Recent Research on Occupational Animal Exposures and Health Risks: A Narrative Review

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Silbergeld EK. Chickenizing farms and food: how industrial meat production endangers workers, animals, and consumers. Baltimore: JHU Press; 2016.

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Leibler JH, Otte J, Roland-Holst D, Pfeiffer DU, Soares Magalhaes R, Rushton J, et al. Industrial food animal production and global health risks: exploring the ecosystems and economics of avian influenza. EcoHealth. 2009;6:58–70.

Brooks JP, Adeli A, McLaughlin MR. Microbial ecology, bacterial pathogens, and antibiotic resistant genes in swine manure wastewater as influenced by three swine management systems. Water Res. 2014;57:96–103.

Spencer JL, Guan J. Public health implications related to spread of pathogens in manure from livestock and poultry operations. Methods Mol Biol Clifton NJ. 2004;268:503–15.

Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG Jr. Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci U S A. 2002;99:6434–9.

Harper AL, Ferguson DD, Leedom Larson KR, Hanson BM, Male MJ, Donham KJ, et al. An overview of livestock-associated MRSA in agriculture. J Agromedicine. 2010;15:101–4.

Koch BJ, Hungate BA, Price LB. Food-animal production and the spread of antibiotic resistance: the role of ecology. Front Ecol Environ. 2017.

Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio [Internet]. 2012 [cited 2012 Aug 7];3. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22354957

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Hogerwerf L, Wallace RG, Ottaviani D, Slingenbergh J, Prosser D, Bergmann L, et al. Persistence of highly pathogenic avian influenza H5N1 virus defined by agro- ecological niche. EcoHealth. 2010;7:213–25.

Brockwell-Staats C, Webster RG, Webby RJ. Diversity of influenza viruses in swine and the emergence of a novel human pandemic influenza A (H1N1). Influenza Other Respir Viruses. 2009;3:207–13.

Gray GC, Trampel DW, Roth JA. Pandemic influenza planning: shouldn’t swine and poultry workers be included? Vaccine. 2007b;25:4376–81.

Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP, Moritz ED, et al. Methicillin- resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PloS One. 2009;4:e4258.

Castillo Neyra R, Frisancho JA, Rinsky JL, Resnick C, Carroll KC, Rule AM, et al. Multidrug-resistant and methicillin-resistant Staphylococcus aureus (MRSA) in hog slaughter and processing plant workers and their community in North Carolina (USA). Environ Health Perspect. 2014;122.

Blood, Sweat and Fear: Workers’ Rights in US Meat and Poultry Plants.

Grzywacz JG, Alterman T, Muntaner C, Gabbard S, Nakamoto J, Carroll DJ. Measuring job characteristics and mental health among Latino farmworkers: results from cognitive testing. J Immigr Minor Health. 2009;11:131–8.

Hiott AE, Grzywacz JG, Davis SW, Quandt SA, Arcury TA. Migrant farmworker stress: mental health implications. J Rural Health Off J Am Rural Health Assoc Natl Rural Health Care Assoc. 2008;24:32–9.

Reynolds SJ, Nonnenmann MW, Basinas I, Davidson M, Elfman L, Gordon J, et al. Systematic review of respiratory health among dairy workers. J Agromedicine. 2013;18:219–43.

Ramos AK, Carlo G, Grant K, Trinidad N, Correa A. Stress, depression, and occupational injury among migrant farmworkers in Nebraska. Saf Basel Switz. 2016;2:23.

Mazurek JM, Henneberger PK. Lifetime allergic rhinitis prevalence among US primary farm operators: findings from the 2011 Farm and Ranch Safety survey. Int Arch Occup Environ Health. 2017;90:507–15.

Bradman A, Whitaker D, Quiros L, Castorina R, Claus Henn B, Nishioka M, et al. Pesticides and their metabolites in the homes and urine of farmworker children living in the Salinas Valley. CA. J Expo Sci Environ Epidemiol. 2007;17:331–49.

Sanborn M, Kerr KJ, Sanin LH, Cole DC, Bassil KL, Vakil C. Non-cancer health effects of pesticides: systematic review and implications for family doctors. Can Fam Physician Med Fam Can. 2007;53:1712–20.

Tanner CM, Kamel F, Ross GW, Hoppin JA, Goldman SM, Korell M, et al. Rotenone, paraquat, and Parkinson’s disease. Environ Health Perspect. 2011;119:866–72.

Kamel F, Goldman SM, Umbach DM, Chen H, Richardson G, Barber MR, et al. Dietary fat intake, pesticide use, and Parkinson’s disease. Parkinsonism Relat Disord. 2014;20:82–7.

Gustafsson B. The health and safety of workers in a confined animal system. Livest Prod Sci. 1997;49:191–202.

