Potential Roles of the Nasal Microbiome in Pathogen Exposures in Dairy Workers

James Seidel , Grant Erlandson , Sheryl Magzamen , Zaid Abdo , Jessica H. Leibler , Jessica Nunez , Gregory C. Gray , Joshua W. Schaeffer

Zoonoses ›› 2025, Vol. 5 ›› Issue (1) : 36

PDF (1180KB)
Zoonoses ›› 2025, Vol. 5 ›› Issue (1) :36 DOI: 10.15212/ZOONOSES-2025-0012
ORIGINAL ARTICLE
research-article
Potential Roles of the Nasal Microbiome in Pathogen Exposures in Dairy Workers
Author information +
History +
PDF (1180KB)

Abstract

Objective: Livestock workers are exposed to bioaerosols comprising pathogens including influenza D virus (IDV), influenza A (IAV), and methicillin-resistant Staphylococcus aureus (MRSA), all of which can colonize the upper airways (e.g., anterior nares) and pose public health risks. The role of the nasal microbiome in occupational exposure is not well understood.

Methods: Here, we characterized the nasal microbiomes of US dairy workers to investigate the microbiome’s effects on pathogen carriage. We collected 237 lavages from 31 dairy workers to determine the presence of influenzas A, C, and D; methicillin-susceptible Staphylococcus aureus (MSSA); and MRSA. Nasal lavages were analyzed via PCR to quantify workers’ nasal microbiomes, and differences in microbiome characteristics were analyzed according to pathogen presence.

Results: Overall, 32.1% of lavages tested positive for MSSA, 11.4% tested positive for MRSA, 17.3% tested positive for IDV, 2.5% tested positive for IAV, and 1.3% tested positive for ICV. Nasal samples positive for IAV and those positive for MSSA clustered separately with robust Aitchison PCA, but no significant differences in alpha diversity were observed. Differential abundance analysis revealed significant differences in genera among lavages testing positive for MRSA, MSSA, IDV, and IAV (e.g., Staphylococcus, Streptococcus, and Bacillus).

Conclusions: Future work is needed to ascertain whether the microbiome might protect against pathogen exposures among livestock workers.

Keywords

Pathogens / influenza virus / MRSA / nasal microbiome / zoonoses / cattle / agricultural health / bioaerosols / nasal lavage

Cite this article

Download citation ▾
James Seidel, Grant Erlandson, Sheryl Magzamen, Zaid Abdo, Jessica H. Leibler, Jessica Nunez, Gregory C. Gray, Joshua W. Schaeffer. Potential Roles of the Nasal Microbiome in Pathogen Exposures in Dairy Workers. Zoonoses, 2025, 5 (1) : 36 DOI:10.15212/ZOONOSES-2025-0012

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

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(3): 219-243.

[2]

Donham KJ, Cumro D, Reynolds SJ, Merchant JA. Dose-response relationships between occupational aerosol exposures and cross-shift declines of lung function in poultry workers: recommendations for exposure limits. J Occup Environ Med. 2000; 42(3): 260-269.

[3]

Garcia J, Bennett DH, Tancredi D, Schenker MB, Mitchell D, Reynolds SJ, et al. Occupational exposure to particulate matter and endotoxin for California dairy workers. Int J Hyg Environ Health. 2013; 216(1): 56-62.

[4]

Bailey ES, Fieldhouse JK, Choi JY, Gray GC. A Mini review of the zoonotic threat potential of influenza viruses, coronaviruses, adenoviruses, and enteroviruses. Front Public Health. 2018; 6: 104.

[5]

Schenker MB. Inorganic agricultural dust exposure causes pneumoconiosis among farmworkers. Proc Am Thorac Soc. 2010; 7(2): 107-110.

[6]

Schaeffer JW, Reynolds S, Magzamen S, VanDyke A, Gottel NR, Gilbert JA, et al. Size, composition, and source profiles of inhalable bioaerosols from Colorado dairies. Environ Sci Technol. 2017; 51(11): 6430-6440.

[7]

Seidel J, Magzamen S, Wang YH, Neujahr V, Schaeffer JW. Lessons from dairy farmers for occupational allergy and respiratory disease. Curr Allergy Asthma Rep. 2023; 23(6): 325-239.

[8]

Martenies SE, Schaeffer JW, Erlandson G, Bradford M, Poole JA, Wilson A, et al. Associations between bioaerosol exposures and lung function changes among dairy workers in Colorado. J Occup Environ Med. 2020; 62(6): 427-430.

[9]

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(3): 182-193.

[10]

Leibler JH, Abdelgadir A, Seidel J, White RF, Johnson WE, Reynolds SJ, et al. Influenza D virus exposure among US cattle workers: a call for surveillance. Zoonoses Public Health. 2023; 70(2): 166-170.

