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Prevention Strategies for Recurrent Community-Associated Staphylococcus aureus Skin and Soft Tissue Infections

  • J. Chase McNeil
  • Stephanie A. FritzEmail author
Skin, Soft Tissue, Bone and Joint Infectious Disease (N Safdar and A Pop-Vicas, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Skin, Soft Tissue, Bone and Joint Infections

Abstract

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.

Recent Findings

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.

Summary

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.

Keywords

Staphylococcus aureus Methicillin-resistant Staphylococcus aureus Skin and soft tissue infection Prevention Decolonization 

Notes

Funding

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).

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Miller LG, Eisenberg DF, Liu H, Chang CL, Wang Y, Luthra R, et al. Incidence of skin and soft tissue infections in ambulatory and inpatient settings, 2005-2010. BMC Infect Dis. 2015;15:362.PubMedPubMedCentralGoogle Scholar
  2. 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. 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. PubMedGoogle Scholar
  4. 4.
    Kaplan SL, Hulten KG, Gonzalez BE, Hammerman WA, Lamberth L, Versalovic J, et al. Three-year surveillance of community-acquired Staphylococcus aureus infections in children. Clin Infect Dis. 2005;40(12):1785–91.PubMedGoogle Scholar
  5. 5.
    Talan DA, Krishnadasan A, Gorwitz RJ, Fosheim GE, Limbago B, Albrecht V, et al. Comparison of Staphylococcus aureus from skin and soft-tissue infections in US emergency department patients, 2004 and 2008. Clin Infect Dis. 2011;53(2):144–9.PubMedGoogle Scholar
  6. 6.
    Johnson JK, Khoie T, Shurland S, Kreisel K, Stine OC, Roghmann MC. Skin and soft tissue infections caused by methicillin-resistant Staphylococcus aureus USA300 clone. Emerg Infect Dis. 2007;13(8):1195–200.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Gonzalez BE, Hulten KG, Dishop MK, Lamberth LB, Hammerman WA, Mason EO, et al. Pulmonary manifestations in children with invasive community-acquired Staphylococcus aureus infection. Clin Infect Dis. 2005;41(5):583–90.PubMedGoogle Scholar
  8. 8.
    Kluytmans JA, Mouton JW, Ijzerman EP, et al. Nasal carriage of Staphylococcus aureus as a major risk factor for wound infections after cardiac surgery. J Infect Dis. 1995;171(1):216–9.PubMedGoogle Scholar
  9. 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. PubMedPubMedCentralGoogle Scholar
  10. 10.
    Faden H, Lesse AJ, Trask J, Hill JA, Hess DJ, Dryja D, et al. Importance of colonization site in the current epidemic of staphylococcal skin abscesses. Pediatrics. 2010;125(3):e618–24.PubMedGoogle Scholar
  11. 11.
    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(6):776–82.PubMedGoogle Scholar
  12. 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. PubMedGoogle Scholar
  13. 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.PubMedPubMedCentralGoogle Scholar
  14. 14.
    von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group N Engl J Med. 2001;344(1):11–6.Google Scholar
  15. 15.
    Fritz SA, Krauss MJ, Epplin EK, Burnham CA, Garbutt J, Dunne WM, et al. The natural history of contemporary Staphylococcus aureus nasal colonization in community children. Pediatr Infect Dis J. 2011;30(4):349–51.PubMedPubMedCentralGoogle Scholar
  16. 16.
    Kuehnert MJ, Kruszon-Moran D, Hill HA, McQuillan G, McAllister SK, Fosheim G, et al. Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002. J Infect Dis. 2006;193(2):172–9.PubMedGoogle Scholar
  17. 17.
    Hersh AL, Chambers HF, Maselli JH, Gonzales R. National trends in ambulatory visits and antibiotic prescribing for skin and soft-tissue infections. Arch Intern Med. 2008;168(14):1585–91.PubMedGoogle Scholar
  18. 18.
