Increased Weekly Mean PM2.5, and NO2 Are Associated With Increased Proportions of Lower Airway Granulocytes in Ontario Horses.
Abstract: Ambient pollution is associated with the development and exacerbation of human asthma, but whether air pollution exposure is associated with lower airway inflammation in horses has not been fully evaluated. The Air Quality Health Index (AQHI) is an online tool used by asthmatic Ontarians to modify their outdoor activity when ambient pollution is high. A single AQHI value, falling on a scale from 1 to 10, is calculated from measurements of fine particulate matter (PM), nitrogen dioxide (NO), and ozone (O). Increased AQHI values predict an increased risk for presenting to a health care provider for assessment of asthma exacerbation, with a time lag of 0-9 days after an increase. Whether ambient air pollution is a risk factor for identifying increased lower airway inflammatory cells on cytologic evaluation of bronchoalveolar lavage fluid (BALF) of horses has not yet been explored. To investigate this relationship, case data including BALF cytology preparations from horses across southern Ontario, Canada, were retrieved from the Guelph Animal Health Laboratory's archives. Spanning the years 2007-2017, 154 cases were identified within a 41- by 30-km area surrounding the cities of Guelph and Kitchener. In 78 of 154 cases, cytologic reevaluation identified increased proportions of one or a combination of BALF neutrophils (mean 5%, range 0-15%), eosinophils (mean 2%, range 0-31%), and mast cells (mean 4%, range 0-10%). To assess the effect of lagged pollutant and temperature exposures in these 78 cases, weekly mean values of AQHI, PM, NO, O, and temperature were recorded for the 4 weeks prior to the date of the horse's presentation for respiratory tract evaluation. The relationship between ambient exposures and increased proportions of lower airway granulocytes was evaluated using a case-crossover design. Single unit increases in 2-, and 3-week lagged weekly mean PM and NO, were associated, respectively, with an 11% ( = 0.04, 95% confidence interval, CI = 1.01-1.22), and 24% ( = 0.03, 95% CI = 1.08-1.43) greater risk of identifying increased lower airway granulocytes. These findings suggest that exposure to increased ambient pollutants is associated with lower airway inflammation in Guelph and Kitchener area horses.
Copyright © 2020 Brankston, Greer, Marshall, Lang, Moore, Hodgins, Hennessey and Beeler-Marfisi.
Publication Date: 2020-05-05 PubMed ID: 32432128PubMed Central: PMC7214617DOI: 10.3389/fvets.2020.00185Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
The research article indicates that exposure to outdoor pollutants, particularly fine particulate matter (PM2.5) and nitrogen dioxide (NO2), correlates with increased inflammation in the lower airways of horses in Ontario, Canada.
Research Context and Methodology
- The scientists based their study on the understanding that ambient pollution contributes to the development of asthma in humans. To examine the impact on horses, they interrogated the relationship between exposure to pollutants and inflammation in the lower airways of horses. To this end, bronchoalveolar lavage fluid (BALF) cytologies from Southern Ontario horses were retrospectively examined.
- The study analyzed 154 cases over a 10 year period. The area covered a 30 km by 41 km region surrounding the cities of Guelph and Kitchener.
- Data concerning weekly mean values of PM, NO, O, temperature, and the Air Quality Health Index (AQHI) for the 4 weeks preceding each horse’s presentation were recorded and analyzed. AQHI is an online tool used by asthmatics to adjust their outdoor activity according to the ambient pollution levels.
Research Findings
- The researchers discovered that in 78 out of 154 cases, horses indicated an increase in the percentage of one or more types of inflammatory cells in their BALF, including neutrophils, eosinophils, and mast cells. This suggests that these cases exhibited signs of lower airway inflammation.
- Evidence showed a direct relationship between the proportions of lower airway granulocytes – a type of white blood cell – and pollutant exposure. In particular, single unit increases in two-week and three-week lagged weekly mean levels of PM and NO were linked with an 11% and 24% increase in the risk of identifying these granulocytes, respectively.
- Therefore, it can be inferred that a higher AQHI value, indicating poorer air quality, could pose a risk for lower airway inflammation in horses, evident up to three weeks after exposure. Particular focus was on two components of the AQHI – PM and NO.
