Lung Function Variation during the Estrus Cycle of Mares Affected by Severe Asthma.
Abstract: While the prevalence of asthma is higher in boys than in girls during childhood, this tendency reverses at puberty, suggesting an effect of sex hormones on the disease pathophysiology. Fluctuations of asthma severity concurring with the estrus cycle are reported in women, but this phenomenon has never been investigated in mares to date. The objective of this exploratory study was to determine whether the estrus cycle modulates airway obstruction in severe equine asthma (SEA). Five mares with SEA during exacerbation of the disease were studied. The whole breath, expiratory and inspiratory resistance, and reactance were compared during the follicular and luteal phases of the estrus cycle. The reproductive tract was evaluated by rectal palpation, ultrasound, and serum progesterone levels. The inspiratory resistance and reactance improved during the luteal phase of the estrus cycle, and variation in progesterone levels and the dominant follicle size correlated with several lung function parameters. The fluctuation of airway dysfunction during the estrus cycle is noteworthy as deterioration of the disease could perhaps be expected and prevented by horse owners and veterinarians. Further studies are required to determine if the equine species could be a suitable model to evaluate the effects of sex hormones on asthma.
Publication Date: 2022-02-17 PubMed ID: 35203202PubMed Central: PMC8868231DOI: 10.3390/ani12040494Google 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 focuses on investigating the potential influence of the estrus cycle on severe equine asthma (SEA) in mares. The study observes changes in lung function according to different phases of the estrus cycle and also suggests the possible use of the equine species as a model to evaluate the effects of sex hormones on asthma.
Objective of the Study
- The primary aim of this exploratory research was to determine if the estrus cycle influences airway obstruction in mares affected by severe equine asthma (SEA).
Methodology
- The study was conducted on five mares diagnosed with SEA during an exacerbation phase of the disease.
- The key parameters of lung function studied included the whole breath, expiratory and inspiratory resistance, and reactance. These factors were compared during both the follicular and luteal phases of the estrus cycle.
- The assessment of the reproductive tract was carried out using rectal palpation, ultrasound, and evaluating serum progesterone levels.
Findings
- The study revealed that the inspiratory resistance and reactance improved during the luteal phase of the estrus cycle.
- It also found a correlation between variations in progesterone levels and the size of the dominant follicle with several lung function parameters.
Significance and Future Directions
- The discovery of airway dysfunction fluctuation during the estrus cycle is significant because it suggests that disease deterioration could potentially be anticipated and prevented by horse owners and veterinarians.
- The study calls for further research to ascertain whether the equine species can be used as a suitable model for evaluating the effects of sex hormones on asthma in general.
Cite This Article
APA
Mainguy-Seers S, Diaw M, Lavoie JP.
(2022).
Lung Function Variation during the Estrus Cycle of Mares Affected by Severe Asthma.
Animals (Basel), 12(4), 494.
https://doi.org/10.3390/ani12040494 Publication
Researcher Affiliations
- Faculty of Veterinary Medicine, Department of Clinical Sciences, Université de Montréal, Saint-Hyacinthe, QC J2S 2M2, Canada.
- Faculty of Veterinary Medicine, Department of Clinical Sciences, Université de Montréal, Saint-Hyacinthe, QC J2S 2M2, Canada.
- Faculty of Veterinary Medicine, Department of Clinical Sciences, Université de Montréal, Saint-Hyacinthe, QC J2S 2M2, Canada.
Grant Funding
- PJT-148807 / CIHR
- Doctoral student grant (272483) / Fonds de Recherche du Quu00e9bec - Santu00e9
Conflict of Interest Statement
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
References
This article includes 58 references
- Shah R, Newcomb DC. Sex Bias in Asthma Prevalence and Pathogenesis.. Front Immunol 2018;9:2997.
- de Marco R, Locatelli F, Sunyer J, Burney P. Differences in incidence of reported asthma related to age in men and women. A retrospective analysis of the data of the European Respiratory Health Survey.. Am J Respir Crit Care Med 2000 Jul;162(1):68-74.
- Moore WC, Meyers DA, Wenzel SE, Teague WG, Li H, Li X, D'Agostino R Jr, Castro M, Curran-Everett D, Fitzpatrick AM, Gaston B, Jarjour NN, Sorkness R, Calhoun WJ, Chung KF, Comhair SA, Dweik RA, Israel E, Peters SP, Busse WW, Erzurum SC, Bleecker ER. Identification of asthma phenotypes using cluster analysis in the Severe Asthma Research Program.. Am J Respir Crit Care Med 2010 Feb 15;181(4):315-23.
