Prevention Strategies for Recurrent Community-Associated Staphylococcus aureus Skin and Soft Tissue Infections
Purpose of Review
Staphylococcus aureus skin and soft tissue infections (SSTI) are a major source of morbidity. More than half of patients experiencing SSTI will have at least one recurrent infection. These infections frequently cluster in households. Given the burden these infections pose to patients and healthcare, prevention strategies are of major clinical importance and represent an active area of research. Bacterial colonization is frequently an early and critical step in the pathogenesis of infection. As such, strategies to prevent reinfection have aimed to decrease staphylococcal colonization of the skin and mucus membranes, a process referred to as decolonization.
Treatment of acute SSTI with incision and drainage and systemic antibiotics is the mainstay of therapy for healing of the acute infection. Systemic antibiotics also provide benefit through reduced incidence of recurrent SSTI. Education for patients and families regarding optimization of personal and household hygiene measures, and avoidance of sharing personal hygiene items, is an essential component in prevention efforts. For patients experiencing recurrent SSTI, or in households in which multiple members have experienced SSTI, decolonization should be recommended for all household members. A recommended decolonization regimen includes application of intranasal mupirocin and antiseptic body washes with chlorhexidine or dilute bleach water baths. For patients who continue to experience recurrent SSTI, periodic decolonization should be considered.
Personal decolonization with topical antimicrobials and antiseptics reduces the incidence of recurrent S. aureus SSTI. Future avenues for investigation include strategies for household environmental decontamination as well as manipulation of the host microbiota.
KeywordsStaphylococcus aureus Methicillin-resistant Staphylococcus aureus Skin and soft tissue infection Prevention Decolonization
J. Chase McNeil reports grants from Allergan, Merck, and Texas Children’s Hospital Pediatric Pilot Research Fund. Stephanie A. Fritz reports grants from the Children's Discovery Institute of Washington University and St, Louis Children's Hospital; National Institutes of Health (NIH)/National Institute of Allergy and Infectious Diseases [grant number K23-AI091690]; NIH/National Center for Advancing Translational Sciences [grant number UL1-TR002345]; and the Agency for Healthcare Research and Quality (AHRQ) [grant numbers R01-HS021736, R01-HS024269]
Compliance with Ethical Standards
Conflict of Interest
Stephanie A. Fritz declares that she has no conflict of interest.
Human and Animal Rights and Informed Consent
All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki declaration and its amendments, institutional/national research committee standards, and international/national/institutional guidelines).
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
- 2.Fritz SA, Epplin EK, Garbutt J, Storch GA. Skin infection in children colonized with community-associated methicillin-resistant Staphylococcus aureus. J Inf Secur. 2009;59(6):394–401.Google Scholar
- 3.•• Daum RS, Miller LG, Immergluck L, et al. A placebo-controlled trial of antibiotics for smaller skin abscesses. N Engl J Med. 2017;376(26):2545–55 An important multicenter trial demonstrating the benefit of systemic antibiotics in the cure of acute SSTI and in preventing recurrent infection. PubMedCrossRefGoogle Scholar
- 9.• Fritz SA, Hogan PG, Hayek G, et al. Staphylococcus aureus colonization in children with community-associated Staphylococcus aureus skin infections and their household contacts. Arch Pediatr Adolesc Med. 2012;166(6):551–7 A study demonstrating that the prevalence of MRSA colonization in household contacts of children with MRSA SSTI is substantially higher than that of the general population. PubMedPubMedCentralCrossRefGoogle Scholar
