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Staphylococcus aureus colonisation and its relationship with skin and soft tissue infection in New Zealand children

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Abstract

New Zealand children suffer from high rates of skin and soft tissue infection (SSTI). Staphylococcus aureus colonisation is known to increase the risk of nosocomial infection. We aimed to determine whether S. aureus colonisation also increased the risk of community-onset SSTI. This study, performed within the Growing Up in New Zealand cohort, used interview and administrative data, and bacterial culture results from the nose, throat, and skin swabs collected at 4½ years of age. Multivariable log-binomial regression was used to derive adjusted risk ratios. S. aureus was isolated from 2225/5126 (43.4%) children. SSTI affected 1509/5126 (29.4%) children before age five. S. aureus colonisation at any site was associated with SSTI (aRR = 1.09, 95%CI 1.01–1.19), particularly in the year prior to swab collection (aRR = 1.18, 95%CI 1.02–1.37). The strongest association was between skin colonisation and SSTI within the year prior to swab collection (aRR = 1.47, 95%CI 1.14–1.84). Socioeconomic and ethnic variables remained independent determinants of SSTI. S. aureus colonisation was associated with an increased risk of community-onset SSTI. Socioeconomic and ethnic factors and eczema had independent effects on SSTI risk. Interventions which reduce the prevalence of S. aureus colonisation may be expected to reduce the incidence of community-onset SSTI.

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References

  1. Williamson DA, Ritchie SR, Roberts SA, Coombs GW, Thomas MG, Hannaford O, Baker MG, Lennon D, Fraser JD (2014) Clinical and molecular epidemiology of community-onset invasive Staphylococcus aureus infection in New Zealand children. Epidemiol Infect:1–9. https://doi.org/10.1017/s0950268814000053

  2. Craig E, Adams J, Oben G, Reddington A, Wicken A, Simpson J, Service obotNCaYE (2012) Te Ohonga Ake The Health Status of Māori Children and Young People in New Zealand

  3. O’Sullivan CE, Baker MG, Zhang J (2011) Increasing hospitalizations for serious skin infections in New Zealand children, 1990-2007. Epidemiol Infect 139(11):1794–1804. https://doi.org/10.1017/s0950268810002761

    Article  PubMed  Google Scholar 

  4. Ritchie SR, Fraser JD, Libby E, Morris AJ, Rainey PB, Thomas MG (2011) Demographic variation in community-based MRSA skin and soft tissue infection in Auckland, New Zealand. N Z Med J 124(1332):21–30

    PubMed  Google Scholar 

  5. Kluytmans J, van Belkum A, Verbrugh H (1997) Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10(3):505–520

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Ritchie SR, Isdale E, Priest P, Rainey PB, Thomas MG (2015) The turnover of strains in intermittent and persistent nasal carriers of Staphylococcus aureus. J Infect. https://doi.org/10.1016/j.jinf.2015.12.010

  7. Sollid JUE, Furberg AS, Hanssen AM, Johannessen M (2014) Staphylococcus aureus: determinants of human carriage. Infect Genet Evol 21:531–541. https://doi.org/10.1016/j.meegid.2013.03.020

    Article  CAS  PubMed  Google Scholar 

  8. Lebon A, Labout JA, Verbrugh HA, Jaddoe VW, Hofman A, van Wamel W, Moll HA, van Belkum A (2008) Dynamics and determinants of Staphylococcus aureus carriage in infancy: the Generation R Study. J Clin Microbiol 46(10):3517–3521. https://doi.org/10.1128/jcm.00641-08

    Article  PubMed  PubMed Central  Google Scholar 

  9. Harrison LM, Morris JA, Telford DR, Brown SM, Jones K (1999) The nasopharyngeal bacterial flora in infancy: effects of age, gender, season, viral upper respiratory tract infection and sleeping position. FEMS Immunol Med Microbiol 25(1–2):19–28. https://doi.org/10.1111/j.1574-695X.1999.tb01323.x

    Article  CAS  PubMed  Google Scholar 

  10. van Belkum A, Verkaik Nelianne J, de Vogel CP, Boelens Hélène A, Verveer J, Nouwen Jan L, Verbrugh Henri A, Wertheim Heiman FL (2009) Reclassification of Staphylococcus aureus nasal carriage types. J Infect Dis 199(12):1820–1826. https://doi.org/10.1086/599119

