Abstract
In several regions worldwide, the presence of livestock in close proximity to residential areas raises questions about public health implications. The rapid expansion of large‐scale livestock farms, increasingly interwoven with urbanized areas, and its potential impact on neighboring residents' health has hardly been accompanied by any research. The current situation in densely populated livestock farming areas could be regarded as a “natural experiment.” Most scientific and public health initiatives have focused on emerging zoonoses and antimicrobial resistance as potential health threats. In this commentary, we emphasize the importance of respiratory health effects of noninfectious air pollutant emissions from livestock farms.
Keywords: air pollution, agriculture, public health
Key Points
The rapid expansion of large‐scale livestock farms near residential areas raises questions about public health implications
A series of recent studies on air pollutant emissions from agriculture emphasize respiratory health risks among neighboring residents
There is a clear need to firmly embed public health perspectives in the decision‐making process in environmental and agricultural planning
1. Introduction
The Netherlands is one of the world's most densely populated countries with more than 500 inhabitants per km2 land area, but it is also characterized by a remarkably high concentration of intensive livestock farms (Robinson et al., 2011). The intensification and expansion of livestock farming is a relatively recent phenomenon. Around the 1950s, Dutch livestock farming was still characterized by small‐scale mixed farming, especially in the sandy regions in the east and the south. In 1950 there were almost 271,000 pig keepers, who kept on average around seven pigs, mostly on mixed farms (Bieleman, 2010). Since the end of the 1950s, a rapidly increasing flow of imported feedstuffs through the port of Rotterdam, together with a process of scaling up and specialization led to highly intensified livestock farms (Bieleman, 2010). Because of the import of soy and other raw materials for animal feed, the numbers of intensively raised animals are disproportionately high relative to land area availability. Currently, the Netherlands is home to 12.5 million pigs that are kept on just over 3,000 specialized pig farms. Furthermore, more than 100 million broilers and laying hens, 4.2 million cows and veal calves, 1 million minks, 0.8 million sheep, and 0.5 million goats are kept (Statistics Netherlands, 2017).
The presence of such a large number of animals in close proximity to residential areas raises questions about public health implications. The situation in the Netherlands, and also in several other regions worldwide, in particular, in the Western world and Asia (Robinson et al., 2011), can be seen as a “natural experiment.” The rapid expansion of large‐scale livestock farms, increasingly interwoven with urbanized areas, and its potential impact on neighboring residents' health have hardly been accompanied by any research. Although various occupational health risks of livestock farming are well described (Schenker et al., 1998), they cannot be directly generalized to the surrounding population's situation. In the first place, levels of exposure to potentially harmful agents such as gases (ammonia, H2S) and organic dust are much higher in farmers than in neighboring residents. On the other hand, farmers are a “healthy worker” population, whereas young children, elderly, and people with chronic illnesses are probably more vulnerable to the effects of environmental pollution. Moreover, because of the industrialization of agriculture and animal production, a growing number of residents in livestock‐dense areas do not have a farming background. This population may be more susceptible to farm‐related illnesses, especially to livestock‐related zoonotic infections, as they have no or limited immunity to specific zoonotic pathogens.
So which agricultural pollutants are of potential relevance for general public health? Water and soil quality may be affected, depending on local conditions, manure treatment methods, and environmental regulations. A striking example was recently brought to the public's attention by a series of Pulitzer Prize winning editorials in a small newspaper in Iowa, which focused on water pollution by agricultural companies (Cullen, 2017). According to one of the editorials: “Anyone with eyes and a nose knows in his gut that Iowa has the dirtiest surface water in America.” The editorials covered a water utility lawsuit over nitrate pollution into rivers used for drinking water supplies and revealed how powerful agricultural corporations secretly financed the defense. In this commentary, we will, however, mainly focus on air pollutants.