    Ray GT, Suaya JA, Baxter R. Incidence, microbiology, and patient characteristics of skin and soft-tissue infections in a U.S. population: a retrospective population-based study. BMC Infect Dis. 2013;13:252.PubMedPubMedCentralGoogle Scholar
  19. 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.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Creech CB, Saye E, McKenna BD, et al. One-year surveillance of methicillin-resistant Staphylococcus aureus nasal colonization and skin and soft tissue infections in collegiate athletes. Arch Pediatr Adolesc Med. 2010;164(7):615–20.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Wright MO, Furuno JP, Venezia RA, Johnson JK, Standiford HC, Hebden JN, et al. Methicillin-resistant Staphylococcus aureus infection and colonization among hospitalized prisoners. Infect Control Hosp Epidemiol. 2007;28(7):877–9.PubMedGoogle Scholar
  22. 22.
    Jimenez-Truque N, Saye EJ, Soper N, et al. Longitudinal assessment of colonization with Staphylococcus aureus in healthy collegiate athletes. J Pediatric Infect Dis Soc. 2016;5(2):105–13.PubMedGoogle Scholar
  23. 23.
    Williams DJ, Cooper WO, Kaltenbach LA, et al. Comparative effectiveness of antibiotic treatment strategies for pediatric skin and soft-tissue infections. Pediatrics. 2011;128(3):e479–87.PubMedPubMedCentralGoogle Scholar
  24. 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.PubMedPubMedCentralGoogle Scholar
  25. 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.PubMedGoogle Scholar
  26. 26.
    Duong M, Markwell S, Peter J, Barenkamp S. Randomized, controlled trial of antibiotics in the management of community-acquired skin abscesses in the pediatric patient. Ann Emerg Med. 2010;55(5):401–7.PubMedGoogle Scholar
  27. 27.
    Chen AE, Cantey JB, Carroll KC, Ross T, Speser S, Siberry GK. Discordance between Staphylococcus aureus nasal colonization and skin infections in children. Pediatr Infect Dis J. 2009;28(3):244–6.PubMedGoogle Scholar
  28. 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.PubMedGoogle Scholar
  29. 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. PubMedGoogle Scholar
  30. 30.
    McNeil JC, Hulten KG, Kaplan SL, Schwarzwald HL, Mason EO. Staphylococcus aureus infections in HIV-positive children and adolescents. Pediatr Infect Dis J. 2012;31(3):284–6.PubMedGoogle Scholar
  31. 31.
    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(7):499–502.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Bocchini CE, Mason EO, Hulten KG, Hammerman WA, Kaplan SL. Recurrent community-associated Staphylococcus aureus infections in children presenting to Texas Children’s Hospital in Houston, Texas. Pediatr Infect Dis J. 2013;32(11):1189–93.PubMedGoogle Scholar
  33. 33.
    L’Heriteau F, Lucet JC, Scanvic A, Bouvet E. Community-acquired methicillin-resistant Staphylococcus aureus and familial transmission. JAMA. 1999;282(11):1038–9.PubMedGoogle Scholar
  34. 34.
    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):e76–8.PubMedGoogle Scholar
  35. 35.
    Nerby JM, Gorwitz R, Lesher L, Juni B, Jawahir S, Lynfield R, et al. Risk factors for household transmission of community-associated methicillin-resistant Staphylococcus aureus. Pediatr Infect Dis J. 2011;30(11):927–32.PubMedGoogle Scholar
  36. 36.
    Rodriguez M, Hogan PG, Burnham CA, Fritz SA. Molecular epidemiology of Staphylococcus aureus in households of children with community-associated S aureus skin and soft tissue infections. J Pediatr. 2014;164(1):105–11.PubMedGoogle Scholar
  37. 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.PubMedGoogle Scholar
  38. 38.
    Acree ME, Morgan E, David MZ. S. aureus Infections in Chicago, 2006-2014: Increase in CA MSSA and decrease in MRSA incidence. Infect Control Hosp Epidemiol. 2017;38(10):1226–34.PubMedGoogle Scholar
  39. 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. PubMedGoogle Scholar
  40. 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.Google Scholar