[11]

Messenger AM, Barnes AN, Gray GC. Reverse zoonotic disease transmission (zooanthroponosis): a systematic review of seldom-documented human biological threats to animals. PLoS One. 2014; 9(2): e89055.

[12]

Fox J. The Threat of MRSA. Copenhagen, Denmark; 2015.

[13]

Trombetta CM, Marchi S, Manini I, Kistner O, Li F, Piu P, et al. Influenza D virus: serological evidence in the Italian population from 2005 to 2017. Viruses. 2019; 12(1): 30.

[14]

Larsen J, Petersen A, Sørum M, Stegger M, van Alphen L, Valentiner-Branth P, et al. Methicillin-resistant staphylococcus aureus CC398 is an increasing cause of disease in people with no livestock contact in Denmark, 1999 to 2011. Euro Surveill. 2015; 20(37): 9.

[15]

Bailey ES, Choi JY, Zemke J, Yondon M, Gray GC. Molecular surveillance of respiratory viruses with bioaerosol sampling in an airport. Trop Dis Travel Med Vaccines. 2018; 4: 11.

[16]

Khan SU, Anderson BD, Heil GL, Liang S, Gray GC. A systematic review and meta-analysis of the seroprevalence of influenza A(H9N2) infection among humans. J Infect Dis. 2015; 212(4): 562-569.

[17]

Butaye P, Argudín MA, Smith TC. Livestock-associated MRSA and its current evolution. Curr Clin Microbiol Rep. 2016; 3: 19-31.

[18]

Reynoso-García J, Miranda-Santiago AE, Meléndez-Vázquez NM, Acosta-Pagán K, Sánchez-Rosado M, Díaz-Rivera J, et al. A complete guide to human microbiomes: body niches, transmission, development, dysbiosis, and restoration. Front Syst Biol. 2022; 2: 951403.

[19]

Dimitri-Pinheiro S, Soares R, Barata P . The microbiome of the nose-friend or foe? Allergy Rhinol (Providence). 2020; 11: 215265672091160.

[20]

Camarinha-Silva A, Jáuregui R, Chaves-Moreno D, Oxley APA, Schaumburg F, Becker K, et al. Comparing the anterior nare bacterial community of two discrete human populations using Illumina amplicon sequencing. Environ Microbiol. 2014; 16(9): 2939-2952.

[21]

Shukla SK, Ye Z, Sandberg S, Reyes I, Fritsche TR, Keifer M. The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci. PLoS One. 2017; 12(8): e0183898.

[22]

Baker D, Chappelle D. Health status and needs of Latino dairy farmworkers in Vermont. J Agromedicine. 2012; 17(3): 277-287.

[23]

Dong TS, Gupta A. Influence of early life, diet, and the environment on the microbiome. Clin Gastroenterol Hepatol. 2019; 17(2): 231-242.

[24]

Domínguez-Díaz C, García-Orozco A, Riera-Leal A, Padilla-Arellano JR, Fafutis-Morris M. Microbiota and its role on viral evasion: is it with us or against us? Front Cell Infect Microbiol. 2019; 9: 256.

[25]

Lee KH, Gordon A, Shedden K, Kuan G, Ng S, Balmaseda A, et al. The respiratory microbiome and susceptibility to influenza virus infection. PLoS One. 2019; 14(1): e0207898.

[26]

Erlandson G, Magzamen S, Seidel J, Reynolds S, Jones K, Sharp J, et al. Impacts of a nasal rinse on inflammation and microbiome diversity in dairy workers. ISES 2022 Annual Meeting. Lisbon, Portugal; 2022.

[27]

Hudzicki J. Kirby-Bauer disk diffusion susceptibility test protocol. Washington, DC: American Society for Microbiology; 2009: 55-63.

[28]

Gray GC, Robie ER, Studstill CJ, Nunn CL. Mitigating future respiratory virus pandemics: new threats and approaches to consider. Viruses. 2021; 13(4): 637.

[29]

Erlandson G, Magzamen S, Sharp JL, Seidel J, Poole JA, Bradford M, et al. Hypertonic saline nasal rinse intervention: immunomodulatory effects in dairy workers. J Agromedicine. 2025; 30(1): 27-37.

[30]

Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019; 37(8): 852-857.

[31]

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016; 13(7): 581-583.

[32]

Robeson MS 2nd, O’Rourke DR, Kaehler BD, Ziemski M, Dillon MR, Foster JT, et al. RESCRIPt: Reproducible sequence taxonomy reference database management. PLoS Comput Biol. 2021; 17(11): e1009581.

