Advertisement

Aerobiologia

pp 1–14 | Cite as

Quantification of airborne dust, endotoxins, human pathogens and antibiotic and metal resistance genes in Eastern Canadian swine confinement buildings

  • Jonathan Pilote
  • Valérie Létourneau
  • Matthieu Girard
  • Caroline DuchaineEmail author
Original Paper
  • 24 Downloads

Abstract

Pig farming practices in Eastern Canada changed drastically into intensified and specialized operations. In large confined finishing facilities, workers are now exposed to concentrated biological particles (bioaerosols) for prolonged periods of time. Occupational exposure to airborne dust, endotoxins, bacteria, human pathogenic agents (Staphylococcus aureus, methicillin-resistant S. aureus, Salmonella spp., Mycobacterium avium, Clostridium difficile and Listeria monocytogenes), and antibiotic and metal resistance genes (cephalosporin, colistin, zinc) were investigated in 10 swine confinement buildings (SCBs). Average concentration in SCBs for airborne total dust and endotoxins was 3.62 mg/m3 and 9.03 × 103 EU/m3, respectively. All the human pathogenic agents and resistance genes investigated in this study were detected in bioaerosols of at least one SCB, with S. aureus and czrC gene (zinc resistance) being recovered from all buildings. A colistin resistance gene (mcr-1) was found in 6 out of 10 SCBs despite restricted use of the antimicrobial agent in Eastern Canadian swine herds. The present study reinforces the fact that SCBs contain bioaerosols that may contribute to the development of adverse health effects among workers.

Keywords

Pig buildings Occupational exposure Bioaerosols Methicillin-resistant Staphylococcus aureus Clostridium difficile Antimicrobial resistance 

Notes

Acknowledgements

The authors would like to thank the participating swine producers and the Institut de recherche Robert-Sauvé en santé et en sécurité au travail (IRSST) and Agriculture and Agri-Food Canada (AAC) for financial support. The research activities were carried out under the Canadian AgriSafety Applied Research Program of AAC coordinated and administered by Agrivita Canada Inc.

