A review on microbial aerosols in livestock and poultry environments: pollution characteristics, damage mechanisms, and mitigation measures

Highlights

● Animal breeding facilities suffer from significant microbial aerosol contamination.

● Aerosol concentrations are higher in poultry houses than in other animal housing.

● The dominant bacterial and fungal species varied among different animal houses.

● ARGs pose a major challenge to disease prevention efforts in animal settings.

● Microbial aerosols mainly cause damage through cytokine storms and oxidative stress.

Abstract

Livestock and poultry breeding environments suffer from serious microbial aerosol pollution, posing a significant challenge to maintaining healthy animal rearing. This study reviewed the sources, pollution status, hazards, pathogenic mechanisms, and mitigation measures of microbial aerosols in livestock and poultry breeding settings, based on research conducted over the past two decades. Notably, the study analyzed the distribution characteristics of aerosol components in various animal houses, with a focus on identifying the main factors affecting these characteristics and the molecular mechanisms by which they damage the animal immune system. Quantitative analysis revealed varying concentrations of bacterial and fungal aerosols in different animal houses, with poultry houses often exhibiting higher concentrations. The dominant bacterial and fungal species varied across different animal houses, emphasizing the complex composition of microbial aerosols. Furthermore, antibiotic-resistant bacteria and genes, particularly those resistant to tetracycline, are prevalent in these environments, challenging disease prevention and control efforts. Thus, the infection source must be controlled through isolation measures and proper waste management. Proper disinfectant use, responsible antibiotic stewardship, biosecurity measures, and alternative disease prevention strategies should be implemented. Future research should focus on developing monitoring technologies for pathogenic microorganisms, implementing purification technologies, and investigating the immune-damaging mechanisms of microbial aerosols. By addressing these areas, we can further understand microbial aerosols in livestock and poultry environments and develop effective strategies to mitigate their harmful effects. This review contributes to the sustainable development of animal farming to ensure the health and welfare of animals.

Graphical abstract

Keywords

Microbial aerosols / Animal breeding environments / Immune damage / PM_2.5 / ARGs

References

[1] AdhikariAClark S (2017). Disinfection of microbial aerosols. In: Hurst C, ed. Modeling the Transmission and Prevention of Infectious Disease. Advances in Environmental Microbiology. Cham: Springer

[2] AkoijamNJoshi S R (2022). Conservation metagenomics: understanding microbiomes for biodiversity sustenance and conservation. In: Kumar A, Choudhury B, Dayanandan S, Khan M L, eds. Molecular Genetics and Genomics Tools in Biodiversity Conservation. Singapore: Springer

[3] Bai H, He L Y, Wu D L, Gao F Z, Zhang M, Zou H Y, Yao M S, Ying G G. (2022). Spread of airborne antibiotic resistance from animal farms to the environment: dispersal pattern and exposure risk. Environment International, 158: 106927

[4] Bakutis B, Monstviliene E, Januskeviciene G. (2004). Analyses of airborne contamination with bacteria, endotoxins and dust in livestock barns and poultry houses. Acta Veterinaria Brno, 73(2): 283–289

[5] Balasubramanian R, Nainar P, Rajasekar A. (2012). Airborne bacteria, fungi, and endotoxin levels in residential microenvironments: a case study. Aerobiologia, 28(3): 375–390

[6] Banhazi T M, Seedorf J, Laffrique M, Rutley D L. (2008). Identification of the risk factors for high airborne particle concentrations in broiler buildings using statistical modelling. Biosystems Engineering, 101(1): 100–110

[7] Bartlett K H, Kennedy S M, Brauer M, van Netten C, Dill B. (2004). Evaluation and determinants of airborne bacterial concentrations in school classrooms. Journal of Occupational and Environmental Hygiene, 1(10): 639–647

[8] Be N A, Thissen J B, Fofanov V Y, Allen J E, Rojas M, Golovko G, Fofanov Y, Koshinsky H, Jaing C J. (2015). Metagenomic analysis of the airborne environment in urban spaces. Microbial Ecology, 69(2): 346–355

[9] Bekki K, Ito T, Yoshida Y, He C, Arashidani K, He M, Sun G, Zeng Y, Sone H, Kunugita N. . (2016). PM_2.5 collected in China causes inflammatory and oxidative stress responses in macrophages through the multiple pathways. Environmental Toxicology and Pharmacology, 45: 362–369