2. Agriculture: A Key Contributor to Air Pollution
Air quality is diminished in livestock farming areas, due to emissions of both coarse and fine particles, (odorous) gases, and endotoxin, the major component of the outer membrane of Gram‐negative bacteria. Potentially pathogenic viruses and bacteria, and antimicrobial‐resistant (AMR) bacteria can also be found in airborne particulate matter (PM) surrounding livestock farms (de Rooij et al., 2016; McEachran et al., 2015; Ssematimba et al., 2012). Although the main sources of PM emitted from livestock houses are of organic nature, for example, manure, bedding material, straw, animal feed, feathers, skin flakes, and hair (Winkel, 2016), recent studies have emphasized the large contribution of livestock farming to anthropogenic fine PM (PM2.5) pollution, which constitutes mainly of secondary inorganic aerosols, including ammonium sulfate and ammonium nitrate (Bauer et al., 2016; Brunekreef et al., 2015; Lelieveld et al., 2015; Vieno et al., 2016). Inorganic ammonium compounds are formed by gaseous ammonia, which is mainly emitted from livestock production, and combustion‐based gases. Long‐range transport substantially contributes to ambient concentrations of PM2.5, and therefore, agricultural ammonia emissions have been identified as major contributors to PM2.5 in urban areas and other nonagricultural areas as well. Vieno et al. argued that while the contribution of agricultural ammonia emissions to particular PM air pollution events is well established by scientific analyses, translation into communicating outside the atmospheric science arena needs improvement. The lack of public awareness of agricultural emissions as a key contributor to air pollution may eventually result in a weaker policy mandate for any emissions reduction targets for ammonia (Vieno et al., 2016).
3. Health Effects From Livestock‐Related Air Pollution
Potential health effects from farm emissions are equally diverse and include zoonotic infections, infections with AMR bacteria, and respiratory disorders. Within the One Health concept, the multidisciplinary and collaborative approach to address potential or existing risks that originate at the animal‐human‐environment interface (Coker et al., 2011; One Health Initiative, 2017), most research initiatives have focused on zoonotic infections and emerging antimicrobial resistance as a potential threat to both human and animal health. However, a series of recent studies on air pollutant emissions from agriculture emphasize the environmental health risks posed by noninfectious farm emissions. Lelieveld et al. showed that agriculture has a remarkably large impact on PM air pollution‐related mortality, and is even the leading source category in Europe, Russia, Turkey, Korea, Japan, and the Eastern USA (Lelieveld et al., 2015). Large‐scale air pollution by secondary inorganic aerosols can affect a large proportion of the population, also outside livestock farming areas. People living at closer proximity to farms are also exposed to other agents that may affect the airways, such as endotoxin, larger particles, and ammonia. Living near a large number of livestock farms is associated with an increased risk of airway obstruction (Borlée et al., 2017; Radon et al., 2007). Furthermore, higher ammonia concentrations in the air are associated with acute deficits in lung function in adults and asthmatic children living in livestock‐dense areas (Borlée et al., 2017; Loftus et al., 2015). Ammonia is considered to be a marker for other livestock‐related air pollutants, as the levels in residential areas are probably too low to cause respiratory effects. Although the average effect on lung function is modest, peak exposures may cause airway symptoms in vulnerable subjects. Patients with chronic obstructive pulmonary disease (COPD) living near livestock farms report more symptoms and are more often diagnosed with an exacerbation than patients living further away from farms (Borlée et al., 2015; van Dijk et al., 2016). The incidence of pneumonia is also found to be increased in livestock‐dense areas, especially near goat and poultry farms (Beninca et al., 2017; Freidl et al., 2017; Smit et al., 2017; van Dijk et al., 2017). Since there is no evidence of zoonotic pathogens playing a role, except during outbreak situations (Huijskens et al., 2016), we hypothesized that endotoxin and other farm‐related air pollutants may predispose to respiratory infections through chronic airway inflammation and subsequent host immune responses. In hospitalized pneumonia patients living close to poultry farms, the abundance of Streptococcus pneumoniae—not a zoonotic pathogen—in the upper airway microbiome was increased, suggesting a role for noninfectious air pollutant emissions (Smit et al., 2017), a hypothesis supported by a growing number of experimental studies (Poroyko et al., 2015; Rylance et al., 2015).