Conclusion and Implications
- The study’s findings suggest that exposure to elevated levels of ambient pollution could lead to lower airway inflammation among horses, mimicking the effect seen in humans.
- These results could raise awareness about the impact of prolonged exposure to outdoor pollutants on the health of horses, potentially influencing regulations and horse care practices in areas where air pollution is of concern.
Cite This Article
APA
Brankston G, Greer AL, Marshall Q, Lang B, Moore K, Hodgins D, Hennessey JTG, Beeler-Marfisi J.
(2020).
Increased Weekly Mean PM2.5, and NO2 Are Associated With Increased Proportions of Lower Airway Granulocytes in Ontario Horses.
Front Vet Sci, 7, 185.
https://doi.org/10.3389/fvets.2020.00185 Publication
Researcher Affiliations
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada.
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada.
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada.
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada.
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada.
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada.
- Hennessey Equine Veterinary Professional Corp., Rockwood, ON, Canada.
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada.
References
This article includes 63 references
- Wood JL, Newton JR, Chanter N, Mumford JA. Inflammatory airway disease, nasal discharge and respiratory infections in young British racehorses.. Equine Vet J 2005 May;37(3):236-42.
- Allen KJ, Tremaine WH, Franklin SH. Prevalence of inflammatory airway disease in national hunt horses referred for investigation of poor athletic performance.. Equine Vet J Suppl 2006 Aug;(36):529-34.
- Couëtil LL, Cardwell JM, Gerber V, Lavoie JP, Léguillette R, Richard EA. Inflammatory Airway Disease of Horses--Revised Consensus Statement.. J Vet Intern Med 2016 Mar-Apr;30(2):503-15.
- Holcombe SJ, Jackson C, Gerber V, Jefcoat A, Berney C, Eberhardt S, Robinson NE. Stabling is associated with airway inflammation in young Arabian horses.. Equine Vet J 2001 May;33(3):244-9.
- Ivester KM, Couëtil LL, Moore GE. An observational study of environmental exposures, airway cytology, and performance in racing thoroughbreds.. J Vet Intern Med 2018 Sep;32(5):1754-1762.
- Bond S, Léguillette R, Richard EA, Couetil L, Lavoie JP, Martin JG, Pirie RS. Equine asthma: Integrative biologic relevance of a recently proposed nomenclature.. J Vet Intern Med 2018 Nov;32(6):2088-2098.
- GINA nGlobal Initiative for Asthma. Global Strategy for Asthma Management and Prevention. 2019.
- Hare JE, Viel L. Pulmonary eosinophilia associated with increased airway responsiveness in young racing horses.. J Vet Intern Med 1998 May-Jun;12(3):163-70.
- Riihimäki M, Lilliehöök I, Raine A, Berg M, Pringle J. Clinical alterations and mRNA levels of IL-4 and IL-5 in bronchoalveolar cells of horses with transient pulmonary eosinophilia.. Res Vet Sci 2008 Aug;85(1):52-5.
- Nolen-Walston RD, Harris M, Agnew ME, Martin BB, Reef VB, Boston RC, Davidson EJ. Clinical and diagnostic features of inflammatory airway disease subtypes in horses examined because of poor performance: 98 cases (2004-2010).. J Am Vet Med Assoc 2013 Apr 15;242(8):1138-45.
- Moore BR, Krakowka S, Robertson JT, Cummins JM. Cytologic evaluation of bronchoalveolar lavage fluid obtained from standardbred racehorses with inflammatory airway disease.. Am J Vet Res 1995 May;56(5):562-7.
- Gibson PG. Inflammatory phenotypes in adult asthma: clinical applications.. Clin Respir J 2009 Oct;3(4):198-206.
- Andersson C, Tufvesson E, Diamant Z, Bjermer L. Revisiting the role of the mast cell in asthma.. Curr Opin Pulm Med 2016 Jan;22(1):10-7.
- Newton JR, Wood JL. Evidence of an association between inflammatory airway disease and EIPH in young Thoroughbreds during training.. Equine Vet J Suppl 2002 Sep;(34):417-24.
- Sánchez A, Couëtil LL, Ward MP, Clark SP. Effect of airway disease on blood gas exchange in racehorses.. J Vet Intern Med 2005 Jan-Feb;19(1):87-92.