- Wu W, Bang S, Bleecker ER, Castro M, Denlinger L, Erzurum SC, Fahy JV, Fitzpatrick AM, Gaston BM, Hastie AT, Israel E, Jarjour NN, Levy BD, Mauger DT, Meyers DA, Moore WC, Peters M, Phillips BR, Phipatanakul W, Sorkness RL, Wenzel SE. Multiview Cluster Analysis Identifies Variable Corticosteroid Response Phenotypes in Severe Asthma.. Am J Respir Crit Care Med 2019 Jun 1;199(11):1358-1367.
- Chen Y, Stewart P, Johansen H, McRae L, Taylor G. Sex difference in hospitalization due to asthma in relation to age.. J Clin Epidemiol 2003 Feb;56(2):180-7.
- Juniper EF, Kline PA, Roberts RS, Hargreave FE, Daniel EE. Airway responsiveness to methacholine during the natural menstrual cycle and the effect of oral contraceptives.. Am Rev Respir Dis 1987 May;135(5):1039-42.
- Gibbs CJ, Coutts II, Lock R, Finnegan OC, White RJ. Premenstrual exacerbation of asthma.. Thorax 1984 Nov;39(11):833-6.
- Hanley SP. Asthma variation with menstruation.. Br J Dis Chest 1981 Jul;75(3):306-8.
- Chandler MH, Schuldheisz S, Phillips BA, Muse KN. Premenstrual asthma: the effect of estrogen on symptoms, pulmonary function, and beta 2-receptors.. Pharmacotherapy 1997 Mar-Apr;17(2):224-34.
- Weinmann GG, Zacur H, Fish JE. Absence of changes in airway responsiveness during the menstrual cycle.. J Allergy Clin Immunol 1987 Apr;79(4):634-8.
- Brenner BE, Holmes TM, Mazal B, Camargo CA Jr. Relation between phase of the menstrual cycle and asthma presentations in the emergency department.. Thorax 2005 Oct;60(10):806-9.
- Zimmerman JL, Woodruff PG, Clark S, Camargo CA. Relation between phase of menstrual cycle and emergency department visits for acute asthma.. Am J Respir Crit Care Med 2000 Aug;162(2 Pt 1):512-5.
- Hotchkiss JW, Reid SW, Christley RM. A survey of horse owners in Great Britain regarding horses in their care. Part 2: Risk factors for recurrent airway obstruction.. Equine Vet J 2007 Jul;39(4):301-8.
- 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.
- Gerber V, Baleri D, Klukowska-Rötzler J, Swinburne JE, Dolf G. Mixed inheritance of equine recurrent airway obstruction.. J Vet Intern Med 2009 May-Jun;23(3):626-30.
- Couëtil LL, Ward MP. Analysis of risk factors for recurrent airway obstruction in North American horses: 1,444 cases (1990-1999).. J Am Vet Med Assoc 2003 Dec 1;223(11):1645-50.
- 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.
- van Erck E, Votion D, Art T, Lekeux P. Measurement of respiratory function by impulse oscillometry in horses.. Equine Vet J 2004 Jan;36(1):21-8.
- Desai U, Joshi JM. Impulse oscillometry.. Adv Respir Med 2019;87(4):235-238.
- Noden PA, Oxender WD, Hafs HD. The cycle of oestrus, ovulation and plasma levels of hormones in the mare.. J Reprod Fertil Suppl 1975 Oct;(23):189-92.
- Popovic RM, White DP. Upper airway muscle activity in normal women: influence of hormonal status.. J Appl Physiol (1985) 1998 Mar;84(3):1055-62.
- King GG, Bates J, Berger KI, Calverley P, de Melo PL, Dellacà RL, Farré R, Hall GL, Ioan I, Irvin CG, Kaczka DW, Kaminsky DA, Kurosawa H, Lombardi E, Maksym GN, Marchal F, Oppenheimer BW, Simpson SJ, Thamrin C, van den Berge M, Oostveen E. Technical standards for respiratory oscillometry.. Eur Respir J 2020 Feb;55(2).
- Satué K, Fazio E, Ferlazzo A, Medica P. Intrafollicular and systemic serotonin, oestradiol and progesterone concentrations in cycling mares.. Reprod Domest Anim 2019 Oct;54(10):1411-1418.
- 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.
- Klein C, Smith HJ, Reinhold P. The use of impulse oscillometry for separate analysis of inspiratory and expiratory impedance parameters in horses: effects of sedation with xylazine.. Res Vet Sci 2006 Apr;80(2):201-8.
- Saaresranta T, Aittokallio T, Polo-Kantola P, Helenius H, Polo O. Effect of medroxyprogesterone on inspiratory flow shapes during sleep in postmenopausal women.. Respir Physiol Neurobiol 2003 Mar 3;134(2):131-43.
- Morello SL, Ducharme NG, Hackett RP, Warnick LD, Mitchell LM, Soderholm LV. Activity of selected rostral and caudal hyoid muscles in clinically normal horses during strenuous exercise.. Am J Vet Res 2008 May;69(5):682-9.