- 12.• 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(7):971–9 Landmark military-based study demonstrating that CA-MRSA colonization is a predisposing factor for subsequent SSTI. PubMedCrossRefGoogle Scholar
- 13.Milstone AM, Goldner BW, Ross T, Shepard JW, Carroll KC, Perl TM. Methicillin-resistant Staphylococcus aureus colonization and risk of subsequent infection in critically ill children: importance of preventing nosocomial methicillin-resistant Staphylococcus aureus transmission. Clin Infect Dis. 2011;53(9):853–9.PubMedPubMedCentralCrossRefGoogle Scholar
- 19.David MZ, Mennella C, Mansour M, Boyle-Vavra S, Daum RS. Predominance of methicillin-resistant Staphylococcus aureus among pathogens causing skin and soft tissue infections in a large urban jail: risk factors and recurrence rates. J Clin Microbiol. 2008;46(10):3222–7.PubMedPubMedCentralCrossRefGoogle Scholar
- 24.Fritz SA, Camins BC, Eisenstein KA, Fritz JM, Epplin EK, Burnham CA, et al. Effectiveness of measures to eradicate Staphylococcus aureus carriage in patients with community-associated skin and soft-tissue infections: a randomized trial. Infect Control Hosp Epidemiol. 2011;32(9):872–80.PubMedPubMedCentralCrossRefGoogle Scholar
- 25.• 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):679–82 A randomized trial investigating the effectiveness of bleach baths in preventing recurrent SSTI.PubMedCrossRefGoogle Scholar
- 28.Miller LG, Quan C, Shay A, Mostafaie K, Bharadwa K, Tan N, et al. A prospective investigation of outcomes after hospital discharge for endemic, community-acquired methicillin-resistant and -susceptible Staphylococcus aureus skin infection. Clin Infect Dis. 2007;44(4):483–92.PubMedCrossRefGoogle Scholar
- 29.•• 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):743–51 A randomized trial demonstrating that, in households of children with S. aureus SSTI, decolonization of all household members is more effective in preventing recurrent infection compared to decolonization of the index patient alone. PubMedCrossRefGoogle Scholar
- 37.Hulten KG, Mason EO, Lamberth LB, Forbes AR, Revell PA, Kaplan SL. Analysis of invasive community-acquired methicillin-susceptible Staphylococcus aureus infections during a period of declining community acquired methicillin-resistant Staphylococcus aureus infections at a large children’s hospital. Pediatr Infect Dis J. 2018;37(3):235–41.PubMedCrossRefGoogle Scholar
- 39.• Sutter DE, Milburn E, Chukwuma U, Dzialowy N, Maranich AM, Hospenthal DR. Changing susceptibility of Staphylococcus aureus in a US pediatric population. Pediatrics. 2016;137(4):e20153099 A surveillance study conducted within the Military Health System illustrating a decline in MRSA infections. PubMedCrossRefGoogle Scholar
- 40.de la Pardos Gandara M, Raygoza Garay JA, Mwangi M, et al. Molecular types of methicillin-resistant Staphylococcus aureus and methicillin-sensitive S. aureus strains causing skin and soft tissue infections and nasal colonization, identified in community health centers in New York City. J Clin Microbiol. 2015;53(8):2648–58.CrossRefGoogle Scholar
- 41.Orscheln RC, Hunstad DA, Fritz SA, Loughman JA, Mitchell K, Storch EK, et al. Contribution of genetically restricted, methicillin-susceptible strains to the ongoing epidemic of community-acquired Staphylococcus aureus infections. Clin Infect Dis. 2009;49(4):536–42.PubMedPubMedCentralCrossRefGoogle Scholar
- 43.Knox J, Sullivan SB, Urena J, Miller M, Vavagiakis P, Shi Q, et al. Association of environmental contamination in the home with the risk for recurrent community-associated, methicillin-resistant Staphylococcus aureus infection. JAMA Intern Med. 2016;176(6):807–15.PubMedPubMedCentralCrossRefGoogle Scholar
- 46.Eells SJ, David MZ, Taylor A, Ortiz N, Kumar N, Sieth J, 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):1373–82.PubMedCrossRefGoogle Scholar
- 48.Washington University School of Medicine. Staph Household Intervention for Eradication (SHINE) NCT02572791. Available at: https://www.clinicaltrials.gov/ct2/show/NCT02572791?term=02572791&rank=1. Accessed Nov 12, 2018.