  41. 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.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Desai R, Pannaraj PS, Agopian J, Sugar CA, Liu GY, Miller LG. Survival and transmission of community-associated methicillin-resistant Staphylococcus aureus from fomites. Am J Infect Control. 2011;39(3):219–25.PubMedGoogle Scholar
  43. 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.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Miller LG, Eells SJ, David MZ, Ortiz N, Taylor AR, Kumar N, 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):753–63.PubMedGoogle Scholar
  45. 45.
    Fritz SA, Hogan PG, Singh LN, Thompson RM, Wallace MA, Whitney K, et al. Contamination of environmental surfaces with Staphylococcus aureus in households with children infected with methicillin-resistant S aureus. JAMA Pediatr. 2014;168(11):1030–8.PubMedPubMedCentralGoogle Scholar
  46. 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.PubMedGoogle Scholar
  47. 47.
    Knox J, Uhlemann AC, Miller M, Hafer C, Vasquez G, Vavagiakis P, et al. Environmental contamination as a risk factor for intra-household Staphylococcus aureus transmission. PLoS One. 2012;7(11):e49900.PubMedPubMedCentralGoogle Scholar
  48. 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.
  49. 49.
    Hanselman BA, Kruth SA, Rousseau J, Low D, Willey B, McGeer A, et al. Methicillin-resistant Staphylococcus aureus colonization in veterinary personnel. Emerg Infect Dis. 2006;12(12):1933–8.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Weese JS, Dick H, Willey BM, et al. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet Microbiol. 2006;115(1–3):148–55.PubMedGoogle Scholar
  51. 51.
    Rutland BE, Weese JS, Bolin C, Au J, Malani AN. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerg Infect Dis. 2009;15(8):1328–30.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Manian FA. Asymptomatic nasal carriage of mupirocin-resistant, methicillin-resistant Staphylococcus aureus (MRSA) in a pet dog associated with MRSA infection in household contacts. Clin Infect Dis. 2003;36(2):e26–8.PubMedGoogle Scholar
  53. 53.
    van Duijkeren E, Wolfhagen MJ, Box AT, Heck ME, Wannet WJ, Fluit AC. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerg Infect Dis. 2004;10(12):2235–7.PubMedPubMedCentralGoogle Scholar
  54. 54.
    van Duijkeren E, Wolfhagen MJ, Heck ME, Wannet WJ. Transmission of a Panton-Valentine leucocidin-positive, methicillin-resistant Staphylococcus aureus strain between humans and a dog. J Clin Microbiol. 2005;43(12):6209–11.PubMedPubMedCentralGoogle Scholar
  55. 55.
    Boost MV, O’Donoghue MM, James A. Prevalence of Staphylococcus aureus carriage among dogs and their owners. Epidemiol Infect. 2008;136(7):953–64.PubMedGoogle Scholar
  56. 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.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Davis MF, Iverson SA, Baron P, Vasse A, Silbergeld EK, Lautenbach E, et al. Household transmission of meticillin-resistant Staphylococcus aureus and other staphylococci. Lancet Infect Dis. 2012;12(9):703–16.PubMedGoogle Scholar
  58. 58.
    Cohn LA, Middleton JR. A veterinary perspective on methicillin-resistant staphylococci. J Vet Emerg Crit Care (San Antonio). 2010;20(1):31–45.Google Scholar
  59. 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.PubMedGoogle Scholar
  60. 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.PubMedGoogle Scholar
  61. 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. PubMedPubMedCentralGoogle Scholar
  62. 62.
    Talan DA, Moran GJ, Krishnadasan A, Abrahamian FM, Lovecchio F, Karras DJ, et al. Subgroup analysis of antibiotic treatment for skin abscesses. Ann Emerg Med. 2018;71(1):21–30.PubMedGoogle Scholar
  63. 63.
    Hogan PG, Rodriguez M, Spenner AM, Brenneisen JM, Boyle MG, Sullivan ML, et al. Impact of systemic antibiotics on Staphylococcus aureus colonization and recurrent skin infection. Clin Infect Dis. 2018;66(2):191–7.PubMedGoogle Scholar
