLennan G, Glen J, et al. Selective digestive or oropharyngeal decontamination and topical oropharyngeal chlorhexidine for prevention of death in general intensive care: systematic review and network meta-analysis. BMJ. 2014;348:g2197.
  • Oostdijk EAN, Kesecioglu J, Schultz MJ, et al. Effects of decontamination of the oropharynx and intestinal tract on antibiotic resistance in ICUs: a randomized clinical trial. JAMA. 2014;312:1429–1437.
  • Daneman N, Sarwar S, Fowler RA, et al. Effect of selective decontamination on antimicrobial resistance in intensive care units: a systematic review and meta-analysis. Lancet Infect Dis. 2013;13:328–341.
  • Liu C, Bayer A, Cosgrove SE, et al. Clinical practice guidelines by the Infectious Diseases Society of America for the treatment of methicillin-resistant Staphylococcus aureus infections in adults and children: executive summary. Clin Infect Dis Off Publ Infect Dis Soc Am. 2011;52:285–292.
  • Eggers S, Barker A, Valentine S, et al. Impact of probiotics for reducing infections in veterans (IMPROVE): study protocol for a double-blind, randomized controlled trial to reduce carriage of Staphylococcus aureus. Contemp Clin Trials. 2017;52:39–45.
  • Eggers S, Barker A, Valentine S, et al. Effect of Lactobacillus rhamnosus HN001 on carriage of Staphylococcus aureus: results of IMPROVE. 2017.
  • Berthelot P, Grattard F, Cazorla C, et al. Is nasal carriage of Staphylococcus aureus the main acquisition pathway for surgical-site infection in orthopaedic surgery? Eur. J Clin Microbiol Infect Dis. 2010;29:373–382.
  • Harris SR, Feil EJ, Holden MTG, et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science. 2010;327:469–474.
  • Kalmeijer MD, van Nieuwland-Bollen E, Bogaers-Hofman D, et al. Nasal carriage of Staphylococcus aureus is a major risk factor for surgical-site infections in orthopedic surgery. Infect Control Hosp Epidemiol. 2000;21:319–323.
  • Verhoeven PO, Gagnaire J, Haddar CH, et al. Identifying hemodialysis patients with the highest risk of Staphylococcus aureus endogenous infection through a simple nasal sampling algorithm. medicine (baltimore). 2016;95:e3231.
  • Price JR, Didelot X, Crook DW, et al. Whole genome sequencing in the prevention and control of Staphylococcus aureus infection. J Hosp Infect. 2013;83:14–21.

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