4. Risk of Zoonotic Infections
The importance of zoonotic infections is increasingly recognized, not in the least because the implications of an outbreak can be far reaching. Between 2007 and 2010, an unprecedented outbreak of Q fever, a zoonosis caused by Coxiella burnetii, occurred in the Netherlands with more than 4,000 human cases (Dijkstra et al., 2012), showing that the risk of resurgence or emergence and spread of zoonotic infections among the general population is more than theoretical. Dairy goat farms with C. burnetii‐induced abortions were implicated as the major source of infection in the neighboring human population. C. burnetii is transmitted primarily through contaminated air, and people living several kilometers from an infected farm were still at increased risk of Q fever. In 2012, the epidemic was declared ended, most likely as a consequence of implemented control measures, including culling of pregnant animals and compulsory vaccination, in combination with a rise in seroprevalence in the human population (Van den Brom et al., 2015). Although other zoonotic infections, such as hepatitis E, psittacosis, and avian influenza are suspected of environmental transmission via infected farms to neighboring residents, there is limited or no scientific evidence of current health risks for the surrounding, nonfarming population (Hogerwerf et al., 2017; van Gageldonk‐Lafeber et al., 2017). For example, in a recent study in more than 2,400 individuals living in a livestock‐dense area in the Netherlands, the presence of hepatitis E virus (HEV) antibodies was strongly age related, but not associated with residential proximity to pig farms, suggesting that airborne spread of HEV is unlikely (van Gageldonk‐Lafeber et al., 2017). The increasing incidence of HEV in Europe is more likely a result of HEV‐contaminated pork consumption (Slot et al., 2017).
5. Antimicrobial Resistance
Infection with AMR bacteria is another potential health risk. Antimicrobial drugs are frequently used in the livestock industry to treat or prevent bacterial infections. Antibiotics can also be administered at subtherapeutic doses to promote growth, a practice that was banned in the EU in 2006, but still common in the United States. In the past decade, a specific clone of methicillin‐resistant Staphylococcus aureus (MRSA), referred to as livestock‐associated MRSA (LA‐MRSA) has emerged in livestock and people in direct contact with livestock, in particular, pigs and veal calves (Graveland et al., 2010; Voss et al., 2005). Although airborne transmission is a likely route of exposure in farmers (Bos et al., 2016), it is unclear whether LA‐MRSA is transmitted to nonfarming residents through the environment, for example, by air. In a large population survey, only 10 out of 2,492 Dutch adults carried LA‐MRSA, but carriers lived closer to a livestock farm than noncarriers, a difference that remained statistically significant after adjustment for farm animal contact (Zomer, Wielders, et al., 2017). In the United States, living near high‐density livestock production was associated with infection with other MRSA strains than the European LA‐MRSA (Casey et al., 2014). Other examples of AMR bacteria occurring in livestock are Enterobacteriaceae that produce extended‐spectrum β‐lactamases (ESBLs) and/or plasmid‐mediated AmpC (pAmpC), and Clostridium difficile, an enteric pathogen in humans and piglets. While there is ample evidence that transmission can take place via direct contact with animals (Dierikx et al., 2013; Keessen et al., 2013), there is currently no epidemiologic evidence that people living near livestock farms are at increased risk of infection with AMR bacteria compared with people living further away. In Dutch population‐based studies, residential distance to farms was not a risk factor for carriage of ESBLs or pAmpC producing Enterobacteriaceae (Huijbers et al., 2013; Wielders et al., 2017) or Clostridium difficile (Zomer, van Duijkeren, et al., 2017).
6. Perspective
A pertinent question is how to protect neighboring residents from potentially harmful farm emissions while maintaining (family) farm viability and food safety, ensuring healthy working conditions, and optimizing animal welfare. The strategy required will depend on the specific exposure considered. The risk of transmission of AMR bacteria from livestock production industries has been considerably reduced by a more than 60% reduction in use of antimicrobials in the Netherlands over the last 5 years. This reduction in antimicrobial use has been accompanied by a reduction in antimicrobial resistance in all livestock production sectors (Dorado‐Garcia et al., 2016). For other risks, such as zoonoses, animal disease management, including improving biosecurity, vaccination, and last but not least surveillance are the most effective strategies. For gas and dust emissions, emission reduction by the use of alternative housing systems is required. Implementing “safe distances” between large‐scale farms and residential areas is hardly an option in densely‐populated regions. Furthermore, because of the dispersion characteristics of the different emissions and lack of knowledge on exposure‐response relations, there is no scientific basis for a distance‐based policy.
