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Transmission through air as a possible route of exposure for MRSA

Journal of Exposure Science & Environmental Epidemiology volume 26, pages 263–269 (2016)Cite this article

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Abstract

Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) is highly prevalent in pigs and veal calves. The environment and air in pig and veal calf barns is often contaminated with LA-MRSA, and can act as a transmission source for humans. This study explores exposure–response relationships between sequence type 398 (ST398) MRSA air exposure level and nasal ST398 MRSA carriage in people working and/or living on farms. Samples and data were used from three longitudinal field studies in pig and veal calf farm populations. Samples consisted of nasal swabs from the human participants and electrostatic dust fall collectors capturing airborne settled dust in barns. In both multivariate and mutually adjusted analyses, a strong association was found between nasal ST398 MRSA carriage in people working in the barns for >20 h per week and MRSA air levels. In people working in the barns < 20 h per week there was a strong association between nasal carriage and number of working hours. Exposure to ST398 MRSA in barn air seems to be an important determinant for nasal carriage, especially in the highly exposed group of farmers, next to duration of contact with animals. Intervention measures should therefore probably also target reduction of ST398 MRSA air levels.

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References

  1. Pletinckx LJ, Verhegghe M, Dewulf J, Crombé F, De Bleecker Y, Rasschaert G et al. Screening of poultry-pig farms for methicillin-resistant Staphylococcus aureus: Sampling methodology and within herd prevalence in broiler flocks and pigs. Infect Genet Evol 2011; 11: 2133–2137.

    Article  CAS  Google Scholar 

  2. Kreausukon K, Fetsch A, Kraushaar B, Alt K, Müller K, Krömker et al. Prevalence, antimicrobial resistance, and molecular characterization of methicillin-resistant Staphylococcus aureus from bulk tank milk of dairy herds. J Dairy Sci 2012; 95: 4382–4388.

    Article  CAS  Google Scholar 

  3. Graveland H, Wagenaar JA, Heesterbeek J, Mevius D, Van Duijkeren E, Heederik DJJ . Methicillin resistant Staphylococcus aureus ST398 in veal calf farming: human MRSA carriage related with animal antimicrobial usage and farm hygiene. PLoS One 2010; 5: e10990.

    Article  Google Scholar 

  4. Broens EM, Graat EA, Van der Wolf PJ, Van de Giessen AW, De Jong MC . Prevalence and risk factor analysis of livestock associated MRSA-positive pig herds in The Netherlands. Prev Vet Med 2011; 102: 41–49.

    Article  CAS  Google Scholar 

  5. Mulders MN, Haenen AP, Geenen PL, Vesseur PC, Poldervaart ES, Bosch T et al. Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in the Netherlands. Epidemiol Infect 2010; 138: 743–755.

    Article  CAS  Google Scholar 

  6. Van den Broek IV, Van Cleef BA, Haenen A, Broens EM, Van der Wolf PJ, Van den Broek MJ et al. Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiol Infect 2009; 137: 700–708.

    Article  CAS  Google Scholar 

  7. Van Cleef BA, Van Benthem BH, Verkade EJ, Van Rijen M, Kluytmans-van den Bergh MF, Schouls LM et al. Dynamics of methicillin-resistant Staphylococcus aureus and methicillin-susceptible Staphylococcus aureus carriage in pig farmers: a prospective cohort study. Clin Microbiol Infect 2014; 20: O764–O771.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Graveland H, Wagenaar JA, Bergs K, Heesterbeek JAP, Heederik D . Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS One 2011; 6: e16830.

    Article  CAS  Google Scholar 

  10. Van Cleef BA, Graveland H, Haenen APJ, Van de Giessen AW, Heederik D, Wagenaar JA et al. Persistence of livestock-associated methicillin-resistant Staphylococcus aureus in field workers after short-term occupational exposure to pigs and veal calves. J Clin Microbiol 2011; 49: 1030–1033.

    Article  Google Scholar 

  11. Van Cleef BA, Broens EM, Voss A, Huijsdens XW, Züchner L, Van Benthem BH et al. High prevalence of nasal MRSA carriage in slaughterhouse workers in contact with live pigs in the Netherlands. Epidemiol Infect 2010; 138: 756–763.

    Article  CAS  Google Scholar 

  12. Gilbert MJ, Bos MEH, Duim B, Urlings BA, Heres L, Wagenaar JA et al. Livestock-associated MRSA ST398 carriage in pig slaughterhouse workers related to quantitative environmental exposure. Occup Environ Med 2012; 69: 472–478.

    Article  Google Scholar 

  13. Merialdi G, Galletti E, Guazzetti S, Rosignoli C, Alborali G, Battisti A et al. Environmental methicillin-resistant Staphylococcus aureus contamination in pig herds in relation to the productive phase and application of cleaning and disinfection. Res Vet Sci 2013; 94: 425–427.