[10] Borlée F, Yzermans C J, Aalders B, Rooijackers J, Krop E, Maassen C B, Schellevis F, Brunekreef B, Heederik D, Smit L A. (2017). Air pollution from livestock farms is associated with airway obstruction in neighboring residents. American Journal of Respiratory and Critical Care Medicine, 196(9): 1152–1161

[11] Brooks J P, McLaughlin M R, Scheffler B, Miles D M. (2010). Microbial and antibiotic resistant constituents associated with biological aerosols and poultry litter within a commercial poultry house. Science of the Total Environment, 408(20): 4770–4777

[12] Calderón-Garcidueñas L, Vojdani A, Blaurock-Busch E, Busch Y, Friedle A, Franco-Lira M, Sarathi-Mukherjee P, Martínez-Aguirre X, Park S B, Torres-Jardón R. . (2015). Air pollution and children: neural and tight junction antibodies and combustion metals, the role of barrier breakdown and brain immunity in neurodegeneration. Journal of Alzheimer’s Disease, 43(3): 1039–1058

[13] Carey J B, Lacey R E, Mukhtar S. (2004). A review of literature concerning odors, ammonia, and dust from broiler production facilities: 2. flock and house management factors. Journal of Applied Poultry Research, 13(3): 509–513

[14] Chen H, Yan H, Xiu Y, Jiang L, Zhang J, Chen G, Yu X, Zhu H, Zhao X, Li Y. . (2022). Seasonal dynamics in bacterial communities of closed-cage broiler houses. Frontiers in Veterinary Science, 9: 1019005

[15] Chen L, Song Z, Zhou X, Yang G, Yu G. (2024). Pathogenic bacteria and fungi in bioaerosols from specialized hospitals in Shandong Province, East China. Environmental Pollution, 341: 122922

[16] Chien Y C, Chen C J, Lin T H, Chen S H, Chien Y C. (2011). Characteristics of microbial aerosols released from chicken and swine feces. Journal of the Air & Waste Management Association, 61(8): 882–889

[17] Corner L A (2006). The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: How to assess the risk? Veterinary Microbiology, 112(2–4): 303–312

[18] Corzo C A, Culhane M, Dee S, Morrison R B, Torremorell M. (2013). Airborne detection and quantification of swine influenza A virus in air samples collected inside, outside and downwind from swine barns. PLoS One, 8(8): e71444

[19] Cowling B J, Ip D K, Fang V J, Suntarattiwong P, Olsen S J, Levy J, Uyeki T M, Leung G M, Malik Peiris J S, Chotpitayasunondh T. . (2013). Aerosol transmission is an important mode of influenza A virus spread. Nature Communications, 4(1): 1935

[20] Cui H, Zhang C, Liu J, Dong S, Zhao K, Chen L, Chen Z, Sun Y, Guo Z. (2022). The distribution characteristics of aerosol bacteria in different types of pig houses. Animals, 12(12): 1540

[21] Cuong N V, Padungtod P, Thwaites G, Carrique-Mas J J. (2018). Antimicrobial usage in animal production: a review of the literature with a focus on low- and middle-income countries. Antibiotics, 7(3): 75

[22] Cyprowski M, Ławniczek-Wałczyk A, Gołofit-Szymczak M, Frączek K, Kozdrój J, Górny R L. (2019). Bacterial aerosols in a municipal landfill environment. Science of the Total Environment, 660: 288–296

[23] de Rooij M M, Hoek G, Schmitt H, Janse I, Swart A, Maassen C B M, Schalk M, Heederik D J, Wouters I M. (2019). Insights into livestock-related microbial concentrations in air at residential level in a livestock dense area. Environmental Science & Technology, 53(13): 7746–7758

[24] Deng X, Zhang F, Rui W, Long F, Wang L, Feng Z, Chen D, Ding W. (2013). PM_2.5-induced oxidative stress triggers autophagy in human lung epithelial A549 cells. Toxicology In Vitro, 27(6): 1762–1770

[25] Douglas P, Robertson S, Gay R, Hansell A L, Gant T W. (2018). A systematic review of the public health risks of bioaerosols from intensive farming. International Journal of Hygiene and Environmental Health, 221(2): 134–173