However, decision making may also lead to–sometimes unforeseen–trade‐offs between these objectives. For example, the transition in the laying hen sector from cage housing to alternative housing systems with littered floors has substantially increased the contribution of the livestock sector to total PM emissions (Winkel, 2016). Due to public health concerns highlighted by recent research discussed in our commentary, the Dutch government now plans to reduce the emissions from poultry houses by 50% over the next 10 years (van Dam & Dijksma, 2017), creating an urgent need for emission‐reducing technologies. The present global interest in reduction of antimicrobials in livestock production is of major importance, but lacks broader production chain‐based approaches that take other risks and changes in livestock production in consideration and may come into conflict with other public or animal and environmental health‐related issues when not considered adequately in a broader context.
There is a clear need to firmly embed public health perspectives in the decision‐making process in environmental planning and agricultural development. Research on exposure and health risks of animal farming should extend beyond infectious disease monitoring, and more awareness of agriculture as a contributor to large‐scale air pollution should be raised. Our decision making requires more scientific underpinning and should consider a broad specter of potential health risks. This makes science‐based decision making a complex and challenging process that is urgently needed. After all, we do not want our rural citizens to be part of an ongoing natural experiment.
Smit, L. A. M. , & Heederik, D. (2017). Impacts of intensive livestock production on human health in densely populated regions. GeoHealth, 1 272–277, 10.1002/2017GH000103
References
- Bauer, S. E. , Tsigaridis, K. , & Miller, R. (2016). Significant atmospheric aerosol pollution caused by world food cultivation. Geophysical Research Letters, 43, 5394–5400. 10.1002/2016GL068354 [DOI] [Google Scholar]
- Beninca, E. , van Boven, M. , Hagenaars, T. , & van der Hoek, W. (2017). Space‐time analysis of pneumonia hospitalisations in the Netherlands. PloS One, 12(7), e0180797. 10.1371/journal.pone.0180797 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bieleman, J. (2010). Five centuries of farming In Five centuries of farming: A short history of dutch agriculture 1500–2000 (p. 367). Netherlands: Wageningen Academic Publishers. [Google Scholar]
- Borlée, F. , Yzermans, C. J. , Aalders, B. , Rooijackers, J. , Krop, E. , Maassen, C. B. M. , … Smit, L. A. M. (2017). Air pollution from livestock farms is associated with airway obstruction in neighboring residents. American Journal of Respiratory and Critical Care Medicine. 10.1164/rccm.201701-0021OC [DOI] [PubMed] [Google Scholar]
- Borlée, F. , Yzermans, C. J. , van Dijk, C. E. , Heederik, D. , & Smit, L. A. M. (2015). Increased respiratory symptoms in COPD patients living in the vicinity of livestock farms. The European Respiratory Journal, 46, 1605–1614. [DOI] [PubMed] [Google Scholar]
- Bos, M. E. , Verstappen, K. M. , van Cleef, B. A. , Dohmen, W. , Dorado‐Garcia, A. , Graveland, H. , … Heederik, D. J. (2016). Transmission through air as a possible route of exposure for MRSA. Journal of Exposure Science & Environmental Epidemiology, 26(3), 263–9. 10.1038/jes.2014.85 [DOI] [PubMed] [Google Scholar]
- Brunekreef, B. , Harrison, R. M. , Kunzli, N. , Querol, X. , Sutton, M. A. , Heederik, D. J. , & Sigsgaard, T. (2015). Reducing the health effect of particles from agriculture. The Lancet Respiratory Medicine, 3, 831–832. 10.1016/S2213-2600(15)00413-0 [DOI] [PubMed] [Google Scholar]