References

  1. Aarnisalo, K., Salo, S., Miettinen, H., Suihko, M. L., Wirtanen, G., Autio, T., et al. (2000). Bactericidal efficiencies of commercial disinfectants against Listeria monocytogenes on surfaces. Journal of Food Safety, 20(4), 237–250.  https://doi.org/10.1111/j.1745-4565.2000.tb00302.x.Google Scholar
  2. ACGIH. (2014). TLVs and BEIs. Cincinnati, OH: American Conference of Governmental Industrial Hygienists.Google Scholar
  3. Agerso, Y., Hasman, H., Cavaco, L. M., Pedersen, K., & Aarestrup, F. M. (2012). Study of methicillin resistant Staphylococcus aureus (MRSA) in Danish pigs at slaughter and in imported retail meat reveals a novel MRSA type in slaughter pigs. Veterinary Microbiology, 157(1–2), 246–250.  https://doi.org/10.1016/j.vetmic.2011.12.023.Google Scholar
  4. Akhtar, M., Viazis, S., Christensen, K., Kraemer, P., & Diez-Gonzalez, F. (2017). Isolation, characterization and evaluation of virulent bacteriophages against Listeria monocytogenes. Food Control, 75, 108–115.  https://doi.org/10.1016/j.foodcont.2016.12.035.Google Scholar
  5. Argudin, M. A., Lauzat, B., Kraushaar, B., Alba, P., Agerso, Y., Cavaco, L., et al. (2016). Heavy metal and disinfectant resistance genes among livestock-associated methicillin-resistant Staphylococcus aureus isolates. Veterinary Microbiology, 191, 88–95.  https://doi.org/10.1016/j.vetmic.2016.06.004.Google Scholar
  6. Bach, H. J., Tomanova, J., Schloter, M., & Munch, J. C. (2002). Enumeration of total bacteria and bacteria with genes for proteolytic activity in pure cultures and in environmental samples by quantitative PCR mediated amplification. Journal of Microbiological Methods, 49(3), 235–245.Google Scholar
  7. Bandelj, P., Logar, K., Usenik, A. M., Vengust, M., & Ocepek, M. (2013). An improved qPCR protocol for rapid detection and quantification of Clostridium difficile in cattle feces. FEMS Microbiology Letters, 341(2), 115–121.  https://doi.org/10.1111/1574-6968.12102.Google Scholar
  8. Biswas, S., Brunel, J. M., Dubus, J. C., Reynaud-Gaubert, M., & Rolain, J. M. (2012). Colistin: An update on the antibiotic of the 21st century. Expert Review of Anti-infective Therapy, 10(8), 917–934.  https://doi.org/10.1586/eri.12.78.Google Scholar
  9. Boscher, E., Houard, E., & Denis, M. (2012). Prevalence and distribution of Listeria monocytogenes serotypes and pulsotypes in sows and fattening pigs in farrow-to-finish farms (France, 2008). Journal of Food Protection, 75(5), 889–895.  https://doi.org/10.4315/0362-028X.JFP-11-340.Google Scholar
  10. Boyen, F., Haesebrouck, F., Vanparys, A., Volf, J., Mahu, M., Van Immerseel, F., et al. (2008). Coated fatty acids alter virulence properties of Salmonella Typhimurium and decrease intestinal colonization of pigs. Veterinary Microbiology, 132(3–4), 319–327.  https://doi.org/10.1016/j.vetmic.2008.05.008.Google Scholar
  11. Cartwright, E. J., Jackson, K. A., Johnson, S. D., Graves, L. M., Silk, B. J., & Mahon, B. E. (2013). Listeriosis outbreaks and associated food vehicles, United States, 1998–2008. Emerging Infectious Diseases, 19(1), 1–9.  https://doi.org/10.3201/eid1901.120393. (quiz 184).Google Scholar
  12. Cavaco, L. M., Hasman, H., Stegger, M., Andersen, P. S., Skov, R., Fluit, A. C., et al. (2010). Cloning and occurrence of czrC, a gene conferring cadmium and zinc resistance in methicillin-resistant Staphylococcus aureus CC398 isolates. Antimicrobial Agents and Chemotherapy, 54(9), 3605–3608.  https://doi.org/10.1128/AAC.00058-10.Google Scholar
  13. Cohen, S. H., Gerding, D. N., Johnson, S., Kelly, C. P., Loo, V. G., McDonald, L. C., et al. (2010). Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infection Control and Hospital Epidemiology, 31(5), 431–455.  https://doi.org/10.1086/651706.Google Scholar