- 56.Davis MF, Misic AM, Morris DO, Moss JT, Tolomeo P, Beiting DP, et al. Genome sequencing reveals strain dynamics of methicillin-resistant Staphylococcus aureus in the same household in the context of clinical disease in a person and a dog. Vet Microbiol. 2015;180(3–4):304–7.PubMedPubMedCentralCrossRefGoogle Scholar
- 59.Morris DO, Loeffler A, Davis MF, Guardabassi L, Weese JS. Recommendations for approaches to meticillin-resistant staphylococcal infections of small animals: diagnosis, therapeutic considerations and preventative measures: Clinical Consensus Guidelines of the World Association for Veterinary Dermatology. Vet Dermatol. 2017;28(3):304–e69.PubMedCrossRefGoogle Scholar
- 60.Liu C, Bayer A, Cosgrove SE, Daum RS, Fridkin SK, Gorwitz RJ, 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. Clin Infect Dis. 2011;52(3):e18–55.PubMedCrossRefGoogle Scholar
- 61.•• Talan DA, Mower WR, Krishnadasan A, et al. Trimethoprim-sulfamethoxazole versus placebo for uncomplicated skin abscess. N Engl J Med. 2016;374(9):823–32 An important multicenter trial demonstrating the benefit of systemic antibiotics in the cure of acute SSTI and in preventing recurrent infection. PubMedPubMedCentralCrossRefGoogle Scholar
- 64.• Mork RL, Hogan PG, Muenks CE, et al. Comprehensive modeling reveals proximity, seasonality, and hygiene practices as key determinants of MRSA colonization in exposed households. Pediatr Res. 2018;84(5):668–76. https://doi.org/10.1038/s41390-018-0113-x. Prospective study which evaluated the impact of social determinant and hygiene behaviors on MRSA colonization.
- 68.Washington University School of Medicine. Individual vs. Household MRSA Decolonization (HOME2DS) (NCT01814371). Available at: https://clinicaltrials.gov/ct2/show/NCT01814371?term=01814371&rank=1. Accessed 11/6/2018.
- 74.Simor AE, Phillips E, McGeer A, Konvalinka A, Loeb M, Devlin HR, 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. 2007;44(2):178–85.PubMedCrossRefGoogle Scholar
- 75.• McNeil JC, Hulten KG, Kaplan SL, Mason EO. Decreased susceptibilities to retapamulin, mupirocin, and chlorhexidine among Staphylococcus aureus isolates causing skin and soft tissue infections in otherwise healthy children. Antimicrob Agents Chemother. 2014;58(5):2878–83 Surveillance study examining the prevalence of in vitro resistance to topical antimicrobials and antiseptics in S. aureus community-associated SSTI isolates. PubMedPubMedCentralCrossRefGoogle Scholar
- 76.Naderer OJ, Anderson M, Roberts K, et al. Nasal decolonization of persistant Staphylococcus aureus (SA) carriers with twice daily application of retapamulin ointment, 1% (Ret) for 3 or 5 days. Washington, D.C.: 48th Annual Interscience Conference on Antimicrobial Agents and Chemotherapy and the Infectious Diseases Society of Ameria 46th Annual Meeting; 2008.Google Scholar
- 77.University of California Irving. Retapamulin for reducing MRSA nasal carriage (NCT01461668). Available at: https://clinicaltrials.gov/ct2/show/study/NCT01461668?sect=X70156. Accessed Oct 29, 2018.
- 80.Peng HM, Wang LC, Zhai JL, Weng XS, Feng B, Wang W. Effectiveness of preoperative decolonization with nasal povidone iodine in Chinese patients undergoing elective orthopedic surgery: a prospective cross-sectional study. Braz J Med Biol Res. 2017;51(2):e6736.PubMedPubMedCentralCrossRefGoogle Scholar
- 81.Centers for Disease Control and Prevention. Hand Hygiene in Healthcare Settings. Available at: https://www.cdc.gov/handhygiene/providers/guideline.html. Accessed Oct 29, 2018.