Linaker C, Smedley J. Respiratory illness in agricultural workers. Occup Med. 2002;52:451–9.

Odetokun IA, Ballhausen B, Adetunji VO, Ghali-Mohammed I, Adelowo MT, Adetunji SA, et al. Staphylococcus aureus in two municipal abattoirs in Nigeria: risk perception, spread and public health implications. Vet Microbiol. 2018;216:52–9.

Amoako DG, Somboro AM, Abia ALK, Allam M, Ismail A, Bester L, et al. Genomic analysis of methicillin-resistant Staphylococcus aureus isolated from poultry and occupational farm workers in Umgungundlovu District. South Africa. Sci Total Environ. 2019;670:704–16.

Chen C-J, Lauderdale T-LY LC-T, Chuang Y-Y, Yang C-C, Wu T-S, et al. Clinical and molecular features of MDR livestock-associated MRSA ST9 with staphylococcal cassette chromosome mecXII in humans. J Antimicrob Chemother. 2018;73:33–40.

Founou LL, Founou RC, Allam M, Ismail A, Finyom Djoko C, Essack SY. Genome analysis of methicillin-resistant Staphylococcus aureus isolated from pigs: detection of the clonal lineage ST398 in Cameroon and South Africa. Zoonoses Public Health. 2019.

Parisi A, Caruso M, Normanno G, Latorre L, Miccolupo A, Fraccalvieri R, et al. MRSA in swine, farmers and abattoir workers in Southern Italy. Food Microbiol. 2019;82:287–93.

Sahibzada S, Hernandez-Jover M, Jordan D, Thomson PC, Heller J. Emergence of highly prevalent CA-MRSA ST93 as an occupational risk in people working on a pig farm in Australia. PloS One. 2018;13:e0195510.

Stewart-Johnson A, Dziva F, Abdela W, Rahaman S, Adesiyun A. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in broilers and workers at “pluck shops” in Trinidad. Trop Anim Health Prod. 2019;51:369–72.

Dang STT, Bortolaia V, Tran NT, Le HQ, Dalsgaard A. Cephalosporin-resistant Escherichia coli isolated from farm workers and pigs in northern Vietnam. Trop Med Int Health TM IH. 2018;23:415–24.

Borkenhagen LK, Mallinson KA, Tsao RW, Ha S-J, Lim W-H, Toh T-H, et al. Surveillance for respiratory and diarrheal pathogens at the human-pig interface in Sarawak. Malaysia. PloS One. 2018;13:e0201295.

•• Ma M-J, Wang G-L, Anderson BD, Bi Z-Q, Lu B, Wang X-J, et al. Evidence for cross-species influenza A virus transmission within swine farms, China: A One Health, Prospective Cohort Study. Clin Infect Dis Off Publ Infect Dis Soc Am. 2018;66:533–40 The authors identified cross-species transmission of human-adapted H1N1 viruses and swine-adapted H3N2 viruses in both swine and swine workers in China, highlighting continued pandemic influenza risk from swine production in this region. The authors also noted symptomatic influenza-like illness among workers using a longitudinal design, indicating that these zoonotic viruses are pathogenic to humans.

Abdelbaset AE, Abushahba MFN, Hamed MI, Rawy MS. Sero-diagnosis of brucellosis in sheep and humans in Assiut and El-Minya governorates. Egypt. Int J Vet Sci Med. 2018;6:S63–7.

Brookes VJ, Gill GS, Singh BB, Sandhu BS, Dhand NK, Aulakh RS, et al. Challenges to human rabies elimination highlighted following a rabies outbreak in bovines and a human in Punjab. India. Zoonoses Public Health. 2019;66:325–36.

Geng Y, Zhao C, Geng K, Wang C, Wang X, Liu H, et al. High seroprevalence of hepatitis E virus in rabbit slaughterhouse workers. Transbound Emerg Dis. 2019;66:1085–9.

Khounvisith V, Tritz S, Khenkha L, Phoutana V, Keosengthong A, Pommasichan S, et al. High circulation of hepatitis E virus in pigs and professionals exposed to pigs in Laos. Zoonoses Public Health. 2018;65:1020–6.

Msimang V, Thompson PN, Jansen van Vuren P, Tempia S, Cordel C, Kgaladi J, et al. Rift Valley fever virus exposure amongst farmers, farm workers, and veterinary professionals in Central South Africa. Viruses. 2019:11.

Cuny C, Layer F, Kock R, Werner G, Witte W. Methicillin susceptible Staphylococcus aureus (MSSA) of clonal complex CC398, t571 from infections in humans are still rare in Germany. PloS One. 2013;8:e83165.

Zhou X, Wang Y, Liu H, Guo F, Doi SA, Smith C, et al. Effectiveness of market- level biosecurity at reducing exposure of poultry and humans to avian influenza: a systematic review and meta-Analysis. J Infect Dis. 2018;218:1861–75.

Bailey ES, Choi JY, Fieldhouse JK, Borkenhagen LK, Zemke J, Zhang D, et al. The continual threat of influenza virus infections at the human-animal interface: what is new from a one health perspective? Evol Med Public Health. 2018;2018:192–8.

• Davidson ME, Schaeffer J, Clark ML, Magzamen S, Brooks EJ, Keefe TJ, et al. Personal exposure of dairy workers to dust, endotoxin, muramic acid, ergosterol, and ammonia on large-scale dairies in the high plains Western United States. J Occup Environ Hyg. 2018;15:182–93 The authors conducted personal exposure monitoring for multiple airborne irritants and toxins among dairy workers in the Western US, and considered exposure-by-exposure mixtures, setting the stage for future work on complex exposure mixtures in this industry.

•• Lee MK, Carnes MU, Butz N, Azcarate-Peril MA, Richards M, Umbach DM, et al. Exposures related to house dust microbiota in a U.S. farming population. Environ Health Perspect. 2018;126:067001-13 The authors evaluated microbial composition of household dust using 16s technology and compared findings to endotoxin levels. This study marks an early foray into microbiome research for understanding health effects associated with occupational exposure to animals.

Viegas C, Monteiro A, Ribeiro E, Caetano LA, Carolino E, Assuncao R, et al. Organic dust exposure in veterinary clinics: a case study of a small-animal practice in Portugal. Arh Hig Rada Toksikol. 2018;69:309–16.

Chmielowiec-Korzeniowska A, Tymczyna L, Pyrz M, Trawinska B, Abramczyk K, Dobrowolska M. Occupational exposure level of pig facility workers to chemical and biological pollutants. Ann Agric Environ Med AAEM. 2018;25:262–7.

El-Zaemey S, Carey RN, Darcey E, Reid A, Glass DC, Benke GP, et al. Prevalence of occupational exposure to asthmagens derived from animals, fish and/or shellfish among Australian workers. Occup Environ Med. 2018;75:310–6.

Jeebhay MF, Moscato G, Bang BE, Folletti I, Lipinska-Ojrzanowska A, Lopata AL, et al. Food processing and occupational respiratory allergy-A EAACI Position Paper. Allergy. 2019.

Pouchieu C, Piel C, Carles C, Gruber A, Helmer C, Tual S, et al. Pesticide use in agriculture and Parkinson’s disease in the AGRICAN cohort study. Int J Epidemiol. 2018;47:299–310.

Darcey E, Carey RN, Reid A, Driscoll T, Glass DC, Benke GP, et al. Prevalence of exposure to occupational carcinogens among farmers. Rural Remote Health. 2018;18:4348.

Hofmann JN, Shiels MS, Friesen MC, Kemp TJ, Chaturvedi AK, Lynch CF, et al. Industrial hog farming is associated with altered circulating immunological markers. Occup Environ Med. 2018;75:212–7.

Ramos AK, Fuentes A, Carvajal-Suarez M. Self-reported occupational injuries and perceived occupational health problems among Latino immigrant swine confinement workers in Missouri. J Environ Public Health. 2018;2018:8710901.

Clouser JM, Bush A, Gan W, Swanberg J. Associations of work stress, supervisor unfairness, and supervisor inability to speak Spanish with occupational injury among Latino farmworkers. J Immigr Minor Health. 2018;20:894–901.

Bush AM, Westneat S, Browning SR, Swanberg J. Missed work due to occupational illness among Hispanic horse workers. J Agric Saf Health. 2018;24:89–107.

Liebman A, Franko E, Reyes I, Keifer M, Sorensen J. An overview and impact assessment of OSHA large dairy local emphasis programs in New York and Wisconsin. Am J Ind Med. 2018;61:658–66. https://doi.org/10.1002/ajim.22868.

Rodriguez A, Hagevoort GR, Leal D, Pompeii L, Douphrate DI. Using mobile technology to increase safety awareness among dairy workers in the United States. J Agromedicine. 2018;23:315–26.

Caffaro F, Micheletti Cremasco M, Bagagiolo G, Vigoroso L, Cavallo E. Effectiveness of occupational safety and health training for migrant farmworkers: a scoping review. Public Health. 2018;160:10–7.

Cuny C, Layer F, Hansen S, Werner G, Witte W. Nasal colonization of humans with occupational exposure to raw meat and to raw meat products with methicillin-susceptible and methicillin-resistant Staphylococcus aureus. Toxins (Basel). 2019; 11:190.