[26] Douwes J, Thorne P, Pearce N, Heederik D. (2003). Bioaerosol health effects and exposure assessment: progress and prospects. Annals of Occupational Hygiene, 47: 187–200

[27] Duan H, Chai T, Liu J, Zhang X, Qi C, Gao J, Wang Y, Cai Y, Miao Z, Yao M. . (2009). Source identification of airborne Escherichia coli of swine house surroundings using ERIC-PCR and REP-PCR. Environmental Research, 109(5): 511–517

[28] Edgar R C. (2018). Accuracy of taxonomy prediction for 16S rRNA and fungal ITS sequences. PeerJ, 6: e4652

[29] Elmberg J, Berg C, Lerner H, Waldenström J, Hessel R. (2017). Potential disease transmission from wild geese and swans to livestock, poultry and humans: a review of the scientific literature from a one health perspective. Infection Ecology & Epidemiology, 7(1): 1300450

[30] Fiegel J, Clarke R, Edwards D A. (2006). Airborne infectious disease and the suppression of pulmonary bioaerosols. Drug Discovery Today, 11(1–2): 51–57

[31] Fu X, Ou Z, Zhang M, Meng Y, Li Y, Wen J, Hu Q, Zhang X, Norbäck D, Deng Y. . (2021). Indoor bacterial, fungal and viral species and functional genes in urban and rural schools in Shanxi Province, China–association with asthma, rhinitis and rhinoconjunctivitis in high school students. Microbiome, 9(1): 138

[32] Grydaki N, Colbeck I, Mendes L, Eleftheriadis K, Whitby C. (2021). Bioaerosols in the Athens Metro: metagenetic insights into the PM₁₀ microbiome in a naturally ventilated subway station. Environment International, 146: 106186

[33] Guo Y, Xiao X, Zhao Y, Liu J, Zhou J, Sun B, Liang Y. (2022). Antibiotic resistance genes in manure-amended paddy soils across eastern China: occurrence and influencing factors. Frontiers of Environmental Science & Engineering, 16(7): 91

[34] Han Y, Yang T, Chen T, Li L, Liu J. (2019). Characteristics of submicron aerosols produced during aeration in wastewater treatment. Science of the Total Environment, 696: 134019

[35] Hao H, Li C, Qiu Y, Wang F, Ai W, Gao J, Wei L, Li X, Sun L, Wu J. . (2014). Generation, transmission and infectiosity of chicken MDV aerosols under experimental conditions. Veterinary Microbiology, 172(3–4): 400–406

[36] He M, Ichinose T, Yoshida Y, Arashidani K, Yoshida S, Takano H, Sun G, Shibamoto T. (2017). Urban PM_2.5 exacerbates allergic inflammation in the murine lung via a TLR2/TLR4/MyD88-signaling pathway. Scientific Reports, 7(1): 11027

[37] HeYYuanQ MathieuJStadler LSenehiNSunRAlvarezP J J (2020). Antibiotic resistance genes from livestock waste: occurrence, dissemination, and treatment. npj Clean Water, 3: 4

[38] Hong P Y, Li X, Yang X, Shinkai T, Zhang Y, Wang X, Mackie R I. (2012). Monitoring airborne biotic contaminants in the indoor environment of pig and poultry confinement buildings. Environmental Microbiology, 14(6): 1420–1431

[39] Hu Y, Cheng H, Tao S. (2017). Environmental and human health challenges of industrial livestock and poultry farming in China and their mitigation. Environment International, 107: 111–130

[40] Islam M A, Ikeguchi A, Naide T. (2020). Influence of temperature and humidity on the dynamics of aerosol numbers and airborne bacteria in a dairy calf house. Biosystems Engineering, 194: 213–226

[41] Jahne M A, Rogers S W, Holsen T M, Grimberg S J, Ramler I P. (2015). Emission and dispersion of bioaerosols from dairy manure application sites: human health risk assessment. Environmental Science & Technology, 49(16): 9842–9849

[42] Ji L, Zhang Q, Fu X, Zheng L, Dong J, Wang J, Guo S. (2019). Feedback of airborne bacterial consortia to haze pollution with different PM_2.5 levels in typical mountainous terrain of Jinan, China. Science of the Total Environment, 695: 133912

[43] Jiang L, Li M, Tang J, Zhao X, Zhang J, Zhu H, Yu X, Li Y, Feng T, Zhang X. (2018a). Effect of different disinfectants on bacterial aerosol diversity in poultry houses. Frontiers in Microbiology, 9: 2113

[44] Jiang L, Zhang J, Tang J, Li M, Zhao X, Zhu H, Yu X, Li Y, Feng T, Zhang X. (2018b). Analyses of aerosol concentrations and bacterial community structures for closed cage broiler houses at different broiler growth stages in winter. Journal of Food Protection, 81(9): 1557–1564

[45] Just N, Kirychuk S, Gilbert Y, Létourneau V, Veillette M, Singh B, Duchaine C. (2011). Bacterial diversity characterization of bioaerosols from cage-housed and floor-housed poultry operations. Environmental Research, 111(4): 492–498

[46] Just N A, Létourneau V, Kirychuk S P, Singh B, Duchaine C. (2012). Potentially pathogenic bacteria and antimicrobial resistance in bioaerosols from cage-housed and floor-housed poultry operations. Annals of Occupational Hygiene, 56: 440–449

[47] Kim K Y, Ko H J. (2019). Indoor distribution characteristics of airborne bacteria in pig buildings as influenced by season and housing type. Asian-Australasian Journal of Animal Sciences, 32(5): 742–747

[48] Kristiansen A, Saunders A M, Hansen A A, Nielsen P H, Nielsen J L. (2012). Community structure of bacteria and fungi in aerosols of a pig confinement building. FEMS Microbiology Ecology, 80(2): 390–401

[49] Kumari P, Choi H L. (2014). Seasonal variability in airborne biotic contaminants in swine confinement buildings. PLoS One, 9(11): e112897

[50] Lawniczek-Walczyk A, Górny R L, Golofit-Szymczak M, Niesler A, Wlazlo A. (2013). Occupational exposure to airborne microorganisms, endotoxins and β-glucans in poultry houses at different stages of the production cycle. Annals of Agricultural and Environmental Medicine, 20: 259–268

[51] Lee G, Yoo K. (2022). A review of the emergence of antibiotic resistance in bioaerosols and its monitoring methods. Reviews in Environmental Science and Biotechnology, 21(3): 799–827

[52] Li M, Wei X, Li Y, Feng T, Jiang L, Zhu H, Yu X, Tang J, Chen G, Zhang J. . (2020). PM_2.5 in poultry houses synergizes with pseudomonas aeruginosa to aggravate lung inflammation in mice through the NF-κB pathway. Journal of Veterinary Science, 21(3): e46

[53] Li T, Hu R, Chen Z, Li Q, Huang S, Zhu Z, Zhou L F. (2018). Fine particulate matter (PM_2.5): the culprit for chronic lung diseases in China. Chronic Diseases and Translational Medicine, 4(3): 176–186

[54] Liu H, Zhang X, Zhang H, Yao X, Zhou M, Wang J, He Z, Zhang H, Lou L, Mao W. . (2018). Effect of air pollution on the total bacteria and pathogenic bacteria in different sizes of particulate matter. Environmental Pollution, 233: 483–493

[55] Liu Y, Zhang X, Qi W, Yang Y, Liu Z, An T, Wu X, Chen J. (2021). Prevention and control strategies of african swine fever and progress on pig farm repopulation in China. Viruses, 13(12): 2552

[56] Lloyd L C, Etheridge J R. (1983). Contagious bovine pleuropneumonia produced by aerosols artificially generated from cultures of Mycoplasma mycoides subsp. mycoides. British Veterinary Journal, 139(4): 330–337

[57] Loor J J, Elolimy A A, McCann J C. (2016). Dietary impacts on rumen microbiota in beef and dairy production. Animal Frontiers, 6(3): 22–29

[58] Lou C, Bai Y, Chai T, Yu H, Lin T, Hu G, Guan Y, Wu B. (2022). Research progress on distribution and exposure risk of microbial aerosols in animal houses. Frontiers in Veterinary Science, 9: 1015238

[59] Madsen A M. (2006). Airborne endotoxin in different background environments and seasons. Annals of agricultural and environmental medicine. Annals of Agricultural and Environmental Medicine, 13: 81–86

[60] Manor O, Borenstein E. (2017). Systematic characterization and analysis of the taxonomic drivers of functional shifts in the human microbiome. Cell Host & Microbe, 21(2): 254–267

[61] Matković K, Vucemilo M, Stokovic I, Simic R, Marusic D, Vinkovic B, Matkovic S. (2013). Concentrations of airborne bacteria and fungi in a livestock building with caged laying hens. Veterinary Archives, 83: 413

[62] Mbareche H, Veillette M, Bilodeau G J, Duchaine C. (2019). Fungal aerosols at dairy farms using molecular and culture techniques. Science of the Total Environment, 653: 253–263

[63] McEachran A D, Blackwell B R, Hanson J D, Wooten K J, Mayer G D, Cox S B, Smith P N. (2015). Antibiotics, bacteria, and antibiotic resistance genes: aerial transport from cattle feed yards via particulate matter. Environmental Health Perspectives, 123(4): 337–343

[64] Mehdi Y, Létourneau-Montminy M P, Gaucher M L, Chorfi Y, Suresh G, Rouissi T, Brar S K, Côté C, Ramirez A A, Godbout S. (2018). Use of antibiotics in broiler production: global impacts and alternatives. Animal Nutrition, 4(2): 170–178

[65] Meng K, Wu B, Gao J, Cai Y, Yao M, Wei L, Chai T. (2016). Immunity-related protein expression and pathological lung damage in mice poststimulation with ambient particulate matter from live bird markets. Frontiers in Immunology, 7: 252

[66] Miao Z, Chai T, Qi C, Cai Y, Liu J, Yuan W, Yao M. (2010). Composition and variability of airborne fungi in an enclosed rabbit house in China. Aerobiologia, 26(2): 135–140

[67] Mullany P. (2014). Functional metagenomics for the investigation of antibiotic resistance. Virulence, 5(3): 443–447

[68] Nair A T. (2021). Bioaerosols in the landfill environment: an overview of microbial diversity and potential health hazards. Aerobiologia, 37(2): 185–203

[69] Pacheco J M, Arzt J, Rodriguez L L. (2010). Early events in the pathogenesis of foot-and-mouth disease in cattle after controlled aerosol exposure. Veterinary Journal, 183(1): 46–53

[70] Pak H, King M. (2022). Impact of seasonal variations on microbiome diversity and antibiotic resistance in aerosolized bacteria in a dairy facility. Journal of Aerosol Science, 166: 106046

[71] Pavan R, Manjunath K. (2014). Qualitative analysis of indoor and outdoor airborne fungi in cowshed. Journal of Mycology, 2014: 1–8

[72] Pei Y, Jiang R, Zou Y, Wang Y, Zhang S, Wang G, Zhao J, Song W. (2016). Effects of fine particulate matter (PM_2.5) on systemic oxidative stress and cardiac function in ApoE^−/− mice. International Journal of Environmental Research and Public Health, 13(5): 484

[73] PieckováE (2017). Indoor microbial aerosol and its health effects: microbial exposure in public buildings–viruses, bacteria, and fungi. In: Viegas C, Viegas S, Gomes A, Täubel M, Sabino R, eds. Exposure to Microbiological Agents in Indoor and Occupational Environments. Cham: Springer

[74] Pileri E, Mateu E. (2016). Review on the transmission porcine reproductive and respiratory syndrome virus between pigs and farms and impact on vaccination. Veterinary Research, 47(1): 108

[75] Pirie R S, Collie D D, Dixon P M, McGorum B C. (2003). Inhaled endotoxin and organic dust particulates have synergistic proinflammatory effects in equine heaves (organic dust-induced asthma). Clinical and Experimental Allergy, 33(5): 676–683

[76] Radon K, Danuser B, Iversen M, Monso E, Weber C, Hartung J, Donham K, Palmgren U, Nowak D. (2002). Air contaminants in different European farming environments. Annals of Agricultural and Environmental Medicine, 9: 41–48

[77] Ruzal M, Shinder D, Malka I, Yahav S. (2011). Ventilation plays an important role in hens’ egg production at high ambient temperature. Poultry Science, 90(4): 856–862

[78] Rysz M, Alvarez P J. (2004). Amplification and attenuation of tetracycline resistance in soil bacteria: aquifer column experiments. Water Research, 38(17): 3705–3712

[79] Samake A, Uzu G, Martins J M, Calas A, Vince E, Parat S, Jaffrezo J L. (2017). The unexpected role of bioaerosols in the oxidative potential of PM. Scientific Reports, 7(1): 10978

[80] Sancheza H M, Echeverria C, Thulsiraj V, Zimmer-Faust A, Flores A, Laitz M, Healy G, Mahendra S, Paulson S E, Zhu Y. . (2016). Antibiotic resistance in airborne bacteria near conventional and organic beef cattle farms in California, USA. Water, Air, and Soil Pollution, 227: 280

[81] Sapkota A R, Ojo K K, Roberts M C, Schwab K J. (2006). Antibiotic resistance genes in multidrug-resistant Enterococcus spp. and Streptococcus spp. recovered from the indoor air of a large-scale swine-feeding operation. Letters in Applied Microbiology, 43(5): 534–540

[82] Schmitt H, Stoob K, Hamscher G, Smit E, Seinen W. (2006). Tetracyclines and tetracycline resistance in agricultural soils: microcosm and field studies. Microbial Ecology, 51(3): 267–276

[83] Shang M, Kong Y, Yang Z, Cheng R, Zheng X, Liu Y, Chen T. (2023). Removal of virus aerosols by the combination of filtration and UV-C irradiation. Frontiers of Environmental Science & Engineering, 17(3): 27

[84] Sharma J, Parsai K, Raghuwanshi P, Ali S A, Tiwari V, Bhargava A, Mishra P K. (2021). Emerging role of mitochondria in airborne particulate matter-induced immunotoxicity. Environmental Pollution, 270: 116242

[85] Sigurdarson S T, Kline J N. (2006). School proximity to concentrated animal feeding operations and prevalence of asthma in students. Chest, 129(6): 1486–1491

[86] Song L, Wang C, Jiang G, Ma J, Li Y, Chen H, Guo J. (2021). Bioaerosol is an important transmission route of antibiotic resistance genes in pig farms. Environment International, 154: 106559

[87] Song Z, Cai Y, Liu G, Yu G. (2023). Fungal aerosols in rabbit breeding environment: metagenetic insight into PM_2.5 based on third-generation sequencing technology. Environmental Research, 224: 115480

[88] SunD Q (2021). Characteristics, hazards and control measures of microbial aerosols in poultry houses. Livestock and Poultry Industry, 32: 33–36 (in Chinese)

[89] Tang Q, Huang K, Liu J, Jin X, Li C. (2021). Distribution characteristics of bioaerosols inside pig houses and the respiratory tract of pigs. Ecotoxicology and Environmental Safety, 212: 112006

[90] Thomas R J. (2013). Particle size and pathogenicity in the respiratory tract. Virulence, 4(8): 847–858

[91] Tisoncik J R, Korth M J, Simmons C P, Farrar J, Martin T R, Katze M G. (2012). Into the eye of the cytokine storm. Microbiology and Molecular Biology Reviews, 76(1): 16–32

[92] Traverse M, Aceto H. (2015). Environmental cleaning and disinfection. Veterinary Clinics of North America. Small Animal Practice, 45(2): 299–330

[93] Uyaguari-Diaz M I, Chan M, Chaban B L, Croxen M A, Finke J F, Hill J E, Peabody M A, Van Rossum T, Suttle C A, Brinkman F S. (2016). A comprehensive method for amplicon-based and metagenomic characterization of viruses, bacteria, and eukaryotes in freshwater samples. Microbiome, 4(1): 20

[94] Vidic J, Manzano M, Chang C M, Jaffrezic-Renault N. (2017). Advanced biosensors for detection of pathogens related to livestock and poultry. Veterinary Research, 48(1): 11

[95] Vučemilo M, Matković K, Vinković B, Jakšić S, Granić K, Mas N. (2007). The effect of animal age on air pollutant concentration in a broiler house. Czech Journal of Animal Science, 52(6): 170–174

[96] Wang H, Xu J, Liu X, Sheng L, Zhang D, Li L, Wang A. (2018). Study on the pollution status and control measures for the livestock and poultry breeding industry in Northeastern China. Environmental Science and Pollution Research International, 25(5): 4435–4445

[97] Wang M, Peng S, Liu D, Long D, Liu Z, Pu S. (2023a). Characteristics and traceability analysis of microbial assemblage in fine particulate matter from a pig house. Animals, 13(6): 1058

[98] Wang K, Shen D, Dai P, Li C. (2023b). Particulate matter in poultry house on poultry respiratory disease: a systematic review. Poultry Science, 102(4): 102556

[99] Wang W, Dang G, Khan I, Ye X, Liu L, Zhong R, Chen L, Ma T, Zhang H. (2022). Bacterial community characteristics shaped by artificial environmental PM_2.5 control in intensive broiler houses. International Journal of Environmental Research and Public Health, 20(1): 723

[100] Wei K, Zheng Y, Li J, Shen F, Zou Z, Fan H, Li X, Wu C, Yao M. (2015). Microbial aerosol characteristics in highly polluted and near-pristine environments featuring different climatic conditions. Science Bulletin, 60(16): 1439–1447

[101] Weichenthal S A, Godri-Pollitt K, Villeneuve P J. (2013). PM_2.5, oxidant defence and cardiorespiratory health. Reviews on Environmental Health, 12: 40

[102] Weinmaier T, Probst A J, La Duc M T, Ciobanu D, Cheng J F, Ivanova N, Rattei T, Vaishampayan P. (2015). A viability-linked metagenomic analysis of cleanroom environments: eukarya, prokaryotes, and viruses. Microbiome, 3(1): 62

[103] Wing S, Wolf S. (2000). Intensive livestock operations, health, and quality of life among eastern North Carolina residents. Environmental Health Perspectives, 108(3): 233–238

[104] Wu B, Duan H, Qi Q, Cai Y, Zhong Z, Chai T. (2018). Identifying virulence factor genes in E. coli in animal houses and their transmission to outside environments. Journal of Aerosol Science, 117: 189–199

[105] Wu B, Lou C, Chen Z, Chai T, Yu H. (2023). Combined 16S and internal transcribed spacer analysis revealed the effect of time on microbial community in animal house. Poultry Science, 102(11): 103039

[106] Wu B, Meng K, Wei L, Cai Y, Chai T. (2017). Seasonal fluctuations of microbial aerosol in live poultry markets and the detection of endotoxin. Frontiers in Microbiology, 8: 551

[107] Wu B, Qin L, Wang M, Zhou T, Dong Y, Chai T. (2019a). The composition of microbial aerosols, PM_2.5, and PM₁₀ in a duck house in Shandong Province, China. Poultry Science, 98(11): 5913–5924

[108] Wu B, Qi Q, Zhang X, Cai Y, Yu G, Lv J, Gao L, Wei L, Chai T. (2019b). Dissemination of Escherichia coli carrying plasmid-mediated quinolone resistance (PMQR) genes from swine farms to surroundings. Science of the Total Environment, 665: 33–40

[109] Wu S, Tang M, Wang Y, Ma Z, Ma Y. (2022). Analysis of the spatial distribution characteristics of livestock and poultry farming pollution and assessment of the environmental pollution load in Anhui Province. Sustainability, 14(7): 4165

[110] Xin H, Gao M, Wang X, Qiu T, Guo Y, Zhang L. (2022). Animal farms are hot spots for airborne antimicrobial resistance. Science of the Total Environment, 851: 158050

[111] Xiong W, Wang Y, Sun Y, Ma L, Zeng Q, Jiang X, Li A, Zeng Z, Zhang T. (2018). Antibiotic-mediated changes in the fecal microbiome of broiler chickens define the incidence of antibiotic resistance genes. Microbiome, 6(1): 34

[112] Xu C, Kong L, Liao Y, Tian Y, Wu Q, Liu H, Wang X. (2022). Mini-review: antibiotic-resistant Escherichia coli from farm animal-associated sources. Antibiotics, 11(11): 1535

[113] Yan H, Chen H, Jiang L, Zhang J, Chen G, Yu X, Zhu H, Zhao X, Li Y, Tang W. . (2023). Spatial distribution of airborne bacterial communities in caged poultry houses. Journal of the Air & Waste Management Association, 73(5): 417–427

[114] Yang F, Gao Y, Zhao H, Li J, Cheng X, Meng L, Dong P, Yang H, Chen S, Zhu J. (2021). Revealing the distribution characteristics of antibiotic resistance genes and bacterial communities in animal-aerosol-human in a chicken farm: from one-health perspective. Ecotoxicology and Environmental Safety, 224: 112687

[115] Yang J, Huo T, Zhang X, Ma J, Wang Y, Dong F, Deng J. (2018a). Oxidative stress and cell cycle arrest induced by short-term exposure to dust fall PM_2.5 in A549 cells. Environmental Science and Pollution Research International, 25(23): 22408–22419

[116] Yang W, Guo M, Liu G, Yu G, Wang P, Wang H, Chai T. (2018b). Detection and analysis of fine particulate matter and microbial aerosol in chicken houses in Shandong Province, China. Poultry. Poultry Science, 97(3): 995–1005

[117] Yang Y, Zhang R, Lou Z. (2022). Bioaerosol emissions variations in large-scale landfill region and their health risk impacts. Frontiers of Environmental Science & Engineering, 16(12): 158

[118] Yu G L, Wei L M, Liu Y Y, Liu J Y, Wang Y, Gao J, Chai T J, Cai Y M. (2016a). Influence of indoor microbial aerosol on the welfare of meat ducks. British Poultry Science, 57(1): 12–22

[119] Yu G, Wang Y, Wang S, Duan C, Wei L, Gao J, Chai T, Cai Y. (2016b). Effects of microbial aerosol in poultry house on meat ducks’ immune function. Frontiers in Microbiology, 7: 1245

[120] Yu G L, Chai T J, Cai Y M. (2016c). Effect of solid formaldehyde fumigation on the microbial aerosol livestock and poultry house. Chinese Journal of Veterinary Science, 36: 1718–1721

[121] ZhangBGuo K KChenL GCuiHZhangC BaiXDongS S (2020). Research progress on microbial aerosols in livestock houses. Heilongjiang Animal Science and Veterinary Medicine, 7: 38-41 (in Chinese)

[122] Zhang J, Li Y, Xu E, Jiang L, Tang J, Li M, Zhao X, Chen G, Zhu H, Yu X. . (2019a). Bacterial communities in PM_2.5 and PM₁₀ in broiler houses at different broiler growth stages in spring. Polish Journal of Veterinary Sciences, 22: 495–504

[123] Zhang J, Wei X, Jiang L, Li Y, Li M, Zhu H, Yu X, Tang J, Chen G, Zhang X. (2019b). Bacterial community diversity in particulate matter (PM_2.5 and PM₁₀) within broiler houses in different broiler growth stages under intensive rearing conditions in summer. Journal of Applied Poultry Research, 28(2): 479–489

[124] Zhang T, Zhang X X, Ye L. (2011). Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PLoS One, 6(10): e26041

[125] Zhao C, Pu W, Niu M, Wazir J, Song S, Wei L, Li L, Su Z, Wang H. (2022). Respiratory exposure to PM_2.5 soluble extract induced chronic lung injury by disturbing the phagocytosis function of macrophage. Environmental Science and Pollution Research International, 29(10): 13983–13997

[126] Zhao J, Gao Z, Tian Z, Xie Y, Xin F, Jiang R, Kan H, Song W. (2013). The biological effects of individual-level PM_2.5 exposure on systemic immunity and inflammatory response in traffic policemen. Occupational and Environmental Medicine, 70(6): 426–431

[127] Zhong S, Zhang L, Jiang X, Gao P. (2019). Comparison of chemical composition and airborne bacterial community structure in PM_2.5 during haze and non-haze days in the winter in Guilin, China. Science of the Total Environment, 655: 202–210

[128] Zhu Y G, Johnson T A, Su J Q, Qiao M, Guo G X, Stedtfeld R D, Hashsham S A, Tiedje J M. (2013). Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proceedings of the National Academy of Sciences of the United States of America, 110(9): 3435–3440

[129] Zucker B A, Trojan S, Müller W. (2000). Airborne gram-negative bacterial flora in animal houses. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health, 47(1): 37–46

CRediT Authorship Contribution Statement

Guanliu Yu: project administration, conceptualization and writing, review and editing. Xilong Wang and Zhicheng Song: original draft preparation and visualization. Yumei Cai: project administration and supervision. All the authors contributed to the review article and approved the submitted version.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 32300087) and the Poultry Innovation Team Environmental Control Post Expert (China) (SDAIT-11-09).

Conflict Interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data Availability

No data was used for the research described in the article.

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