    Article  PubMed  Google Scholar 

  11. Verhoeven PO, Grattard F, Carricajo A, Lucht F, Cazorla C, Garraud O, Pozzetto B, Berthelot P (2012) An algorithm based on one or two nasal samples is accurate to identify persistent nasal carriers of Staphylococcus aureus. Clin Microbiol Infect 18(6):551–557. https://doi.org/10.1111/j.1469-0691.2011.03611.x

    Article  CAS  PubMed  Google Scholar 

  12. Johnson RC, Ellis MW, Lanier JB, Schlett CD, Cui T, Merrell DS (2015) Correlation between nasal microbiome composition and remote purulent skin and soft tissue infections. Infect Immun 83(2):802–811. https://doi.org/10.1128/iai.02664-14

    Article  PubMed  PubMed Central  Google Scholar 

  13. Nurjadi D, Lependu J, Kremsner PG, Zanger P (2012) Staphylococcus aureus throat carriage is associated with ABO−/secretor status. J Infect 65(4):310–317. https://doi.org/10.1016/j.jinf.2012.05.011

    Article  PubMed  Google Scholar 

  14. Zanger P, Nurjadi D, Vath B, Kremsner PG (2011) Persistent nasal carriage of Staphylococcus aureus is associated with deficient induction of human beta-defensin 3 after sterile wounding of healthy skin in vivo. Infect Immun 79(7):2658–2662. https://doi.org/10.1128/iai.00101-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Nakatsuji T, Chen TH, Narala S, Chun KA, Two AM, Yun T, Shafiq F, Kotol PF, Bouslimani A, Melnik AV, Latif H, Kim J-N, Lockhart A, Artis K, David G, Taylor P, Streib J, Dorrestein PC, Grier A, Gill SR, Zengler K, Hata TR, Leung DYM, Gallo RL (2017) Antimicrobials from human skin commensal bacteria protect against <em>Staphylococcus aureus</em> and are deficient in atopic dermatitis. Sci Transl Med 9 (378). https://doi.org/10.1126/scitranslmed.aah4680

  16. Verhoeven PO, Gagnaire J, Botelho-Nevers E, Grattard F, Carricajo A, Lucht F, Pozzetto B, Berthelot P (2014) Detection and clinical relevance of Staphylococcus aureus nasal carriage: an update. Expert Rev Anti-Infect Ther 12(1):75–89. https://doi.org/10.1586/14787210.2014.859985

    Article  CAS  PubMed  Google Scholar 

  17. Nouwen JL, Fieren MW, Snijders S, Verbrugh HA, van Belkum A (2005) Persistent (not intermittent) nasal carriage of Staphylococcus aureus is the determinant of CPD-related infections. Kidney Int 67(3):1084–1092. https://doi.org/10.1111/j.1523-1755.2005.00174.x

    Article  PubMed  Google Scholar 

  18. Morton SMB, Grant CC, Atatoa Carr PE, Robinson EM, Kinloch JM, Fleming CJ, Kingi TKR, Perese LM, Liang R (2012) How do you recruit and retain a prebirth cohort? Lessons learnt from growing up in New Zealand. Eval Health Prof 1–23. https://doi.org/10.1177/0163278712462717

  19. Morton S, Ramke J, Kinloch J, Grant C, Atatoa Carr P, Leeson H, Lee A, Robinson E (2015) Growing up in New Zealand cohort alignment with all New Zealand births. Aust N Z J Public Health 39(1):82–87

    Article  PubMed  Google Scholar 

  20. Morton SMB, Atatoa Carr PE, Grant CC, Robinson EM, Bandara DK, Bird A, Ivory VC, Kingi TKR, Liang R, Marks EJ, Perese LM, Peterson ER, Pryor JE, Reese E, Schmidt JM, Waldie KE, Wall C (2013) Cohort profile: growing up in New Zealand. Int J Epidemiol 42(1):65–75. https://doi.org/10.1093/ije/dyr206

    Article  PubMed  Google Scholar 

  21. Salmond C, Crampton P, King P, Waldegrave C (2014) NZiDep an index of socioeconomic deprivation for individuals. University of Otago, Wellington