- Goldman MD, Carter R, Klein R, Fritz G, Carter B, Pachucki P. Within- and between-day variability of respiratory impedance, using impulse oscillometry in adolescent asthmatics.. Pediatr Pulmonol 2002 Oct;34(4):312-9.
- Foster PS, Goldie RG, Paterson JW. Effect of steroids on beta-adrenoceptor-mediated relaxation of pig bronchus.. Br J Pharmacol 1983 Feb;78(2):441-5.
- White DP, Douglas NJ, Pickett CK, Weil JV, Zwillich CW. Sexual influence on the control of breathing.. J Appl Physiol Respir Environ Exerc Physiol 1983 Apr;54(4):874-9.
- Zhang X, Bao W, Fei X, Zhang Y, Zhang G, Zhou X, Zhang M. Progesterone attenuates airway remodeling and glucocorticoid resistance in a murine model of exposing to ozone.. Mol Immunol 2018 Apr;96:69-77.
- Beynon HL, Garbett ND, Barnes PJ. Severe premenstrual exacerbations of asthma: effect of intramuscular progesterone.. Lancet 1988 Aug 13;2(8607):370-2.
- Jain R, Ray JM, Pan JH, Brody SL. Sex hormone-dependent regulation of cilia beat frequency in airway epithelium.. Am J Respir Cell Mol Biol 2012 Apr;46(4):446-53.
- Bayliss DA, Millhorn DE. Central neural mechanisms of progesterone action: application to the respiratory system.. J Appl Physiol (1985) 1992 Aug;73(2):393-404.
- Van Erck E, Votion D, Kirschvink N, Genicot B, Lindsey J, Art T, Lekeux P. Influence of breathing pattern and lung inflation on impulse oscillometry measurements in horses.. Vet J 2004 Nov;168(3):259-69.
- Asavasupreechar T, Saito R, Miki Y, Edwards DP, Boonyaratanakornkit V, Sasano H. Systemic distribution of progesterone receptor subtypes in human tissues.. J Steroid Biochem Mol Biol 2020 May;199:105599.
- Intapad S, Dimitropoulou C, Snead C, Piyachaturawat P, Catravas JD. Regulation of asthmatic airway relaxation by estrogen and heat shock protein 90.. J Cell Physiol 2012 Aug;227(8):3036-43.
- Dimitropoulou C, White RE, Ownby DR, Catravas JD. Estrogen reduces carbachol-induced constriction of asthmatic airways by stimulating large-conductance voltage and calcium-dependent potassium channels.. Am J Respir Cell Mol Biol 2005 Mar;32(3):239-47.
- Flores-Delgado G, Bringas P, Buckley S, Anderson KD, Warburton D. Nongenomic estrogen action in human lung myofibroblasts.. Biochem Biophys Res Commun 2001 May 11;283(3):661-7.
- Degano B, Mourlanette P, Valmary S, Pontier S, Prévost MC, Escamilla R. Differential effects of low and high-dose estradiol on airway reactivity in ovariectomized rats.. Respir Physiol Neurobiol 2003 Nov 14;138(2-3):265-74.
- Dimitropoulou C, Drakopanagiotakis F, Chatterjee A, Snead C, Catravas JD. Estrogen replacement therapy prevents airway dysfunction in a murine model of allergen-induced asthma.. Lung 2009 Mar-Apr;187(2):116-27.
- Carey MA, Card JW, Bradbury JA, Moorman MP, Haykal-Coates N, Gavett SH, Graves JP, Walker VR, Flake GP, Voltz JW, Zhu D, Jacobs ER, Dakhama A, Larsen GL, Loader JE, Gelfand EW, Germolec DR, Korach KS, Zeldin DC. Spontaneous airway hyperresponsiveness in estrogen receptor-alpha-deficient mice.. Am J Respir Crit Care Med 2007 Jan 15;175(2):126-35.
- Tam A, Wadsworth S, Dorscheid D, Man SF, Sin DD. Estradiol increases mucus synthesis in bronchial epithelial cells.. PLoS One 2014;9(6):e100633.
- Ensom MH, Chong G, Zhou D, Beaudin B, Shalansky S, Bai TR. Estradiol in premenstrual asthma: a double-blind, randomized, placebo-controlled, crossover study.. Pharmacotherapy 2003 May;23(5):561-71.
- DeBoer MD, Phillips BR, Mauger DT, Zein J, Erzurum SC, Fitzpatrick AM, Gaston BM, Myers R, Ross KR, Chmiel J, Lee MJ, Fahy JV, Peters M, Ly NP, Wenzel SE, Fajt ML, Holguin F, Moore WC, Peters SP, Meyers D, Bleecker ER, Castro M, Coverstone AM, Bacharier LB, Jarjour NN, Sorkness RL, Ramratnam S, Irani AM, Israel E, Levy B, Phipatanakul W, Gaffin JM, Gerald Teague W. Effects of endogenous sex hormones on lung function and symptom control in adolescents with asthma.. BMC Pulm Med 2018 Apr 10;18(1):58.