- Ter Woort F, Caswell JL, Arroyo LG, Viel L. Histologic investigation of airway inflammation in postmortem lung samples from racehorses.. Am J Vet Res 2018 Mar;79(3):342-347.
- Hinchcliff KW, Couetil LL, Knight PK, Morley PS, Robinson NE, Sweeney CR, van Erck E. Exercise induced pulmonary hemorrhage in horses: American College of Veterinary Internal Medicine consensus statement.. J Vet Intern Med 2015 May-Jun;29(3):743-58.
- Avdalovic M. Pulmonary vasculature and critical asthma syndromes: a comprehensive review.. Clin Rev Allergy Immunol 2015 Feb;48(1):97-103.
- Nicolai T, Illi S, Tenbörg J, Kiess W, v Mutius E. Puberty and prognosis of asthma and bronchial hyper-reactivity.. Pediatr Allergy Immunol 2001 Jun;12(3):142-8.
- Millerick-May ML, Karmaus W, Derksen FJ, Berthold B, Holcombe SJ, Robinson NE. Local airborne particulate concentration is associated with visible tracheal mucus in Thoroughbred racehorses.. Equine Vet J 2013 Jan;45(1):85-90.
- Mills PC, Roberts CA, Smith NC. Effects of ozone and airway inflammation on glutathione status and iron homeostasis in the lungs of horses.. Am J Vet Res 1996 Sep;57(9):1359-63.
- Gates MC. The influence of air pollution on Thoroughbred race performance. Equine Comp Exerc Physiol 2007;4:79–88.
- Achakulwisut P, Brauer M, Hystad P, Anenberg SC. Global, national, and urban burdens of paediatric asthma incidence attributable to ambient NO(2) pollution: estimates from global datasets.. Lancet Planet Health 2019 Apr;3(4):e166-e178.
- Khreis H, Kelly C, Tate J, Parslow R, Lucas K, Nieuwenhuijsen M. Exposure to traffic-related air pollution and risk of development of childhood asthma: A systematic review and meta-analysis.. Environ Int 2017 Mar;100:1-31.
- To T, Shen S, Atenafu EG, Guan J, McLimont S, Stocks B, Licskai C. The air quality health index and asthma morbidity: a population-based study.. Environ Health Perspect 2013 Jan;121(1):46-52.
- Szyszkowicz M, Kousha T. Emergency department visits for asthma in relation to the Air Quality Health Index: a case-crossover study in Windsor, Canada.. Can J Public Health 2014 Jul 31;105(5):e336-41.
- Stieb DM, Burnett RT, Smith-Doiron M, Brion O, Shin HH, Economou V. A new multipollutant, no-threshold air quality health index based on short-term associations observed in daily time-series analyses.. J Air Waste Manag Assoc 2008 Mar;58(3):435-50.
- Regional Office for Europe. Air Quality Guidelines Global Update 2005:Particulate Matter, Ozone, Nitrogen Dioxide and Sulfur Dioxide. 2006.
- Mills IC, Atkinson RW, Anderson HR, Maynard RL, Strachan DP. Distinguishing the associations between daily mortality and hospital admissions and nitrogen dioxide from those of particulate matter: a systematic review and meta-analysis.. BMJ Open 2016 Jul 21;6(7):e010751.
- Fan J, Li S, Fan C, Bai Z, Yang K. The impact of PM2.5 on asthma emergency department visits: a systematic review and meta-analysis.. Environ Sci Pollut Res Int 2016 Jan;23(1):843-50.
- Ghio AJ, Turi JL, Madden MC, Dailey LA, Richards JD, Stonehuerner JG, Morgan DL, Singleton S, Garrick LM, Garrick MD. Lung injury after ozone exposure is iron dependent.. Am J Physiol Lung Cell Mol Physiol 2007 Jan;292(1):L134-43.
- Putman E, Liese W, Voorhout WF, van Bree L, van Golde LM, Haagsman HP. Short-term ozone exposure affects the surface activity of pulmonary surfactant.. Toxicol Appl Pharmacol 1997 Feb;142(2):288-96.