    Google Scholar 

  22. World Health Organisation (2015) ICD-10 version:2015. World Health Organisation, Geneva

    Google Scholar 

  23. O'Sullivan CE, Baker MG (2010) Proposed epidemiological case definition for serious skin infection in children. J Paediatr Child Health 46(4):176–183. https://doi.org/10.1111/j.1440-1754.2009.01658.x

    Article  PubMed  Google Scholar 

  24. Baker MG, Barnard LT, Kvalsvig A, Verrall A, Zhang J, Keall M, Wilson N, Wall T, Howden-Chapman P (2012) Increasing incidence of serious infectious diseases and inequalities in New Zealand: a national epidemiological study. Lancet 379(9821):1112–1119

    Article  PubMed  Google Scholar 

  25. Miller LG, Eisenberg DF, Liu H, Chang CL, Wang Y, Luthra R, Wallace A, Fang C, Singer J, Suaya JA (2015) Incidence of skin and soft tissue infections in ambulatory and inpatient settings, 2005-2010. BMC Infect Dis 15:362. https://doi.org/10.1186/s12879-015-1071-0

    Article  PubMed  PubMed Central  Google Scholar 

  26. Carville KS, Lehmann D, Hall G, Moore H, Richmond P, de Klerk N, Burgner D (2007) Infection is the major component of the disease burden in aboriginal and non-aboriginal Australian children: a population-based study. Pediatr Infect Dis J 26(3):210–216. https://doi.org/10.1097/1001.inf.0000254148.0000209831.0000254147f

    Article  PubMed  Google Scholar 

  27. Williamson DA, Ritchie SR, Lennon D, Roberts SA, Stewart J, Thomas MG, Baker MG (2013) Increasing incidence and sociodemographic variation in community-onset Staphylococcus aureus skin and soft tissue infections in New Zealand children. Pediatr Infect Dis J 32(8):923–925. https://doi.org/10.1097/INF.0b013e3182905f3d

    Article  PubMed  Google Scholar 

  28. Craig E, Adams J, Oben G, Reddington A, Wicken A, Simpson J (2011) The health status of children and young people in the Northern District health boards. University of Otago, NZ Child and Youth Epidemiology Service

  29. Simpson J, Duncanson M, Oben G, Adams J, Wicken A, Pierson M, Lilley R, Gallagher S (2017) Te Ohonga Ake the health of Māori children and young people in New Zealand series two. New Zealand Child and Youth Epidemiology Service, University of Otago, Dunedin

    Google Scholar 

  30. O'Sullivan C, Baker MG (2012) Skin infections in children in a New Zealand primary care setting: exploring beneath the tip of the iceberg. N Z Med J 125(1351):70–79

    PubMed  Google Scholar 

  31. O'Sullivan C, Baker MG, Zhang J, Davies A, Cramp G (2012) The epidemiology of serious skin infections in New Zealand children: comparing the Tairawhiti region with national trends. N Z Med J 125(1351):40–54

    PubMed  Google Scholar 

  32. Reid P, Robson B (2007) Understanding health inequities. In: Robson B, Harris R (eds) Hauora: Maori standards of health IV. A study of the years 2000–2005. Te Ropu Rangahau Hauora a Eru Pomare, School of Medicine and Health Sciences, University of Otago, Wellington

    Google Scholar 

  33. Mertz D, Frei R, Jaussi B, Tietz A, Stebler C, Fluckiger U, Widmer AF (2007) Throat swabs are necessary to reliably detect carriers of Staphylococcus aureus. Clin Infect Dis 45(4):475–477. https://doi.org/10.1086/520016

    Article  PubMed  Google Scholar 

  34. Blumental S, Deplano A, Jourdain S, De Mendonça R, Hallin M, Nonhoff C, Rottiers S, Vergison A, Denis O (2013) Dynamic pattern and genotypic diversity of Staphylococcus aureus nasopharyngeal carriage in healthy pre-school children. J Antimicrob Chemother 68(7):1517–1523. https://doi.org/10.1093/jac/dkt080