[33]

Willis A, Bunge J. Estimating diversity via frequency ratios. Biometrics. 2015; 71(4): 1042-1049.

[34]

Martino C, Morton JT, Marotz CA, Thompson LR, Tripathi A, Knight R, et al. A novel sparse compositional technique reveals microbial perturbations. mSystems. 2019; 4(1): e00016-19.

[35]

McMurdie PJ, Holmes S. Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013; 8(4): e61217.

[36]

Shetty SA, Lahti L. Microbiomeutilities: utilities for microbiome analytics. 2020.

[37]

Cuny C, Wieler LH, Witte W. Livestock-associated MRSA: the impact on humans. Antibiotics (Basel). 2015; 4(4): 521-543.

[38]

Ingham AC, Urth TR, Sieber RN, Stegger M, Edslev SM, Angen Ø, et al. Dynamics of the human nasal microbiota and staphylococcus aureus CC398 carriage in pig truck drivers across one workweek. Appl Environ Microbiol. 2021; 87(18): e0122521.

[39]

Islam MZ, Johannesen TB, Lilje B, Urth TR, Larsen AR, Angen Ø, et al. Investigation of the human nasal microbiome in persons with long- and short-term exposure to methicillin-resistant Staphylococcus aureus and other bacteria from the pig farm environment . PLoS One. 2020; 15(4): e0232456.

[40]

Nadimpalli M, Stewart JR, Pierce E, Pisanic N, Love DC, Hall D, et al. Livestock-associated, antibiotic-resistant Staphylococcus aureus nasal carriage and recent skin and soft tissue infection among industrial hog operation workers . PLoS One. 2016; 11(11): e0165713.

[41]

Nadimpalli ML, Stewart JR, Pierce E, Pisanic N, Love DC, Hall D, et al. Face mask use and persistence of livestock-associated Staphylococcus aureus nasal carriage among industrial hog operation workers and household contacts, USA . Environ Health Perspect. 2018; 126(12): 127005.

[42]

Dulon M, Peters C, Schablon A, Nienhaus A. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. BMC Infect Dis. 2014; 14: 363.

[43]

Duong TB, Duong MC, Campbell JI, Nguyen HVM, Nguyen HH, Bui HTB, et al. MRSA carriage among healthcare workers in a Vietnamese intensive care unit: a prospective cohort study. Drug Target Insights. 2022; 16: 71-77.

[44]

Mainous AG 3rd, Hueston WJ, Everett CJ, Diaz VA. Nasal carriage of Staphylococcus aureus and methicillin-resistant S aureus in the United States, 2001-2002. Ann Fam Med. 2006; 4(2): 132-137.

[45]

Choi CS, Yin CS, Bakar AA, Sakewi Z, Naing NN, Jamal F, et al. Nasal carriage of Staphylococcus aureus among healthy adults. J Microbiol Immunol Infect. 2006; 39(6): 458-464.

[46]

Hause BM, Collin EA, Liu R, Huang B, Sheng Z, Lu W, et al. Characterization of a novel influenza virus in cattle and swine: proposal for a new genus in the Orthomyxoviridae family. mBio. 2014; 5(2):e00031-14.

[47]

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(1): 192-198.

[48]

Cookson B, Peters B, Webster M, Phillips I, Rahman M, Noble W. Staff carriage of epidemic methicillin-resistant Staphylococcus aureus . J Clin Microbiol. 1989; 27(7): 1471-1476.

[49]

Brito IL, Gurry T, Zhao S, Huang K, Young SK, Shea TP, et al. Transmission of human-associated microbiota along family and social networks. Nat Microbiol. 2019; 4(6): 964-971.

[50]

Ursell LK, Metcalf JL, Parfrey LW, Knight R. Defining the human microbiome. Nutr Rev. 2012; 70(Suppl 1): S38-S44.

[51]

Scher JU, Joshua V, Artacho A, Abdollahi-Roodsaz S, Öckinger J, Kullberg S, et al. The lung microbiota in early rheumatoid arthritis and autoimmunity. Microbiome. 2016; 4(1): 60.

[52]

Wu BG, Sulaiman I, Wang J, Shen N, Clemente JC, Li Y, et al. Severe obstructive sleep apnea is associated with alterations in the nasal microbiome and an increase in inflammation. Am J Respir Crit Care Med. 2019; 199(1): 99-109.

[53]

Kumpitsch C, Koskinen K, Schöpf V, Moissl-Eichinger C. The microbiome of the upper respiratory tract in health and disease. BMC Biol. 2019; 17(1): 87.

[54]

Choi EB, Hong SW, Kim DK, Jeon SG, Kim KR, Cho SH, et al. Decreased diversity of nasal microbiota and their secreted extracellular vesicles in patients with chronic rhinosinusitis based on a metagenomic analysis. Allergy. 2014; 69(4): 517-526.

[55]

Fazlollahi M, Lee TD, Andrade J, Oguntuyo K, Chun Y, Grishina G, et al. The nasal microbiome in asthma. J Allergy Clin Immunol. 2018; 142(3): 834-843.e2.

[56]

Wolff B, Boutin S, Lorenz H-M, Ueffing H, Dalpke A, Wolff D. FRI0698 Prevotella and alloprevotella species characterize the oral microbiome of early rheumatoid arthritis. Ann Rheum Dis. 2017; 76(Suppl 2): 754.

[57]

Omland Ø, Hjort C, Pedersen OF, Miller MR, Sigsgaard T. New-onset asthma and the effect of environment and occupation among farming and nonfarming rural subjects. J Allergy Clin Immunol. 2011; 128(4): 761-765.

[58]

Guilloux CA, Lamoureux C, Beauruelle C, Héry-Arnaud G. Porphyromonas: a neglected potential key genus in human microbiomes. Anaerobe. 2021; 68: 10223.

[59]

Hillman DR, Murphy AS, Pezzullo L. The economic cost of sleep disorders. Sleep. 2006; 29(3): 299-305.

[60]

Melamed S, Oksenberg A. Excessive daytime sleepiness and risk of occupational injuries in non-shift daytime workers. Sleep. 2002; 25(3): 315-322.

[61]

Reynolds AC, Coenen P, Lechat B, Straker L, Zabatiero J, Maddison KJ, et al. Insomnia and workplace productivity loss among young working adults: a prospective observational study of clinical sleep disorders in a community cohort. Med J Aust. 2023; 219(3): 107-112.

[62]

Hirsch Allen AJ, Park JE, Daniele PR, Fleetham J, Ryan CF, Ayas NT. Obstructive sleep apnoea and frequency of occupational injury. Thorax. 2016; 71(7): 664-666.

[63]

Douphrate DI, Nonnenmann MW, Hagevoort R, Gimeno Ruiz de Porras D. Work-related musculoskeletal symptoms and job factors among large-herd dairy milkers. J Agromedicine. 2016; 21(3): 224-233.

[64]

Brown K, Church D, Lynch T, Gregson D. Bloodstream infections due to Peptoniphilus spp.: report of 15 cases . Clin Microbiol Infect. 2014; 20(11): O857-O860.

[65]

Cobo F, Navarro-Marí JM . First description of Anaerococcus octavius as cause of bacteremia. Anaerobe. 2020; 61: 102130.

[66]

Kim JH, Kim SH, Lim JY, Kim D, Jeong IS, Lee DK, et al. Association between the sinus microbiota with eosinophilic inflammation and prognosis in chronic rhinosinusitis with nasal polyps. Exp Mol Med. 2020; 52(6): 978-987.

[67]

Mahdavinia M, Engen PA, LoSavio PS, Naqib A, Khan RJ, Tobin MC, et al. The nasal microbiome in patients with chronic rhinosinusitis: analyzing the effects of atopy and bacterial functional pathways in 111 patients. J Allergy Clin Immunol. 2018; 142(1): 287-290.e4.

[68]

Wollenberg MS, Claesen J, Escapa IF, Aldridge KL, Fischbach MA, Lemon KP. Propionibacterium-produced coproporphyrin III induces staphylococcus aureus aggregation and biofilm formation. mBio. 2014; 5(4): e01286-14.

[69]

Tran DM, Tran TT, Phung TTB, Bui HT, Nguyen PTT, Vu TT, et al. Nasal-spraying Bacillus spores as an effective symptomatic treatment for children with acute respiratory syncytial virus infection. Sci Rep. 2022; 12(1): 12402.

[70]

Starosila D, Rybalko S, Varbanetz L, Ivanskaya N, Sorokulova I. Anti-influenza activity of a Bacillus subtilis probiotic strain. Antimicrob Agents Chemother. 2017; 61(7): e00539-17.

[71]

Li S, Su B, Wu H, He Q, Zhang T. Integrated analysis of gut and oral microbiome in men who have sex with men with HIV infection. Microbiol Spectr. 2023; 11(6): e0106423.

[72]

Lehtoranta L, Pitkäranta A, Korpela R. Probiotics in respiratory virus infections. Eur J Clin Microbiol Infect Dis. 2014; 33(8): 1289-1302.

[73]

Kates AE, Dalman M, Torner JC, Smith TC. The nasal and oropharyngeal microbiomes of healthy livestock workers. PLoS One. 2019; 14(3): e0212949.

PDF (1180KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/