- Casey, J. A. , Shopsin, B. , Cosgrove, S. E. , Nachman, K. E. , Curriero, F. C. , Rose, H. R. , & Schwartz, B. S. (2014). High‐density livestock production and molecularly characterized MRSA infections in Pennsylvania. Environmental Health Perspectives, 122(5), 464–470. 10.1289/ehp.1307370 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Coker, R. , Rushton, J. , Mounier‐Jack, S. , Karimuribo, E. , Lutumba, P. , Kambarage, D. , … Rweyemamu, M. (2011). Towards a conceptual framework to support one‐health research for policy on emerging zoonoses. The Lancet Infectious Diseases, 11(4), 326–331. 10.1016/S1473-3099(10)70312-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cullen, A. (2017). Our Pulitzer Prize‐winning editorials. Retrieved from https://sltimesblog.wordpress.com/project-type/winning-work/ [Google Scholar]
- de Rooij, M. M. , Borlee, F. , Smit, L. A. , de Bruin, A. , Janse, I. , Heederik, D. J. , & Wouters, I. M. (2016). Detection of Coxiella burnetii in ambient air after a large Q fever outbreak. PloS One, 11(3), e0151281. 10.1371/journal.pone.0151281 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dierikx, C. , van der Goot, J. , Fabri, T. , van Essen‐Zandbergen, A. , Smith, H. , & Mevius, D. (2013). Extended‐spectrum‐beta‐lactamase‐ and AmpC‐beta‐lactamase‐producing Escherichia coli in Dutch broilers and broiler farmers. The Journal of Antimicrobial Chemotherapy, 68(1), 60–67. 10.1093/jac/dks349 [DOI] [PubMed] [Google Scholar]
- Dijkstra, F. , van der Hoek, W. , Wijers, N. , Schimmer, B. , Rietveld, A. , Wijkmans, C. J. , … Schneeberger, P. M. (2012). The 2007–2010 Q fever epidemic in the Netherlands: Characteristics of notified acute Q fever patients and the association with dairy goat farming. FEMS Immunology and Medical Microbiology, 64(1), 3–12. 10.1111/j.1574-695X.2011.00876.x [DOI] [PubMed] [Google Scholar]
- Dorado‐Garcia, A. , Mevius, D. J. , Jacobs, J. J. , Van Geijlswijk, I. M. , Mouton, J. W. , Wagenaar, J. A. , & Heederik, D. J. (2016). Quantitative assessment of antimicrobial resistance in livestock during the course of a nationwide antimicrobial use reduction in the Netherlands. The Journal of Antimicrobial Chemotherapy, 71(12), 3607–3619. 10.1093/jac/dkw308 [DOI] [PubMed] [Google Scholar]
- Freidl, G. S. , Spruijt, I. T. , Borlee, F. , Smit, L. A. , van Gageldonk‐Lafeber, A. B. , Heederik, D. J. , … van der Hoek, W. (2017). Livestock‐associated risk factors for pneumonia in an area of intensive animal farming in the Netherlands. PloS One, 12(3), e0174796. 10.1371/journal.pone.0174796 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Graveland, H. , Wagenaar, J. A. , Heesterbeek, H. , Mevius, D. , van Duijkeren, E. , & Heederik, D. (2010). Methicillin resistant Staphylococcus aureus ST398 in veal calf farming: Human MRSA carriage related with animal antimicrobial usage and farm hygiene. PloS One, 5(6), e10990. 10.1371/journal.pone.0010990 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hogerwerf, L. , Holstege, M. M. C. , Beninca, E. , Dijkstra, F. , & van der Hoek, W. (2017). Temporal and spatial analysis of psittacosis in association with poultry farming in the Netherlands, 2000–2015. BMC Infectious Diseases, 17(1), 519. 10.1186/s12879-017-2608-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huijbers, P. M. , de Kraker, M. , Graat, E. A. , van Hoek, A. H. , van Santen, M. G. , de Jong, M. C. , … de Greeff, S. C. (2013). Prevalence of extended‐spectrum beta‐lactamase‐producing Enterobacteriaceae in humans living in municipalities with high and low broiler density. Clinical Microbiology and Infection, 19(6), E256‐9. 10.1111/1469-0691.12150 [DOI] [PubMed] [Google Scholar]
- Huijskens, E. G. , Smit, L. A. , Rossen, J. W. , Heederik, D. , & Koopmans, M. (2016). Evaluation of patients with community‐acquired pneumonia caused by zoonotic pathogens in an area with a high density of animal farms. Zoonoses and Public Health, 63(2), 160–166. 10.1111/zph.12218 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 10.3201/eid1906.121645 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lelieveld, J. , Evans, J. S. , Fnais, M. , Giannadaki, D. , & Pozzer, A. (2015). The contribution of outdoor air pollution sources to premature mortality on a global scale. Nature, 525(7569), 367–371. 10.1038/nature15371 [DOI] [PubMed] [Google Scholar]
- Loftus, C. , Yost, M. , Sampson, P. , Torres, E. , Arias, G. , Breckwich Vasquez, V. , … Karr, C. (2015). Ambient ammonia exposures in an agricultural community and pediatric asthma morbidity. Epidemiology, 26(6), 794–801. 10.1097/EDE.0000000000000368 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 10.1289/ehp.1408555 [DOI] [PMC free article] [PubMed] [Google Scholar]
- One Health Initiative (2017). One Health Initiative will unite human and veterinary medicine. Retrieved from http://www.onehealthinitiative.com/index.php [Google Scholar]
- Poroyko, V. , Meng, F. , Meliton, A. , Afonyushkin, T. , Ulanov, A. , Semenyuk, E. , … Birukov, K. G. (2015). Alterations of lung microbiota in a mouse model of LPS‐induced lung injury. American Journal of Physiology. Lung Cellular and Molecular Physiology, 309(1), L76–L83. 10.1152/ajplung.00061.2014 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Radon, K. , Schulze, A. , Ehrenstein, V. , van Strien, R. T. , Praml, G. , & Nowak, D. (2007). Environmental exposure to confined animal feeding operations and respiratory health of neighboring residents. Epidemiology, 18(3), 300–308. 10.1097/01.ede.0000259966.62137.84 [DOI] [PubMed] [Google Scholar]
- Robinson, T. P. , Thornton, P. K. , Franceschini, G. , Kruska, R. L. , Chiozza, F. , Notenbaert, A. , … See, L. (2011). Global livestock production systems (152 pp.). Rome, Italy and Nairobi, Kenya: FAO and ILRI; Retrieved from https://www.fao.org/docrep/014/i2414e/i2414e.pdf [Google Scholar]
- Rylance, J. , Fullerton, D. G. , Scriven, J. , Aljurayyan, A. N. , Mzinza, D. , Barrett, S. , … Gordon, S. B. (2015). Household air pollution causes dose‐dependent inflammation and altered phagocytosis in human macrophages. American Journal of Respiratory Cell and Molecular Biology, 52(5), 584–593. 10.1165/rcmb.2014-0188OC [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schenker, M. B. , Christiani, D. , Cormier, Y. , Dimich‐Ward, H. , Doekes, G. , Dosman, J. , … Chan‐Yeung, M. (1998). Respiratory health hazards in agriculture. American Journal of Respiratory and Critical Care Medicine, 158(5 Pt 2), S1–S76. [DOI] [PubMed] [Google Scholar]
- Slot, E. , Zaaijer, H. L. , Molier, M. , Van den Hurk, K. , Prinsze, F. , & Hogema, B. M. (2017). Meat consumption is a major risk factor for hepatitis E virus infection. PloS One, 12(4), e0176414. 10.1371/journal.pone.0176414 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smit, L. A. M. , Boender, G. J. , de Steenhuijsen Piters, W. A. A. , Hagenaars, T. J. , Huijskens, E. G. W. , Rossen, J. W. A. , … Heederik, D. (2017). Increased risk of pneumonia in residents living near poultry farms: Does the upper respiratory tract microbiota play a role? Pneumonia (Nathan), 9, 3. 10.1186/s41479-017-0027-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ssematimba, A. , Hagenaars, T. J. , & de Jong, M. C. (2012). Modelling the wind‐borne spread of highly pathogenic avian influenza virus between farms. PloS One, 7(2), e31114. 10.1371/journal.pone.0031114 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Statistics Netherlands (2017). Statline, Livestock Retrieved from https://www.cbs.nl/nl-NL/menu/themas/landbouw/nieuws/default.htm
- van Dam, M. H. P. , & Dijksma, S. A. M. (2017). Reaction to various research into the relationship between livestock and health. Retrieved from https://zoek.officielebekendmakingen.nl/kst-28973-191
- Van den Brom, R. , van Engelen, E. , Roest, H. I. , van der Hoek, W. , & Vellema, P. (2015). Coxiella burnetii infections in sheep or goats: An opinionated review. Veterinary Microbiology, 181(1‐2), 119–129. 10.1016/j.vetmic.2015.07.011 [DOI] [PubMed] [Google Scholar]
- van Dijk, C. E. , Garcia‐Aymerich, J. , Carsin, A. E. , Smit, L. A. , Borlee, F. , Heederik, D. J. , … Zock, J. P. (2016). Risk of exacerbations in COPD and asthma patients living in the neighbourhood of livestock farms: Observational study using longitudinal data. International Journal of Hygiene and Environmental Health, 219(3), 278–287. 10.1016/j.ijheh.2016.01.002 [DOI] [PubMed] [Google Scholar]
- van Dijk, C. E. , Zock, J. P. , Baliatsas, C. , Smit, L. A. , Borlee, F. , Spreeuwenberg, P. , … Yzermans, C. J. (2017). Health conditions in rural areas with high livestock density: Analysis of seven consecutive years. Environmental Pollution, 222, 374–382. 10.1016/j.envpol.2016.12.023 [DOI] [PubMed] [Google Scholar]
- van Gageldonk‐Lafeber, A. B. , van der Hoek, W. , Borlee, F. , Heederik, D. J. , Mooi, S. H. , Maassen, C. B. , … Reimerink, J. H. (2017). Hepatitis E virus seroprevalence among the general population in a livestock‐dense area in the Netherlands: A cross‐sectional population‐based serological survey. BMC Infectious Diseases, 17(1), 21. 10.1186/s12879-016-2160-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vieno, M. , Heal, M. R. , Twigg, M. M. , MacKenzie, I. A. , Braban, C. F. , Lingard, J. J. N. , … Ots, R. (2016). The UK particulate matter air pollution episode of March–April 2014: More than Saharan dust. Environmental Research Letters, 11, 044004. [Google Scholar]
- Voss, A. , Loeffen, F. , Bakker, J. , Klaassen, C. , & Wulf, M. (2005). Methicillin‐resistant Staphylococcus aureus in pig farming. Emerging Infectious Diseases, 11(12), 1965–1966. 10.3201/eid1112.050428 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wielders, C. C. , van Hoek, A. H. , Hengeveld, P. D. , Veenman, C. , Dierikx, C. M. , Zomer, T. P. , … van Duijkeren, E. (2017). Extended‐spectrum beta‐lactamase‐ and pAmpC‐producing Enterobacteriaceae among the general population in a livestock‐dense area. Clinical Microbiology and Infection, 23(2), 120.e1–120.e8. 10.1016/j.cmi.2016.10.013 [DOI] [PubMed] [Google Scholar]
- Winkel, A. (2016). Particulate matter emission from livestock houses: Measurement methods, emission levels and abatement systems , (Doctoral dissertation). Retrieved from https://edepot.wur.nl/390454. Wageningen, Netherlands: Wageningen University. [Google Scholar]
- Zomer, T. P. , van Duijkeren, E. , Wielders, C. C. H. , Veenman, C. , Hengeveld, P. , van der Hoek, W. , … Maassen, C. B. M. (2017). Prevalence and risk factors for colonization of Clostridium difficile among adults living near livestock farms in the Netherlands. Epidemiology and Infection. 10.1017/S0950268817001753 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zomer, T. P. , Wielders, C. C. , Veenman, C. , Hengeveld, P. , van der Hoek, W. , de Greeff, S. C. , … van Duijkeren, E. (2017). MRSA in persons not living or working on a farm in a livestock‐dense area: Prevalence and risk factors. The Journal of Antimicrobial Chemotherapy, 72(3), 893–899. 10.1093/jac/dkw483 [DOI] [PubMed] [Google Scholar]