- 84.Steed LL, Costello J, Lohia S, Jones T, Spannhake EW, Nguyen S. Reduction of nasal Staphylococcus aureus carriage in health care professionals by treatment with a nonantibiotic, alcohol-based nasal antiseptic. Am J Infect Control. 2014;42(8):841–6.Google Scholar
- 92.•• Ellis MW, Schlett CD, Millar EV, et al. Hygiene strategies to prevent methicillin-resistant Staphylococcus aureus skin and soft tissue infections: a cluster-randomized controlled trial among high-risk military trainees. Clin Infect Dis. 2014;58(11):1540–8 Large cluster randomized trial examining the effectiveness of hygiene interventions and chlorhexidine washes for SSTI prevention in military recruits. PubMedPubMedCentralCrossRefGoogle Scholar
- 93.Morrison SM, Blaesing CR, Millar EV, Chukwuma U, Schlett CD, Wilkins KJ, et al. Evaluation of methicillin-resistant Staphylococcus aureus skin and soft-tissue infection prevention strategies at a military training center. Infect Control Hosp Epidemiol. 2013;34(8):841–3.PubMedPubMedCentralCrossRefGoogle Scholar
- 98.TopMD Skin Care Inc. A study to evaluate CLn BodyWash as added therapy in eczema patients (CLeaN) (NCT01714245). Available at: https://clinicaltrials.gov/ct2/show/NCT01714245?term=Cln+bodywash&rank=2. Accessed Nov 6, 2018.
- 102.Bessesen MT, Kotter CV, Wagner BD, et al. MRSA colonization and the nasal microbiome in adults at high risk of colonization and infection. J Inf Secur. 2015;71(6):649–57.Google Scholar
- 106.SanMiguel AJ, Meisel JS, Horwinski J, Zheng Q, Grice EA. Topical antimicrobial treatments can elicit shifts to resident skin bacterial communities and reduce colonization by Staphylococcus aureus competitors. Antimicrob Agents Chemother. 2017:61(9).Google Scholar
- 114.van Rensburg JJ, Lin H, Gao X, et al. The human skin microbiome associates with the outcome of and is influenced by bacterial infection. MBio. 2015;6(5):e01315–5.Google Scholar
- 115.Nakatsuji T, Chen TH, Narala S, et al. Antimicrobials from human skin commensal bacteria protect against Staphylococcus aureus and are deficient in atopic dermatitis. Sci Transl Med 2017; 9(378).Google Scholar
- 117.Eggers S, Barker AK, Valentine S, Hess T, Duster M, Safdar N. Effect of Lactobacillus rhamnosus HN001 on carriage of Staphylococcus aureus: results of the impact of probiotics for reducing infections in veterans (IMPROVE) study. BMC Infect Dis. 2018;18(1):129.PubMedPubMedCentralCrossRefGoogle Scholar
- 119.Johnson RC, Schlett CD, Crawford K, Lanier JB, Merrell DS, Ellis MW. Recurrent methicillin-resistant Staphylococcus aureus cutaneous abscesses and selection of reduced chlorhexidine susceptibility during chlorhexidine use. J Clin Microbiol. 2015;53(11):3677–82.PubMedPubMedCentralCrossRefGoogle Scholar
- 121.• McNeil JC, Kok EY, Vallejo JG, et al. Clinical and molecular features of decreased chlorhexidine susceptibility among nosocomial Staphylococcus aureus isolates at Texas Children’s Hospital. Antimicrob Agents Chemother. 2016;60(2):1121–8 This study conducted of hospital acquired pediatric S. aureus infections illustrated the relationship between reduced susceptibility to CHG and/or mupirocin and resistance to systemic antimicrobials. PubMedPubMedCentralCrossRefGoogle Scholar
- 123.Hardy K, Sunnucks K, Gil H, et al. Increased usage of antiseptics Is associated with reduced susceptibility in clinical isolates of Staphylococcus aureus. MBio 2018; 9(3).Google Scholar
- 124.Lee AS, Macedo-Vinas M, Francois P, et al. Impact of combined low-level mupirocin and genotypic chlorhexidine resistance on persistent methicillin-resistant Staphylococcus aureus carriage after decolonization therapy: a case-control study. Clin Infect Dis. 2011;52(12):1422–30.PubMedCrossRefGoogle Scholar
- 125.Batra R, Cooper BS, Whiteley C, Patel AK, Wyncoll D, Edgeworth JD. Efficacy and limitation of a chlorhexidine-based decolonization strategy in preventing transmission of methicillin-resistant Staphylococcus aureus in an intensive care unit. Clin Infect Dis. 2010;50(2):210–7.PubMedCrossRefGoogle Scholar