    Article  CAS  Google Scholar 

  14. Pletinckx LJ, Verhegghe M, Crombe F, Dewulf J, De Bleecker Y, Rasschaert G et al. Evidence of possible methicillin-resistant Staphylococcus aureus ST398 spread between pigs and other animals and people residing on the same farm. Prev Vet Med 2013; 109: 293–303.

    Article  Google Scholar 

  15. Springer B, Orendi U, Much P, Höger G, Ruppitsch W, Krziwanek K et al. Methicillin-resistant Staphylococcus aureus: a new zoonotic agent? Wiener Klin Wochenschr 2009; 121: 86–90.

    Article  CAS  Google Scholar 

  16. Friese A, Schulz J, Hoehle L, Fetsch A, Tenhagen B-A, Hartung J et al. Occurrence of MRSA in air and housing environment of pig barns. Vet Microbiol 2012; 158: 129–135.

    Article  Google Scholar 

  17. Fessler At, Olde Riekerink RG, Rothkamp A, Kadlec K, Sampimon OC, Lam TJ et al. Characterization of methicillin-resistant Staphylococcus aureus CC398 obtained from humans and animals on dairy farms. Vet Microbiol 2012; 160: 77–84.

    Article  CAS  Google Scholar 

  18. Broens EM, Van Cleef BA, Graat EA, Kluytmans JA . Transmission of methicillin resistant Staphylococcus aureus from food production animals to humans: a review. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2008; 3 No. 095, page 1–12.

  19. Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005; 5: 751–762.

    Article  Google Scholar 

  20. Masclaux FG, Sakwinska O, Charrière N, Semaani E, Oppliger A . Concentration of airborne Staphylococcus aureus (MRSA and MSSA), total bacteria, and endotoxins in pig farms. Ann Occup Hyg 2013; 57: 550–557.

    CAS  PubMed  Google Scholar 

  21. Dorado-Garcia A, Bos MEH, Graveland H, Van Cleef BA, Verstappen KM, Kluytmans JA et al. Risk factors for persistence of livestock-associated MRSA and environmental exposure in veal calf farmers and their family members: an observational longitudinal study. BMJ Open 2013; 3: e003272.

    Article  Google Scholar 

  22. Gibbs SG, Green CF, Tarwater PM, Mota LC, Mena KD, Scarpino PV . Isolation of antibiotic-resistant bacteria from the air plume downwind of a swine confined or concentrated animal feeding operation. Environ Health Perspect 2006; 114: 1032–1037.

    Article  CAS  Google Scholar 

  23. Heederik DJJ, Opstal-van Winden AJW, Smit LAM, Wouters IM, Hooiveld M, Ijzermans CJ et al. Mogelijke effecten van de intensieve-veehouderij op de gezondheid van omwonenden: onderzoek naar potentiële blootstelling en gezondheidsproblemen. IRAS Universiteit Utrecht, NIVEL, RIVM 2011.

  24. Bisdorff B, Scholhölter JL, Claußen K, Pulz M, Nowak D, Radon K . MRSA-ST398 in livestock farmers and neighbouring residents in a rural area in Germany. Epidemiol Infect 2012; 140: 1800–1808.

    Article  CAS  Google Scholar 

  25. Van Cleef BA, Verkade EJ, Wulf MW, Buiting AG, Voss A, Huijsdens XW et al. Prevalence of livestock-associated MRSA in communities with high pig-densities in the Netherlands. PLoS One 2010; 5: e9385.

    Article  Google Scholar 

  26. Graveland H, Wagenaar JA, Verstappen KM, Oosting-van Schothorst I, Heederik DJ, Bos MEH . Dynamics of MRSA carriage in veal calves: a longitudinal field study. Prev Vet Med 2012; 107: 180–186.

    Article  Google Scholar 

  27. Dohmen W, Bonten MJM, Bos MEH, Van Marm S, Scharringa J, Wagenaar JA et alCarriage of Extended Spectrum Beta-Lactamases in pig farmers is associated to occurrence in pigs, 2013 (submitted)..

  28. Noss I, Wouters IM, Visser M, Heederik DJ, Thorne PS, Brunekreef B et al. Evaluation of a low-cost electrostatic dust fall collector for indoor air endotoxin exposure assessment. Appl Environ Microbiol 2008; 74: 5621–5627.

    Article  CAS  Google Scholar 

  29. Francois P, Pittet D, Bento M, Pepey B, Vaudaux P, Lew D et al. Rapid detection of methicillin-resistant Staphylococcus aureus directly from sterile or nonsterile clinical samples by a new molecular assay. J Clin Microbiol 2003; 41: 254–260.

    Article  CAS  Google Scholar 

  30. Van Meurs ML, Schellekens JJ, De Neeling AJ, Duim B, Schneeberger PM, Hermans MH . Real-time PCR to distinguish livestock-associated (ST398) from non-livestock-associated (methicillin-resistant) Staphylococcus aureus. Infection 2013; 41: 339–346.

    Article  CAS  Google Scholar 

  31. Tulinski P, Fluit AC, Wagenaar JA, Mevius DJ, Van de Vijver L, Duim B . Methicillin-resistant coagulase-negative staphylococci on pig farms as a reservoir of heterogeneous staphylococcal cassette chromosome mec elements. Appl Environ Microbiol 2012; 78: 299–304.

    Article  CAS  Google Scholar 

  32. Kilic A, Muldrew KL, Tang YW, Basustaoglu AC . Triplex real-time polymerase chain reaction assay for simultaneous detection of Staphylococcus aureus and coagulase-negative staphylococci and determination of methicillin resistance directly from positive blood culture bottles. Diagn Microbiol Infect Dis 2010; 66: 349–355.

    Article  CAS  Google Scholar 

  33. Van Leeuwen W, Roorda L, Hendriks W, Francois P, Schrenzel J . A nuc-deficient methicillin-resistant Staphylococcus aureus strain. FEMS Immunol Med Microbiol 2008; 54: 157.

    Article  CAS  Google Scholar 

  34. Den Heijer CDJ, van Bijnen EME, Paget WJ, Pringle M, Goossens H, Bruggeman CA et al. Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S aureus, in nine European countries: a cross-sectional study. Lancet Infect Dis 2013; 13: 409–415.

    Article  Google Scholar 

  35. Verkade E, van Benthem B, den Bergh MK, van Cleef B, van Rijen M, Bosch T et al. Dynamics and determinants of Staphylococcus aureus carriage in livestock veterinarians: a prospective cohort study. Clin Infect Dis 2013; 57: e11–e17.

    Article  Google Scholar 

  36. Tebbens BD . Personal dosimetry versus environmental monitoring. J Occup Med 1973; 15: 639–641.

    CAS  PubMed  Google Scholar 

  37. Stevens DC . The particle size and mean concentrations of radioactive aerosols measured by personal and static air samples. Ann Occup Hyg 1969; 12: 33–40.

    CAS  PubMed  Google Scholar 

  38. Broens EM, Graat EA, van der Wolf PJ, van de Giessen AW, van Duijkeren E, Wagenaar JA et al. MRSA CC398 in the pig production chain. Prev Vet Med 2011; 98: 182–189.

    Article  CAS  Google Scholar 

  39. Bos MEH, Graveland H, Portengen L, Wagenaar JA, Heederik DJ . Livestock-associated MRSA prevalence in veal calf production is associated with farm hygiene, use of antimicrobials, and age of the calves. Prev Vet Med 2012; 105: 155–159.

    Article  Google Scholar 

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Acknowledgements

We would like to acknowledge all field workers and laboratory assistants, especially Isabella Oosting-van Schothorst, Arjen Timmerman and Marian Broekhuizen-Stins. The research included in this paper was funded by Senter Novem, The Netherlands Organization for Health Research and Development (ZonMw) (grant numbers 125020009 and 505170098053), the Product Boards for Livestock Meat and Eggs, and the Dutch Ministry of Agriculture Nature and Food Quality (POM and BACTOPATH projects).

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Authors and Affiliations

  1. Division of Environmental Epidemiology, Institute for Risk Assessment Sciences, Utrecht University, Utrecht, The Netherlands

    Marian E H Bos, Wietske Dohmen, Alejandro Dorado-García, Haitske Graveland & Dick J J Heederik

  2. Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands

    Koen M Verstappen, Alejandro Dorado-García, Birgitta Duim & Jaap A Wagenaar

  3. Central Veterinary Institute of Wageningen UR, Lelystad, The Netherlands

    Jaap A Wagenaar

  4. Laboratory for Medical Microbiology and Immunology, St. Elisabeth Hospital, Tilburg, The Netherlands

    Brigitte A G L van Cleef & Jan A J W Kluytmans

  5. Laboratory for Microbiology and Infection Control, Amphia Hospital, Breda, The Netherlands

    Brigitte A G L van Cleef & Jan A J W Kluytmans

  6. Department of Medical Microbiology and Infection Control, VU University Medical Center, Amsterdam, The Netherlands

    Jan A J W Kluytmans

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  1. Marian E H Bos
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Correspondence to Marian E H Bos.

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Bos, M., Verstappen, K., van Cleef, B. et al. Transmission through air as a possible route of exposure for MRSA. J Expo Sci Environ Epidemiol 26, 263–269 (2016). https://doi.org/10.1038/jes.2014.85

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