- McCleary N, Nwaru BI, Nurmatov UB, Critchley H, Sheikh A. Endogenous and exogenous sex steroid hormones in asthma and allergy in females: A systematic review and meta-analysis.. J Allergy Clin Immunol 2018 Apr;141(4):1510-1513.e8.
- Dijkstra A, Howard TD, Vonk JM, Ampleford EJ, Lange LA, Bleecker ER, Meyers DA, Postma DS. Estrogen receptor 1 polymorphisms are associated with airway hyperresponsiveness and lung function decline, particularly in female subjects with asthma.. J Allergy Clin Immunol 2006 Mar;117(3):604-11.
- Mainguy-Seers S, Picotte K, Lavoie JP. Efficacy of tamoxifen for the treatment of severe equine asthma.. J Vet Intern Med 2018 Sep;32(5):1748-1753.
- Lam SM, Huang SC. Premenstrual asthma: report of a case with hormonal studies.. J Microbiol Immunol Infect 1998 Sep;31(3):197-9.
- Schatz M, Harden K, Forsythe A, Chilingar L, Hoffman C, Sperling W, Zeiger RS. The course of asthma during pregnancy, post partum, and with successive pregnancies: a prospective analysis.. J Allergy Clin Immunol 1988 Mar;81(3):509-17.
- Claes A, Ball BA, Scoggin KE, Roser JF, Woodward EM, Davolli GM, Squires EL, Troedsson MHT. The influence of age, antral follicle count and diestrous ovulations on estrous cycle characteristics of mares.. Theriogenology 2017 Jul 15;97:34-40.
- Carnevale EM. The mare model for follicular maturation and reproductive aging in the woman.. Theriogenology 2008 Jan 1;69(1):23-30.
- Matteis M, Polverino F, Spaziano G, Roviezzo F, Santoriello C, Sullo N, Bucci MR, Rossi F, Polverino M, Owen CA, D'Agostino B. Effects of sex hormones on bronchial reactivity during the menstrual cycle.. BMC Pulm Med 2014 Jul 1;14:108.
- Scott HA, Gibson PG, Garg ML, Upham JW, Wood LG. Sex hormones and systemic inflammation are modulators of the obese-asthma phenotype.. Allergy 2016 Jul;71(7):1037-47.
- Arathimos R, Granell R, Haycock P, Richmond RC, Yarmolinsky J, Relton CL, Tilling K. Genetic and observational evidence supports a causal role of sex hormones on the development of asthma.. Thorax 2019 Jul;74(7):633-642.
- Asa CS, Robinson JA, Ginther OJ. Changes in plasma cortisol concentrations during the ovulatory cycle of the mare.. J Endocrinol 1983 Nov;99(2):329-34.
- Satué K, Montesinos P, Muñoz A. Modulation of the renin-angiotensin-aldosterone system by steroid hormones during the oestrous cycle in mares.. Acta Vet Hung 2020 Mar;68(1):79-84.
- Young SS, Tesarowski D, Viel L. Frequency dependence of forced oscillatory respiratory mechanics in horses with heaves.. J Appl Physiol (1985) 1997 Mar;82(3):983-7.
Citations
This article has been cited 5 times.- Lo Feudo CM, Ferrucci F, Bizzotto D, Dellacà R, Lavoie JP, Stucchi L. Differences in pulmonary function measured by oscillometry between horses with mild-moderate equine asthma and healthy controls. Equine Vet J 2025 May;57(3):619-628.
- Mozo Vives B, Mainguy-Seers S, Lavoie JP. Comparative study of the bronchodilator efficacy and adverse effects of salbutamol and hyoscine butylbromide in horses with severe asthma. J Vet Intern Med 2024 May-Jun;38(3):1835-1841.
- Greim E, Naef J, Mainguy-Seers S, Lavoie JP, Sage S, Dolf G, Gerber V. Breath characteristics and adventitious lung sounds in healthy and asthmatic horses. J Vet Intern Med 2024 Jan-Feb;38(1):495-504.
- Mönki J, Holopainen M, Ruhanen H, Karikoski N, Käkelä R, Mykkänen A. Lipid species profiling of bronchoalveolar lavage fluid cells of horses housed on two different bedding materials. Sci Rep 2023 Dec 8;13(1):21778.
- Stucchi L, Lo Feudo CM, Ferrucci F. Equine Respiratory Medicine and Cardiology. Animals (Basel) 2023 Sep 18;13(18).
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