  14. Coombs, G. W., Nimmo, G. R., Bell, J. M., Huygens, F., O’Brien, F. G., Malkowski, M. J., et al. (2004). Genetic diversity among community methicillin-resistant Staphylococcus aureus strains causing outpatient infections in Australia. Journal of Clinical Microbiology, 42(10), 4735–4743.  https://doi.org/10.1128/JCM.42.10.4735-4743.2004.Google Scholar
  15. Coque, T. M., Novais, A., Carattoli, A., Poirel, L., Pitout, J., Peixe, L., et al. (2008). Dissemination of clonally related Escherichia coli strains expressing extended-spectrum beta-lactamase CTX-M-15. Emerging Infectious Diseases, 14(2), 195–200.  https://doi.org/10.3201/eid1402.070350.Google Scholar
  16. Cormier, Y., Boulet, L. P., Bedard, G., & Tremblay, G. (1991). Respiratory health of workers exposed to swine confinement buildings only or to both swine confinement buildings and dairy barns. Scandinavian Journal of Work, Environment and Health, 17(4), 269–275.Google Scholar
  17. Cousins, D. V., Wilton, S. D., Francis, B. R., & Gow, B. L. (1992). Use of polymerase chain reaction for rapid diagnosis of tuberculosis. Journal of Clinical Microbiology, 30(1), 255–258.Google Scholar
  18. Crook, B., Robertson, J. F., Glass, S. A., Botheroyd, E. M., Lacey, J., & Topping, M. D. (1991). Airborne dust, ammonia, microorganisms, and antigens in pig confinement houses and the respiratory health of exposed farm workers. American Industrial Hygiene Association Journal, 52(7), 271–279.  https://doi.org/10.1080/15298669191364721.Google Scholar
  19. Desneux, J., Biscuit, A., Picard, S., & Pourcher, A. M. (2016). Fate of viable but non-culturable Listeria monocytogenes in pig manure microcosms. Frontiers in Microbiology, 7, 245.  https://doi.org/10.3389/fmicb.2016.00245.Google Scholar
  20. Donham, K., Haglind, P., Peterson, Y., Rylander, R., & Belin, L. (1989). Environmental and health studies of farm workers in Swedish swine confinement buildings. British Journal of Industrial Medicine, 46(1), 31–37.Google Scholar
  21. Dore, K., Buxton, J., Henry, B., Pollari, F., Middleton, D., Fyfe, M., et al. (2004). Risk factors for Salmonella Typhimurium DT104 and non-DT104 infection: A Canadian multi-provincial case-control study. Epidemiology and Infection, 132(3), 485–493.Google Scholar
  22. Duchaine, C., Grimard, Y., & Cormier, Y. (2000). Influence of building maintenance, environmental factors, and seasons on airborne contaminants of swine confinement buildings. AIHAJ, 61(1), 56–63.Google Scholar
  23. Duchaine, C., Thorne, P. S., Meriaux, A., Grimard, Y., Whitten, P., & Cormier, Y. (2001). Comparison of endotoxin exposure assessment by bioaerosol impinger and filter-sampling methods. Applied and Environment Microbiology, 67(6), 2775–2780.  https://doi.org/10.1128/AEM.67.6.2775-2780.2001.Google Scholar
  24. Espinosa-Gongora, C., Dahl, J., Elvstrom, A., van Wamel, W. J., & Guardabassi, L. (2015). Individual predisposition to Staphylococcus aureus colonization in pigs on the basis of quantification, carriage dynamics, and serological profiles. Applied and Environment Microbiology, 81(4), 1251–1256.  https://doi.org/10.1128/AEM.03392-14.Google Scholar
  25. Fallschissel, K., Kampfer, P., & Jackel, U. (2009). Direct detection of salmonella cells in the air of livestock stables by real-time PCR. Annals of Occupational Hygiene, 53(8), 859–868.  https://doi.org/10.1093/annhyg/mep060.Google Scholar
  26. Fischer, O. A., Matlova, L., Bartl, J., Dvorska, L., Svastova, P., du Maine, R., et al. (2003). Earthworms (Oligochaeta, Lumbricidae) and mycobacteria. Veterinary Microbiology, 91(4), 325–338.Google Scholar
  27. Flanagan, A. D. (1971). Adverse effects of sodium colistimethate. Annals of Internal Medicine, 74(1), 143–144.Google Scholar