- Che L, Jin Y, Zhang C, Lai T, Zhou H, Xia L, Tian B, Zhao Y, Liu J, Wu Y, Wu Y, Du J, Li W, Ying S, Chen Z, Shen H. Ozone-induced IL-17A and neutrophilic airway inflammation is orchestrated by the caspase-1-IL-1 cascade.. Sci Rep 2016 Jan 7;6:18680.
- Cheng W, Duncan KE, Ghio AJ, Ward-Caviness C, Karoly ED, Diaz-Sanchez D, Conolly RB, Devlin RB. Changes in Metabolites Present in Lung-Lining Fluid Following Exposure of Humans to Ozone.. Toxicol Sci 2018 Jun 1;163(2):430-439.
- Analitis A, De' Donato F, Scortichini M, Lanki T, Basagana X, Ballester F, Astrom C, Paldy A, Pascal M, Gasparrini A, Michelozzi P, Katsouyanni K. Synergistic Effects of Ambient Temperature and Air Pollution on Health in Europe: Results from the PHASE Project.. Int J Environ Res Public Health 2018 Aug 28;15(9).
- Malley CS, Henze DK, Kuylenstierna JCI, Vallack HW, Davila Y, Anenberg SC, Turner MC, Ashmore MR. Updated Global Estimates of Respiratory Mortality in Adults ≥30Years of Age Attributable to Long-Term Ozone Exposure.. Environ Health Perspect 2017 Aug 28;125(8):087021.
- Zu K, Shi L, Prueitt RL, Liu X, Goodman JE. Critical review of long-term ozone exposure and asthma development.. Inhal Toxicol 2018 Feb;30(3):99-113.
- Riihimäki M, Raine A, Elfman L, Pringle J. Markers of respiratory inflammation in horses in relation to seasonal changes in air quality in a conventional racing stable.. Can J Vet Res 2008 Oct;72(5):432-9.
- Davis MS, Malayer JR, Vandeventer L, Royer CM, McKenzie EC, Williamson KK. Cold weather exercise and airway cytokine expression.. J Appl Physiol (1985) 2005 Jun;98(6):2132-6.
- Robinson NE, Karmaus W, Holcombe SJ, Carr EA, Derksen FJ. Airway inflammation in Michigan pleasure horses: prevalence and risk factors.. Equine Vet J 2006 Jul;38(4):293-9.
- Bullone M, Murcia RY, Lavoie JP. Environmental heat and airborne pollen concentration are associated with increased asthma severity in horses.. Equine Vet J 2016 Jul;48(4):479-84.
- Kim J, Lim Y, Kim H. Outdoor temperature changes and emergency department visits for asthma in Seoul, Korea: A time-series study.. Environ Res 2014 Nov;135:15-20.
- Xu Z, Huang C, Su H, Turner LR, Qiao Z, Tong S. Diurnal temperature range and childhood asthma: a time-series study.. Environ Health 2013 Feb 1;12:12.
- Rundell KW, Anderson SD, Sue-Chu M, Bougault V, Boulet LP. Air quality and temperature effects on exercise-induced bronchoconstriction.. Compr Physiol 2015 Apr;5(2):579-610.
- Hyrkäs H, Ikäheimo TM, Jaakkola JJ, Jaakkola MS. Asthma control and cold weather-related respiratory symptoms.. Respir Med 2016 Apr;113:1-7.
- Mirabelli MC, Vaidyanathan A, Flanders WD, Qin X, Garbe P. Outdoor PM2.5, Ambient Air Temperature, and Asthma Symptoms in the Past 14 Days among Adults with Active Asthma.. Environ Health Perspect 2016 Dec;124(12):1882-1890.
- Ren C, Williams GM, Tong S. Does particulate matter modify the association between temperature and cardiorespiratory diseases?. Environ Health Perspect 2006 Nov;114(11):1690-6.
- Dharmarajan S, Lee JY, Izem R. Sample size estimation for case-crossover studies.. Stat Med 2019 Mar 15;38(6):956-968.
- Hoffman AM. Bronchoalveolar lavage: sampling technique and guidelines for cytologic preparation and interpretation.. Vet Clin North Am Equine Pract 2008 Aug;24(2):423-35, vii-viii.