  64. 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.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Al-Zubeidi D, Burnham CA, Hogan PG, Collins R, Hunstad DA, Fritz SA. Molecular epidemiology of recurrent cutaneous methicillin-resistant Staphylococcus aureus infections in children. J Pediatric Infect Dis Soc. 2014;3(3):261–4.PubMedGoogle Scholar
  66. 66.
    Chen CJ, Su LH, Lin TY, Huang YC. Molecular analysis of repeated methicillin-resistant Staphylococcus aureus infections in children. PLoS One. 2010;5(12):e14431.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Cluzet VC, Gerber JS, Nachamkin I, Metlay JP, Zaoutis TE, Davis MF, et al. Duration of colonization and determinants of earlier clearance of colonization with methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 2015;60(10):1489–96.PubMedPubMedCentralGoogle Scholar
  68. 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.
  69. 69.
    Kohler P, Sommerstein R, Schonrath F, et al. Effect of perioperative mupirocin and antiseptic body wash on infection rate and causative pathogens in patients undergoing cardiac surgery. Am J Infect Control. 2015;43(7):e33–8.PubMedGoogle Scholar
  70. 70.
    Huang SS, Septimus E, Kleinman K, Moody J, Hickok J, Avery TR, et al. Targeted versus universal decolonization to prevent ICU infection. N Engl J Med. 2013;368(24):2255–65.PubMedGoogle Scholar
  71. 71.
    Popoola VO, Colantuoni E, Suwantarat N, Pierce R, Carroll KC, Aucott SW, et al. Active surveillance cultures and decolonization to reduce Staphylococcus aureus infections in the neonatal intensive care unit. Infect Control Hosp Epidemiol. 2016;37(4):381–7.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Raz R, Miron D, Colodner R, Staler Z, Samara Z, Keness Y. A 1-year trial of nasal mupirocin in the prevention of recurrent staphylococcal nasal colonization and skin infection. Arch Intern Med. 1996;156(10):1109–12.PubMedGoogle Scholar
  73. 73.
    Weintrob A, Bebu I, Agan B, Diem A, Johnson E, Lalani T, et al. Randomized, double-blind, placebo-controlled study on decolonization procedures for methicillin-resistant Staphylococcus aureus (MRSA) among HIV-infected adults. PLoS One. 2015;10(5):e0128071.PubMedPubMedCentralGoogle Scholar
  74. 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.PubMedGoogle Scholar
  75. 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. PubMedPubMedCentralGoogle Scholar
  76. 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. 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.
  78. 78.
    Bebko SP, Green DM, Awad SS. Effect of a preoperative decontamination protocol on surgical site infections in patients undergoing elective orthopedic surgery with hardware implantation. JAMA Surg. 2015;150(5):390–5.PubMedGoogle Scholar
  79. 79.
    Phillips M, Rosenberg A, Shopsin B, Cuff G, Skeete F, Foti A, et al. Preventing surgical site infections: a randomized, open-label trial of nasal mupirocin ointment and nasal povidone-iodine solution. Infect Control Hosp Epidemiol. 2014;35(7):826–32.PubMedPubMedCentralGoogle Scholar
  80. 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.PubMedPubMedCentralGoogle Scholar
  81. 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.
  82. 82.
    Allegranzi B, Pittet D. Role of hand hygiene in healthcare-associated infection prevention. J Hosp Infect. 2009;73(4):305–15.PubMedGoogle Scholar
  83. 83.
    Allegranzi B, Sax H, Pittet D. Hand hygiene and healthcare system change within multi-modal promotion: a narrative review. J Hosp Infect. 2013;83(Suppl 1):S3–10.PubMedGoogle Scholar
  84. 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.PubMedGoogle Scholar
  85. 85.
    McDonnell G, Russell AD. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev. 1999;12(1):147–79.PubMedPubMedCentralGoogle Scholar
  86. 86.
    Bleasdale SC, Trick WE, Gonzalez IM, Lyles RD, Hayden MK, Weinstein RA. Effectiveness of chlorhexidine bathing to reduce catheter-associated bloodstream infections in medical intensive care unit patients. Arch Intern Med. 2007;167(19):2073–9.PubMedGoogle Scholar
  87. 87.
    Climo MW, Yokoe DS, Warren DK, Perl TM, Bolon M, Herwaldt LA, et al. Effect of daily chlorhexidine bathing on hospital-acquired infection. N Engl J Med. 2013;368(6):533–42.PubMedPubMedCentralGoogle Scholar
  88. 88.
    Lee BY, Bartsch SM, Wong KF, McKinnell JA, Cui E, Cao C, et al. Beyond the intensive care unit (ICU): countywide impact of universal ICU Staphylococcus aureus decolonization. Am J Epidemiol. 2016;183(5):480–9.PubMedPubMedCentralGoogle Scholar
  89. 89.
    Milstone AM, Elward A, Song X, Zerr DM, Orscheln R, Speck K, et al. Daily chlorhexidine bathing to reduce bacteraemia in critically ill children: a multicentre, cluster-randomised, crossover trial. Lancet. 2013;381(9872):1099–106.PubMedPubMedCentralGoogle Scholar
  90. 90.
    Quach C, Milstone AM, Perpete C, Bonenfant M, Moore DL, Perreault T. Chlorhexidine bathing in a tertiary care neonatal intensive care unit: impact on central line-associated bloodstream infections. Infect Control Hosp Epidemiol. 2014;35(2):158–63.PubMedGoogle Scholar
  91. 91.
    Toltzis P, O’Riordan M, Cunningham DJ, Ryckman FC, Bracke TM, Olivea J, et al. A statewide collaborative to reduce pediatric surgical site infections. Pediatrics. 2014;134(4):e1174–80.PubMedGoogle Scholar
  92. 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. PubMedPubMedCentralGoogle Scholar
  93. 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.PubMedPubMedCentralGoogle Scholar
  94. 94.
    Roll A, Cozzio A, Fischer B, Schmid-Grendelmeier P. Microbial colonization and atopic dermatitis. Curr Opin Allergy Clin Immunol. 2004;4(5):373–8.PubMedGoogle Scholar
  95. 95.
    Huang JT, Abrams M, Tlougan B, Rademaker A, Paller AS. Treatment of Staphylococcus aureus colonization in atopic dermatitis decreases disease severity. Pediatrics. 2009;123(5):e808–14.PubMedGoogle Scholar
  96. 96.
    Fisher RG, Chain RL, Hair PS, Cunnion KM. Hypochlorite killing of community-associated methicillin-resistant Staphylococcus aureus. Pediatr Infect Dis J. 2008;27(10):934–5.PubMedGoogle Scholar
  97. 97.
    Ryan C, Shaw RE, Cockerell CJ, Hand S, Ghali FE. Novel sodium hypochlorite cleanser shows clinical response and excellent acceptability in the treatment of atopic dermatitis. Pediatr Dermatol. 2013;30(3):308–15.PubMedPubMedCentralGoogle Scholar
  98. 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.
  99. 99.
    •• Cogen AL, Nizet V, Gallo RL. Skin microbiota: a source of disease or defence? Br J Dermatol. 2008;158(3):442–55 A comprehensive review of the role of skin microbiota in host health and disease. PubMedPubMedCentralGoogle Scholar
  100. 100.
    Reid G, Howard J, Gan BS. Can bacterial interference prevent infection? Trends Microbiol. 2001;9(9):424–8.PubMedGoogle Scholar
  101. 101.
    Alvarez AS, Remy L, Allix-Beguec C, et al. Patient nostril microbial flora: individual-dependency and diversity precluding prediction of Staphylococcus aureus acquisition. Clin Microbiol Infect. 2014;20(1):70–8.PubMedGoogle Scholar
  102. 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
  103. 103.
    Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR. The human nasal microbiota and Staphylococcus aureus carriage. PLoS One. 2010;5(5):e10598.PubMedPubMedCentralGoogle Scholar
  104. 104.
    Johnson RC, Ellis MW, Lanier JB, Schlett CD, Cui T, Merrell DS. Correlation between nasal microbiome composition and remote purulent skin and soft tissue infections. Infect Immun. 2015;83(2):802–11.PubMedPubMedCentralGoogle Scholar
  105. 105.
    Liu CM, Price LB, Hungate BA, Abraham AG, Larsen LA, Christensen K, et al. Staphylococcus aureus and the ecology of the nasal microbiome. Sci Adv. 2015;1(5):e1400216.PubMedPubMedCentralGoogle Scholar
  106. 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
  107. 107.
    Uehara Y, Nakama H, Agematsu K, Uchida M, Kawakami Y, Abdul Fattah ASM, et al. Bacterial interference among nasal inhabitants: eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp. J Hosp Infect. 2000;44(2):127–33.PubMedGoogle Scholar
  108. 108.
    Yan M, Pamp SJ, Fukuyama J, Hwang PH, Cho DY, Holmes S, et al. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe. 2013;14(6):631–40.PubMedPubMedCentralGoogle Scholar
  109. 109.
    Piewngam P, Zheng Y, Nguyen TH, Dickey SW, Joo HS, Villaruz AE, et al. Pathogen elimination by probiotic Bacillus via signalling interference. Nature. 2018;562(7728):532–7.PubMedPubMedCentralGoogle Scholar
  110. 110.
    Casadevall A, Pirofski LA. What is a host? Incorporating the microbiota into the damage-response framework. Infect Immun. 2015;83(1):2–7.PubMedGoogle Scholar
  111. 111.
    Cogen AL, Yamasaki K, Sanchez KM, Dorschner RA, Lai Y, MacLeod DT, et al. Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin. J Invest Dermatol. 2010;130(1):192–200.PubMedPubMedCentralGoogle Scholar
  112. 112.
    Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature. 2010;465(7296):346–9.PubMedGoogle Scholar
  113. 113.
    Zipperer A, Konnerth MC, Laux C, Berscheid A, Janek D, Weidenmaier C, et al. Human commensals producing a novel antibiotic impair pathogen colonization. Nature. 2016;535(7613):511–6.PubMedGoogle Scholar
  114. 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. 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
  116. 116.
    Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8(1):15–25.PubMedPubMedCentralGoogle Scholar
  117. 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.PubMedPubMedCentralGoogle Scholar
  118. 118.
    Muenks CE, Sewell WC, Hogan PG, Thompson RM, Ross DG, Wang JW, et al. Methicillin-resistant Staphylococcus aureus: the effects are more than skin deep. J Pediatr. 2018;199:158–65.PubMedGoogle Scholar
  119. 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.PubMedPubMedCentralGoogle Scholar
  120. 120.
    McNeil JC, Hulten KG, Kaplan SL, Mahoney DH, Mason EO. Staphylococcus aureus infections in pediatric oncology patients: high rates of antimicrobial resistance, antiseptic tolerance and complications. Pediatr Infect Dis J. 2013;32(2):124–8.PubMedGoogle Scholar
  121. 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. PubMedPubMedCentralGoogle Scholar
  122. 122.
    Suwantarat N, Carroll KC, Tekle T, Ross T, Maragakis LL, Cosgrove SE, et al. High prevalence of reduced chlorhexidine susceptibility in organisms causing central line-associated bloodstream infections. Infect Control Hosp Epidemiol. 2014;35(9):1183–6.PubMedGoogle Scholar
  123. 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. 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.PubMedGoogle Scholar
  125. 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.PubMedGoogle Scholar
  126. 126.
    Antonov NK, Garzon MC, Morel KD, Whittier S, Planet PJ, Lauren CT. High prevalence of mupirocin resistance in Staphylococcus aureus isolates from a pediatric population. Antimicrob Agents Chemother. 2015;59(6):3350–6.PubMedPubMedCentralGoogle Scholar
  127. 127.
    Fritz SA, Hogan PG, Camins BC, Ainsworth AJ, Patrick C, Martin MS, 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):559–68.PubMedPubMedCentralGoogle Scholar
  128. 128.
    DeMarco CE, Cushing LA, Frempong-Manso E, Seo SM, Jaravaza TA, Kaatz GW. Efflux-related resistance to norfloxacin, dyes, and biocides in bloodstream isolates of Staphylococcus aureus. Antimicrob Agents Chemother. 2007;51(9):3235–9.PubMedPubMedCentralGoogle Scholar
  129. 129.
    Diep BA, Gill SR, Chang RF, Phan THV, Chen JH, Davidson MG, et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet. 2006;367(9512):731–9.PubMedGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Pediatrics, Section of Infectious DiseasesBaylor College of MedicineHoustonUSA
  2. 2.Department of Pediatrics, Division of Infectious DiseasesWashington University School of MedicineSt. LouisUSA

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