  28. Fowler, V. G., Jr., Miro, J. M., Hoen, B., Cabell, C. H., Abrutyn, E., Rubinstein, E., et al. (2005). Staphylococcus aureus endocarditis: A consequence of medical progress. JAMA, 293(24), 3012–3021.  https://doi.org/10.1001/jama.293.24.3012.Google Scholar
  29. Frazee, B. W., Lynn, J., Charlebois, E. D., Lambert, L., Lowery, D., & Perdreau-Remington, F. (2005). High prevalence of methicillin-resistant Staphylococcus aureus in emergency department skin and soft tissue infections. Annals of Emergency Medicine, 45(3), 311–320.  https://doi.org/10.1016/j.annemergmed.2004.10.011.Google Scholar
  30. Fritz, S. A., Garbutt, J., Elward, A., Shannon, W., & Storch, G. A. (2008). Prevalence of and risk factors for community-acquired methicillin-resistant and methicillin-sensitive staphylococcus aureus colonization in children seen in a practice-based research network. Pediatrics, 121(6), 1090–1098.  https://doi.org/10.1542/peds.2007-2104.Google Scholar
  31. Gao, R., Li, Y., Lin, J., Tan, C., & Feng, Y. (2016). Unexpected complexity of multidrug resistance in the mcr-1-harbouring Escherichia coli. Science China Life Sciences, 59(7), 732–734.  https://doi.org/10.1007/s11427-016-5070-1.Google Scholar
  32. Gaskins, H. R., Collier, C. T., & Anderson, D. B. (2002). Antibiotics as growth promotants: Mode of action. Animal Biotechnology, 13(1), 29–42.  https://doi.org/10.1081/ABIO-120005768.Google Scholar
  33. Gouvernement du Québec. (2018). Schedule A, Regulation respecting the quality of the work environment (chapter S-2.1, r. 11), Act respecting occupational health and safety (chapter S-2.1, a. 223), Environment Quality Act (chapter Q-2). Québec, Canada.Google Scholar
  34. Goyer, N., Lavoie, J., Lazure, L., & Marchand, G. (2001). Les bioaérosols en milieu de travail : guide d’évaluation, de contrôle et de prévention. Montréal, QC: Institut de recherche Robert-Sauvé en santé et en sécurité du travail.Google Scholar
  35. Gravel, D., Miller, M., Simor, A., Taylor, G., Gardam, M., McGeer, A., et al. (2009). Health care-associated Clostridium difficile infection in adults admitted to acute care hospitals in Canada: A Canadian Nosocomial Infection Surveillance Program Study. Clinical Infectious Diseases, 48(5), 568–576.  https://doi.org/10.1086/596703.Google Scholar
  36. Hassan, M. T., van der Lelie, D., Springael, D., Romling, U., Ahmed, N., & Mergeay, M. (1999). Identification of a gene cluster, czr, involved in cadmium and zinc resistance in Pseudomonas aeruginosa. Gene, 238(2), 417–425.Google Scholar
  37. Hedelin, A. S., Sundblad, B. M., Sahlander, K., Wilkinson, K., Seisenbaeva, G., Kessler, V., et al. (2016). Comparing human respiratory adverse effects after acute exposure to particulate matter in conventional and particle-reduced swine building environments. Occupational and Environmental Medicine, 73(10), 648–655.  https://doi.org/10.1136/oemed-2015-103522.Google Scholar
  38. Heederik, D., & Douwes, J. (1997). Towards an occupational exposure limit for endotoxins? Annals of Agricultural and Environmental Medicine, 4(1), 17–19.Google Scholar
  39. Hendriksen, S. W., Orsel, K., Wagenaar, J. A., Miko, A., & van Duijkeren, E. (2004). Animal-to-human transmission of Salmonella Typhimurium DT104A variant. Emerging Infectious Diseases, 10(12), 2225–2227.  https://doi.org/10.3201/eid1012.040286.Google Scholar
  40. Hibiya, K., Kazumi, Y., Nishiuchi, Y., Sugawara, I., Miyagi, K., Oda, Y., et al. (2010). Descriptive analysis of the prevalence and the molecular epidemiology of Mycobacterium avium complex-infected pigs that were slaughtered on the main island of Okinawa. Comparative Immunology, Microbiology and Infectious Diseases, 33(5), 401–421.  https://doi.org/10.1016/j.cimid.2009.03.002.Google Scholar
  41. Hitchins, A. D., Jinneman, K., & Chen, Y. (2017). Detection of Listeria monocytogenes in foods and environmental samples, and enumeration of Listeria monocytogenes in foods. In Bacteriological analytical manual. Silver Spring, MD: U.S. Food and Drug Administration.Google Scholar
  42. Hopman, N. E., Keessen, E. C., Harmanus, C., Sanders, I. M., van Leengoed, L. A., Kuijper, E. J., et al. (2011). Acquisition of Clostridium difficile by piglets. Veterinary Microbiology, 149(1–2), 186–192.  https://doi.org/10.1016/j.vetmic.2010.10.013.Google Scholar
  43. Horton, R. A., Randall, L. P., Snary, E. L., Cockrem, H., Lotz, S., Wearing, H., et al. (2011). Fecal carriage and shedding density of CTX-M extended-spectrum {beta}-lactamase-producing Escherichia coli in cattle, chickens, and pigs: Implications for environmental contamination and food production. Applied and Environment Microbiology, 77(11), 3715–3719.  https://doi.org/10.1128/AEM.02831-10.Google Scholar
  44. Huletsky, A., Giroux, R., Rossbach, V., Gagnon, M., Vaillancourt, M., Bernier, M., et al. (2004). New real-time PCR assay for rapid detection of methicillin-resistant Staphylococcus aureus directly from specimens containing a mixture of staphylococci. Journal of Clinical Microbiology, 42(5), 1875–1884.Google Scholar
  45. Inderlied, C. B., Kemper, C. A., & Bermudez, L. E. (1993). The Mycobacterium avium complex. Clinical Microbiology Reviews, 6(3), 266–310.Google Scholar
  46. Ito, T., Katayama, Y., & Hiramatsu, K. (1999). Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrobial Agents and Chemotherapy, 43(6), 1449–1458.Google Scholar
  47. Iversen, M., Kirychuk, S., Drost, H., & Jacobson, L. (2000). Human health effects of dust exposure in animal confinement buildings. Journal of Agricultural Safety and Health, 6(4), 283–288.Google Scholar
  48. Jarzembowski, J. A., & Young, M. B. (2008). Nontuberculous mycobacterial infections. Archives of Pathology and Laboratory Medicine, 132(8), 1333–1341.  https://doi.org/10.1043/1543-2165(2008)132%5b1333:NMI%5d2.0.CO;2.Google Scholar
  49. Jevons, M. P., Rolinson, G. N., & Knox, R. (1961). Celbenin-resistant staphylococci. British Medical Journal, 1(521), 124.  https://doi.org/10.1136/bmj.1.5219.124-a.Google Scholar
  50. Katayama, Y., Ito, T., & Hiramatsu, K. (2000). A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy, 44(6), 1549–1555.Google Scholar
  51. Keessen, E. C., Harmanus, C., Dohmen, W., Kuijper, E. J., & Lipman, L. J. (2013). Clostridium difficile infection associated with pig farms. Emerging Infectious Diseases, 19(6), 1032–1034.  https://doi.org/10.3201/eid1906.121645.Google Scholar
  52. Kich, J. D., Coldebella, A., Mores, N., Nogueira, M. G., Cardoso, M., Fratamico, P. M., et al. (2011). Prevalence, distribution, and molecular characterization of Salmonella recovered from swine finishing herds and a slaughter facility in Santa Catarina, Brazil. International Journal of food Microbiology, 151(3), 307–313.  https://doi.org/10.1016/j.ijfoodmicro.2011.09.024.Google Scholar
  53. Letourneau, V., Nehme, B., Meriaux, A., Masse, D., & Duchaine, C. (2010). Impact of production systems on swine confinement buildings bioaerosols. Journal of Occupational and Environmental Hygiene, 7(2), 94–102.  https://doi.org/10.1080/15459620903425642.Google Scholar
  54. Liu, Y. Y., Wang, Y., Walsh, T. R., Yi, L. X., Zhang, R., Spencer, J., et al. (2016). Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: A microbiological and molecular biological study. The Lancet Infectious Diseases, 16(2), 161–168.  https://doi.org/10.1016/S1473-3099(15)00424-7.Google Scholar
  55. Livermore, D. M. (1995). beta-Lactamases in laboratory and clinical resistance. Clinical Microbiology Reviews, 8(4), 557–584.Google Scholar
  56. Looft, T., Johnson, T. A., Allen, H. K., Bayles, D. O., Alt, D. P., Stedtfeld, R. D., et al. (2012). In-feed antibiotic effects on the swine intestinal microbiome. Proceedings of the National Academy of Sciences USA, 109(5), 1691–1696.  https://doi.org/10.1073/pnas.1120238109.Google Scholar
  57. Lu, Z., Wang, J., & Zhang, Y. (2012). Quantitative real-time PCR detection of airborne Staphylococcus aureus in hospital indoor atmosphere. Modern Applied Science, 6(3), 22–26.  https://doi.org/10.5539/mas.v6n3p22.Google Scholar
  58. Moodley, A., & Guardabassi, L. (2009). Transmission of IncN plasmids carrying blaCTX-M-1 between commensal Escherichia coli in pigs and farm workers. Antimicrobial Agents and Chemotherapy, 53(4), 1709–1711.  https://doi.org/10.1128/AAC.01014-08.Google Scholar
  59. Nagase, N., Sasaki, A., Yamashita, K., Shimizu, A., Wakita, Y., Kitai, S., et al. (2002). Isolation and species distribution of staphylococci from animal and human skin. Journal of Veterinary Medical Science, 64(3), 245–250.Google Scholar
  60. Nehme, B., Letourneau, V., Forster, R. J., Veillette, M., & Duchaine, C. (2008). Culture-independent approach of the bacterial bioaerosol diversity in the standard swine confinement buildings, and assessment of the seasonal effect. Environmental Microbiology, 10(3), 665–675.  https://doi.org/10.1111/j.1462-2920.2007.01489.x.Google Scholar
  61. Niederweis, M., Danilchanka, O., Huff, J., Hoffmann, C., & Engelhardt, H. (2010). Mycobacterial outer membranes: In search of proteins. Trends in Microbiology, 18(3), 109–116.  https://doi.org/10.1016/j.tim.2009.12.005.Google Scholar
  62. Nies, D. H. (1992). CzcR and CzcD, gene products affecting regulation of resistance to cobalt, zinc, and cadmium (czc system) in Alcaligenes eutrophus. Journal of Bacteriology, 174(24), 8102–8110.Google Scholar
  63. Nijhuis, R. H., Veldman, K. T., Schelfaut, J., Van Essen-Zandbergen, A., Wessels, E., Claas, E. C., et al. (2016). Detection of the plasmid-mediated colistin-resistance gene mcr-1 in clinical isolates and stool specimens obtained from hospitalized patients using a newly developed real-time PCR assay. Journal of Antimicrobial Chemotherapy, 71(8), 2344–2346.  https://doi.org/10.1093/jac/dkw192.Google Scholar
  64. Partridge, S. R., Zong, Z., & Iredell, J. R. (2011). Recombination in IS26 and Tn2 in the evolution of multiresistance regions carrying blaCTX-M-15 on conjugative IncF plasmids from Escherichia coli. Antimicrobial Agents and Chemotherapy, 55(11), 4971–4978.  https://doi.org/10.1128/AAC.00025-11.Google Scholar
  65. Pedersen, S., Nonnenmann, M., Rautiainen, R., Demmers, T. G., Banhazi, T., & Lyngbye, M. (2000). Dust in pig buildings. Journal of Agricultural Safety and Health, 6(4), 261–274.Google Scholar
  66. Poggenborg, R., Gaini, S., Kjaeldgaard, P., & Christensen, J. J. (2008). Streptococcus suis: Meningitis, spondylodiscitis and bacteraemia with a serotype 14 strain. Scandinavian Journal of Infectious Diseases, 40(4), 346–349.  https://doi.org/10.1080/00365540701716825.Google Scholar
  67. Powers, R. A., Caselli, E., Focia, P. J., Prati, F., & Shoichet, B. K. (2001). Structures of ceftazidime and its transition-state analogue in complex with AmpC beta-lactamase: Implications for resistance mutations and inhibitor design. Biochemistry, 40(31), 9207–9214.Google Scholar
  68. Pui, C. F., Wong, W. C., Chai, L. C., Nillian, E., Ghazali, F. M., Cheah, Y. K., et al. (2011). Simultaneous detection of Salmonella spp, Salmonella Typhi and Salmonella Typhimurium in sliced fruits using multiplex PCR. Food Control, 22(2), 337–342.  https://doi.org/10.1016/j.foodcont.2010.05.021.Google Scholar
  69. Radon, K., Monso, E., Weber, C., Danuser, B., Iversen, M., Opravil, U., et al. (2002). Prevalence and risk factors for airway diseases in farmers—Summary of results of the European Farmers’ Project. Annals of Agricultural and Environmental Medicine, 9(2), 207–213.Google Scholar
  70. Roschanski, N., Fischer, J., Guerra, B., & Roesler, U. (2014). Development of a multiplex real-time PCR for the rapid detection of the predominant beta-lactamase genes CTX-M, SHV, TEM and CIT-type AmpCs in Enterobacteriaceae. PLoS ONE, 9(7), e100956.  https://doi.org/10.1371/journal.pone.0100956.Google Scholar
  71. Shah, N. M., Davidson, J. A., Anderson, L. F., Lalor, M. K., Kim, J., Thomas, H. L., et al. (2016). Pulmonary Mycobacterium avium-intracellulare is the main driver of the rise in non-tuberculous mycobacteria incidence in England, Wales and Northern Ireland, 2007–2012. BMC Infectious Diseases, 16, 195.  https://doi.org/10.1186/s12879-016-1521-3.Google Scholar
  72. Skov, L., & Baadsgaard, O. (2000). Bacterial superantigens and inflammatory skin diseases. Clinical and Experimental Dermatology, 25(1), 57–61.Google Scholar
  73. Springer, B., Orendi, U., Much, P., Hoger, G., Ruppitsch, W., Krziwanek, K., et al. (2009). Methicillin-resistant Staphylococcus aureus: A new zoonotic agent? Wiener Klinische Wochenschrift, 121(3–4), 86–90.  https://doi.org/10.1007/s00508-008-1126-y.Google Scholar
  74. Statistics Canada. (2018). Table 32-10-0148-01 (formerly CANSIM 003-0103) Hogs statistics, number of farms reporting and average number of hogs per farm, semi-annual. https://www150.statcan.gc.ca/t1/tbl1/en/tv.action?pid=32100148012018. Accessed 17 Jan 2019.
  75. Sun, J., Yang, M., Sreevatsan, S., & Davies, P. R. (2015). Prevalence and characterization of Staphylococcus aureus in growing pigs in the USA. PLoS ONE, 10(11), e0143670.  https://doi.org/10.1371/journal.pone.0143670.Google Scholar
  76. Uhlemann, A. C., Porcella, S. F., Trivedi, S., Sullivan, S. B., Hafer, C., Kennedy, A. D., et al. (2012). Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio, 3(2), e00027.  https://doi.org/10.1128/mbio.00027-12.Google Scholar
  77. van der Mee-Marquet, N., Francois, P., Domelier-Valentin, A. S., Coulomb, F., Decreux, C., Hombrock-Allet, C., et al. (2011). Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France. Clinical Infectious Diseases, 52(1), 152–153.  https://doi.org/10.1093/cid/ciq053.Google Scholar
  78. Visek, W. J. (1978). Mode of growth promotion by antibiotics. Journal of Animal Science, 46(5), 1447–1469.Google Scholar
  79. Xu, W., Zheng, K., Meng, L. M., Liu, X. J., Hartung, E., Roelcke, M., et al. (2016). Concentrations and emissions of particulate matter from intensive pig production at a large farm in North China. Aerosol and Air Quality Research, 16(1), 79–90.  https://doi.org/10.4209/aaqr.2015.02.0078.Google Scholar
  80. Yang, X., Lee, J., Zhang, Y., Wang, X., & Yang, L. (2015). Concentration, size, and density of total suspended particulates at the air exhaust of concentrated animal feeding operations. Journal of the Air and Waste Management Association, 65(8), 903–911.  https://doi.org/10.1080/10962247.2015.1032446.Google Scholar
  81. Zhu, Y. G., Johnson, T. A., Su, J. Q., Qiao, M., Guo, G. X., Stedtfeld, R. D., et al. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences USA, 110(9), 3435–3440.  https://doi.org/10.1073/pnas.1222743110.Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Jonathan Pilote
    • 1
    • 2
  • Valérie Létourneau
    • 2
  • Matthieu Girard
    • 3
  • Caroline Duchaine
    • 1
    • 2
    Email author
  1. 1.Faculté des sciences et de génieUniversité LavalQuebecCanada
  2. 2.Centre de recherche de l’Institut universitaire de cardiologie et de pneumologie de QuébecUniversité LavalQuebecCanada
  3. 3.Institut de recherche et de développement en agroenvironnementQuebecCanada

Personalised recommendations