    Article  CAS  PubMed  Google Scholar 

  35. Munckhof WJ, Nimmo GR, Schooneveldt JM, Schlebusch S, Stephens AJ, Williams G, Huygens F, Giffard P (2009) Nasal carriage of Staphylococcus aureus, including community-associated methicillin-resistant strains, in Queensland adults. Clin Microbiol Infect 15(2):149–155. https://doi.org/10.1111/j.1469-0691.2008.02652.x

    Article  CAS  PubMed  Google Scholar 

  36. Cole AM, Tahk S, Oren A, Yoshioka D, Kim Y-H, Park A, Ganz T (2001) Determinants of Staphylococcus aureus nasal carriage. Clin Diagn Lab Immunol 8(6):1064–1069. https://doi.org/10.1128/cdli.8.6.1064-1069.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Shukla SK, Rose W, Schrodi SJ (2015) Complex host genetic susceptibility to Staphylococcus aureus infections. Trends Microbiol 23(9):529–536. https://doi.org/10.1016/j.tim.2015.05.008

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The study has been designed and conducted by the Growing Up in New Zealand study team, led by the University of Auckland. The authors would like to thank the families who have participated in the study and acknowledge the contributions of the original study investigators: Susan M.B. Morton, Polly E. Atatoa Carr, Cameron C. Grant, Arier C. Lee, Dinusha K. Bandara, Jatender Mohal, Jennifer M. Kinloch, Johanna M. Schmidt, Mary R. Hedges, Vivienne C. Ivory, Te Kani R. Kingi, Renee Liang, Lana M. Perese, Elizabeth Peterson, Jan E. Pryor, Elaine Reese, Elizabeth M. Robinson, Karen E. Waldie, and Clare R. Wall.

Funding

Dr. Hobbs is supported by the Auckland Medical Research Foundation Douglas Goodfellow Medical Research Fellowship (grant number 1414001). Growing Up in New Zealand has been funded by the New Zealand Ministries of Social Development, Health, Education, Justice and Pacific Island Affairs; the former Ministry of Science Innovation and the former Department of Labour (now both part of the Ministry of Business, Innovation and Employment); the former Ministry of Women’s Affairs (now the Ministry for Women); the Department of Corrections; the Families Commission (now known as the Social Policy Evaluation and Research Unit); Te Puni Kokiri; New Zealand Police; Sport New Zealand; the Housing New Zealand Corporation; and the former Mental Health Commission, The University of Auckland and Auckland UniServices Limited. Other support for the study has been provided by the Health Research Council of New Zealand, Statistics New Zealand, the Office of the Children’s Commissioner, and the Office of Ethnic Affairs.

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Authors and Affiliations

  1. Growing Up in New Zealand, The Centre for Longitudinal Research – He Ara ki Mua, University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand

    Mark R. Hobbs, Cameron C. Grant, Sarah Berry, Susan M. B. Morton & Emma Marks

  2. Infectious Diseases Department, Auckland District Health Board, Auckland City Hospital, Auckland, New Zealand

    Mark R. Hobbs, Mark G. Thomas & Stephen R. Ritchie

  3. General Paediatrics, Auckland District Health Board, Starship Children’s Hospital, Auckland, New Zealand

    Cameron C. Grant

  4. Department of Paediatrics: Child and Youth Health, Faculty of Medicine and Health Sciences, University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand

    Cameron C. Grant

  5. Department of Molecular Medicine and Pathology, Faculty of Medicine and Health Sciences, University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand

    Mark G. Thomas & Stephen R. Ritchie

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  1. Mark R. Hobbs
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  2. Cameron C. Grant
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Correspondence to Mark R. Hobbs.

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Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

Ethical approval was obtained from the Ministry of Health Northern Y Regional Ethics Committee (NTY/08106/055).

Informed consent

Parents of participating children provided written informed consent for microbiological sampling, and for linkage with administrative health datasets.

Disclaimer

The views reported in this paper are those of the authors and do not necessarily represent the views of the Growing Up in New Zealand investigators. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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Hobbs, M.R., Grant, C.C., Thomas, M.G. et al. Staphylococcus aureus colonisation and its relationship with skin and soft tissue infection in New Zealand children. Eur J Clin Microbiol Infect Dis 37, 2001–2010 (2018). https://doi.org/10.1007/s10096-018-3336-1

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