- Fernandez NJ, Hecker KG, Gilroy CV, Warren AL, Léguillette R. Reliability of 400-cell and 5-field leukocyte differential counts for equine bronchoalveolar lavage fluid.. Vet Clin Pathol 2013 Mar;42(1):92-8.
- Rossi H, Virtala AM, Raekallio M, Rahkonen E, Rajamäki MM, Mykkänen A. Comparison of Tracheal Wash and Bronchoalveolar Lavage Cytology in 154 Horses With and Without Respiratory Signs in a Referral Hospital Over 2009-2015.. Front Vet Sci 2018;5:61.
- Maclure M. The case-crossover design: a method for studying transient effects on the risk of acute events.. Am J Epidemiol 1991 Jan 15;133(2):144-53.
- Levy D, Lumley T, Sheppard L, Kaufman J, Checkoway H. Referent selection in case-crossover analyses of acute health effects of air pollution.. Epidemiology 2001 Mar;12(2):186-92.
- Dohoo IR, Martin SW, Strhyn H. Veterinary Epidemiologic Research. 2003.
- He M, Ichinose T, Yoshida S, Ito T, He C, Yoshida Y, Arashidani K, Takano H, Sun G, Shibamoto T. PM2.5-induced lung inflammation in mice: Differences of inflammatory response in macrophages and type II alveolar cells.. J Appl Toxicol 2017 Oct;37(10):1203-1218.
- Orellano P, Quaranta N, Reynoso J, Balbi B, Vasquez J. Effect of outdoor air pollution on asthma exacerbations in children and adults: Systematic review and multilevel meta-analysis.. PLoS One 2017;12(3):e0174050.
- Han M, Ji X, Li G, Sang N. NO(2) inhalation enhances asthma susceptibility in a rat model.. Environ Sci Pollut Res Int 2017 Dec;24(36):27843-27854.
- Martin RA, Ather JL, Lundblad LK, Suratt BT, Boyson JE, Budd RC, Alcorn JF, Flavell RA, Eisenbarth SC, Poynter ME. Interleukin-1 receptor and caspase-1 are required for the Th17 response in nitrogen dioxide-promoted allergic airway disease.. Am J Respir Cell Mol Biol 2013 May;48(5):655-64.
- Millerick-May ML, Karmaus W, Derksen FJ, Berthold B, Robinson NE. Airborne particulates (PM10) and tracheal mucus: A case-control study at an American Thoroughbred racetrack.. Equine Vet J 2015 Jul;47(4):410-4.
- Wålinder R, Riihimäki M, Bohlin S, Hogstedt C, Nordquist T, Raine A, Pringle J, Elfman L. Installation of mechanical ventilation in a horse stable: effects on air quality and human and equine airways.. Environ Health Prev Med 2011 Jul;16(4):264-72.
- Ivester KM, Couëtil LL, Zimmerman NJ. Investigating the link between particulate exposure and airway inflammation in the horse.. J Vet Intern Med 2014 Nov-Dec;28(6):1653-65.
- Dauchet L, Hulo S, Cherot-Kornobis N, Matran R, Amouyel P, Edmé JL, Giovannelli J. Short-term exposure to air pollution: Associations with lung function and inflammatory markers in non-smoking, healthy adults.. Environ Int 2018 Dec;121(Pt 1):610-619.
- Houtsma A, Bedenice D, Pusterla N, Pugliese B, Mapes S, Hoffman AM, Paxson J, Rozanski E, Mukherjee J, Wigley M, Mazan MR. Association between inflammatory airway disease of horses and exposure to respiratory viruses: a case control study.. Multidiscip Respir Med 2015;10:33.
Citations
This article has been cited 3 times.- Araneda OF. Horse Racing as a Model to Study the Relationship between Air Pollutants and Physical Performance.. Animals (Basel) 2022 Apr 28;12(9).
- Huang W, Wu J, Lin X. Ozone Exposure and Asthma Attack in Children.. Front Pediatr 2022;10:830897.
- Kang H, Bienzle D, Lee GKC, Piché É, Viel L, Odemuyiwa SO, Beeler-Marfisi J. Flow cytometric analysis of equine bronchoalveolar lavage fluid cells in horses with and without severe equine asthma.. Vet Pathol 2022 Jan;59(1):91-99.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists