Severely Asthmatic Horses Residing in a Mediterranean Climate Shed a Significantly Lower Number of Parasite Eggs Compared to Healthy Farm Mates.
Abstract: The relationship between helminth infection and allergic diseases has long intrigued the scientific community. This interaction was previously studied in a horse family with high incidence of severe equine asthma and in non-related severely asthmatic horses from equine hospital referrals in Switzerland. Our aim was to determine if this interaction would also be observed in a group of non-related client-owned severely asthmatic horses living in a Mediterranean climate and recruited through a first-opinion veterinarian group. Fecal samples from severe equine asthma-affected and healthy horses living in the same farms and subjected to identical environmental and deworming management were evaluated qualitatively and quantitatively. Strongyle-type eggs and larvae were the most abundant parasites in the studied population of horses; no significant differences between the groups were observed regarding the types of egg and infective larvae. However, we observed significant differences in the number of eggs and infective larvae per gram of feces shed, as this number was significantly lower in the SEA group than in the healthy horses. This may indicate that severely asthmatic horses have an intrinsic resistance to gastrointestinal helminths. Further studies in a larger population of horses are required to ascertain the immunological mechanisms responsible for these findings.
Publication Date: 2023-09-15 PubMed ID: 37760328PubMed Central: PMC10525552DOI: 10.3390/ani13182928Google Scholar: Lookup
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Summary
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The article investigates the relationship between parasite infection and severe equine asthma in horses, observing that asthmatic horses living in Mediterranean climates shed fewer eggs than healthy counterparts.
Background
- The research is driven by an ongoing scientific intrigue towards the interaction between helminth (a type of parasite) infections and allergic diseases. Previous studies in Switzerland on related asthmatic horses, and those referred by equine hospitals, identified a potential interaction.
- The aim of this paper was to explore whether this interaction also occurs in a select group of non-related, owner-owned asthmatic horses living in a Mediterranean climate.
Methodology
- The researchers used fecal samples from horses suffering from severe equine asthma, and compared these to samples from healthy horses living on the same farms, and under the same environmental and deworming conditions.
- These samples were tested both qualitatively and quantitatively.
Findings and Results
- The research identified Strongyle-type eggs and larvae as the most common parasites in the studied horse population.
- No significant differences were observed between the asthmatic and healthy horses in terms of the types of eggs and infective larvae present in their systems.
- A significant difference was observed in the number of eggs and infective larvae per gram of feces shed – the count was significantly lower in the group of severely asthmatic horses compared with the healthy horses.
Conclusion and Further Studies
- The study suggests that severely asthmatic horses might have an intrinsic resistance towards gastrointestinal helminths, which could explain the decreased egg count.
- The findings indicate potential for further studies on a larger population of horses, in order to better understand the immunological mechanisms causing this phenomenon.
Cite This Article
APA
Simões J, Sales Luís JP, Madeira de Carvalho L, Tilley P.
(2023).
Severely Asthmatic Horses Residing in a Mediterranean Climate Shed a Significantly Lower Number of Parasite Eggs Compared to Healthy Farm Mates.
Animals (Basel), 13(18), 2928.
https://doi.org/10.3390/ani13182928 Publication
Researcher Affiliations
- Equine Health and Welfare Academic Division, Faculty of Veterinary Medicine, Lusófona University, Campo Grande 376, 1749-024 Lisbon, Portugal.
- CIISA-Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
- Associate Laboratory for Animal and Veterinary Sciences (AL4Animals), Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
- CIISA-Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
- Associate Laboratory for Animal and Veterinary Sciences (AL4Animals), Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
- CIISA-Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
- Associate Laboratory for Animal and Veterinary Sciences (AL4Animals), Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
- CIISA-Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
- Associate Laboratory for Animal and Veterinary Sciences (AL4Animals), Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
Grant Funding
- UIDB/00276/2020 and LA/P/0059/2020 / Fundau00e7u00e3o para a Ciu00eancia e Tecnologia
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 48 references
- Weiss S.T.. Parasites and asthma/allergy: What is the relationship?. J. Allergy Clin. Immunol. 2000;105:205–210.
- Lambrecht B.N., Hammad H.. The immunology of the allergy epidemic and the hygiene hypothesis. Nat. Immunol. 2017;18:1076–1083.
- Aldakheel F.M.. Allergic diseases: A comprehensive review on risk factors, immunological mechanisms, link with COVID-19, potential treatments, and role of allergen bioinformatics. Int. J. Environ. Res. Public Health 2021;18:12105.
- Bullone M., Lavoie J.P.. The equine asthma model of airway remodeling: From a veterinary to a human perspective. Cell Tissue Res. 2020;380:223–236.
- Couëtil L.L., Cardwell J.M., Gerber V., Lavoie J.P., Léguillette R., Richard E.A.. Inflammatory Airway Disease of Horses-Revised Consensus Statement. J. Vet. Intern. Med. 2016;30:503–515.
- Hotchkiss J.W., Reid S.W.J., Christley R.M.. A survey of horse owners in Great Britain regarding horses in their care. Part 1: Horse demographic characteristics and management. Equine Vet. J. 2007;39:294–300.
- Ireland J.L., Christley R.M., McGowan C.M., Clegg P.D., Pinchbeck G.L., Martynski P.D., Payne R.J., Wylie C.E., Smith S., Marr C.M.. Prevalence of and Risk Factors for Recurrent Airway Obstruction in Geriatric Horses and Ponies. Equine Vet. J. 2015;47:25.
- Gerber V., Straub R., Marti E., Hauptman J., Herholz C., King M., Imhof A., Tahon L., Robinson N.E.. Endoscopic scoring of mucus quantity and quality: Observer and horse variance and relationship to inflammation, mucus viscoelasticity and volume. Equine Vet. J. 2004;36:576–582.
- Tilley P., Sales Luis J.P., Branco Ferreira M.. Correlation and discriminant analysis between clinical, endoscopic, thoracic X-ray and bronchoalveolar lavage fluid cytology scores, for staging horses with recurrent airway obstruction (RAO). Res. Vet. Sci. 2012;93:1006–1014.
- Simões J., Sales Luís J., Tilley P.. Contribution of lung function tests to the staging of severe equine asthma syndrome in the field. Res. Vet. Sci. 2019;123:112–117.
- Lynch N.R., Hagel I.A., Palenque M.E., Di Prisco M.C., Escudero J.E., Alejandra Corao L., Sandia J.A., Ferreira L.J., Botto C., Perez M.. Relationship between helminthic infection and IgE response in atopic and nonatopic children in a tropical environment. J. Allergy Clin. Immunol. 1998;101:217–221.
- Capron A., Dombrowicz D., Capron M.. Helminth Infections and Allergic Diseases: From the Th2 Paradigm to Regulatory Networks. Clin. Rev. Allergy Immunol. 2004;26:25–34.
- Neuhaus S., Bruendler P., Frey C.F., Gottstein B., Doherr M.G., Gerber V.. Increased parasite resistance and recurrent airway obstruction in horses of a high-prevalence family. J. Vet. Intern. Med. 2010;24:407–413.
- Lanz S., Gerber V., Marti E., Rettmer H., Klukowska-Rötzler J., Gottstein B., Matthews J.B., Pirie S., Hamza E.. Effect of hay dust extract and cyathostomin antigen stimulation on cytokine expression by PBMC in horses with recurrent airway obstruction. Vet. Immunol. Immunopathol. 2013;155:229–237.
- von Mutius E.. Allergies, infections and the hygiene hypothesis–The epidemiological evidence. Immunobiology 2007;212:433–439.
- Smits H.H., Hartgers F.C., Yazdanbakhsh M.. Helminth infections: Protection from atopic disorders. Curr. Allergy Asthma Rep. 2005;5:42–50.
- Marti E., Ehrensperger F., Burger D., Ousey J., Day M.J., Wilson A.D.. Maternal transfer of IgE and subsequent development of IgE responses in the horse (Equus callabus). Vet. Immunol. Immunopathol. 2009;127:203–211.
- Smits H.H., Everts B., Hartgers F.C., Yazdanbakhsh M.. Chronic helminth infections protect against allergic diseases by active regulatory processes. Curr. Allergy Asthma Rep. 2010;10:3–12.
- Ianiro G., Iorio A., Porcari S., Masucci L., Sanguinetti M., Perno C.F., Gasbarrini A., Putignani L., Cammarota G.. How the gut parasitome affects human health. Therap. Adv. Gastroenterol. 2022;15:1524.
- Bründler P., Frey C.F., Gottstein B., Nussbaumer P., Neuhaus S., Gerber V.. Lower shedding of strongylid eggs by Warmblood horses with recurrent airway obstruction compared to unrelated healthy horses. Vet. J. 2011;190:e12–e15.
- Thienpont D., Rochette F., Vanparijs O.F.J.. Diagnosing Helminthiasis by Coprological Examination. Janssen; Beerse, Belgium: 2003.
- Carvalho L.M.M., Gomes L., Cernea M., Cernea C., Santos C.A., Bernardes N., Rosário M.A., Soares M.J., Fazendeiro I.. Gastrointestinal parasites and its control in stabled donkeys and mules. Rev. Port. Ciências Vet. 2007;102:225–231.
- Madeira de Carvalho L.M., Cernea M.S., Martins S., Sousa S., Gersão S., Cernea L.C.. Comparative study of cyathostomin horse infection in Portugal and Romania based in L3 subpopulations of Cyathostomum sensu latum. Sci. Parasitol. 2008;2:48–56.
- Marti E., Gerber V., Wilson A.D., Lavoie J.P., Horohov D., Crameri R., Lunn D.P., Antczak D., Björnsdóttir S., Björnsdóttir T.S.. Report of the 3rd Havemeyer workshop on allergic diseases of the Horse, Hólar, Iceland, June 2007. Vet. Immunol. Immunopathol. 2008;126:351–361.
- Jost U., Klukowska-Rötzler J., Dolf G., Swinburne J.E., Ramseyer A., Bugno M., Burger D., Blott S., Gerber V.. A region on equine chromosome 13 is linked to recurrent airway obstruction in horses. Equine Vet. J. 2007;39:236–241.
- Swinburne J.E., Bogle H., Klukowska-Rötzler J., Drögemüller M., Leeb T., Temperton E., Dolf G., Gerber V.. A whole-genome scan for recurrent airway obstruction in Warmblood sport horses indicates two positional candidate regions. Mamm. Genome. 2009;20:504–515.
- Simões J., Batista M., Tilley P.. The Immune Mechanisms of Severe Equine Asthma—Current Understanding and What Is Missing. Animals 2022;12:744.
- Deaton C.M., Deaton L., Jose-Cunilleras E., Vincent T.L., Baird A.W., Dacre K., Marlin D.J.. Early onset airway obstruction in response to organic dust in the horse. J. Appl. Physiol. 2007;102:1071–1077.
- Klei T.R., Chapman M.R.. Immunity in equine cyathostome infections. Vet. Parasitol. 1999;85:123–136.
- Stancampiano L., Usai F., Marigo A., Rinnovati R.. Are small strongyles (Cyathostominae) involved in horse colic occurrence?. Vet. Parasitol. 2017;247:33–36.
- Lawson A.L., Malalana F., Mair T.S.. Larval cyathostominosis: Clinicopathological data and treatment outcomes of 38 hospitalised horses (2009–2020). Equine Vet. Educ. 2023;35:424–435.
- Platts-Mills T.A.E., Erwin E., Heymann P., Woodfolk J.. Is the hygiene hypothesis still a viable explanation for the increased prevalence of asthma?. Allergy Eur. J. Allergy Clin. Immunol. Suppl. 2005;60:25–31.
- Liu A.H.. Revisiting the hygiene hypothesis for allergy and asthma. J. Allergy Clin. Immunol. 2015;136:860–865.
- Yazdanbakhsh M., Kremsner P.G., Van Ree R.. Immunology: Allergy, parasites, and the hygiene hypothesis. Science 2002;296:490–494.
- Piazzesi A., Putignani L.. Impact of helminth–microbiome interactions on childhood health and development—A clinical perspective. Parasite Immunol. 2023;45:e12949.
- Mpairwe H., Webb E.L., Muhangi L., Ndibazza J., Akishule D., Nampijja M., Ngom-wegi S., Tumusime J., Jones F.M., Fitzsimmons C.. Anthelminthic treatment during pregnancy is associated with increased risk of infantile eczema: Randomised-controlled trial results. Pediatr. Allergy Immunol. 2011;22:305–312.
- Straubinger K., Paul S., Prazeres Da Costa O., Ritter M., Buch T., Busch D.H., Layland L.E., Prazeres Da Costa C.U.. Maternal immune response to helminth infection during pregnancy determines offspring susceptibility to allergic airway inflammation. J. Allergy Clin. Immunol. 2014;134:1271–1279.e10.
- Klukowska-Rötzler J., Swinburne J.E., Drögemüller C., Dolf G., Janda J., Leeb T., Gerber V.. The interleukin 4 receptor gene and its role in recurrent airway obstruction in Swiss Warmblood horses. Anim. Genet. 2012;43:450–453.
- Ober C., Leavitt S.A., Tsalenko A., Howard T.D., Hoki D.M., Daniel R., Newman D.L., Wu X., Parry R., Lester L.A.. Variation in the interleukin 4-receptor α gene confers susceptibility to asthma and atopy in ethnically diverse populations. Am. J. Hum. Genet. 2000;66:517–526.
- Youn J., Hwang S.H., Cho C.S., Min J.K., Kim W.U., Park S.H., Kim H.Y.. Association of the interleukin-4 receptor α variant Q576R with Th1/Th2 imbalance in connective tissue disease. Immunogenetics 2000;51:743–746.
- Kaplan R.M., Nielsen M.K.. An evidence-based approach to equine parasite control: It ain’t the 60s anymore. Equine Vet. Educ. 2010;22:306–316.
- Kaplan R.M., Vidyashankar A.N.. An inconvenient truth: Global worming and anthelmintic resistance. Vet. Parasitol. 2012;186:70–78.
- Sousa S.R., Anastácio S., Nóvoa M., Paz-Silva A., de Carvalho L.M.M.. Gastrointestinal parasitism in miranda donkeys: Epidemiology and selective control of strongyles infection in the northeast of Portugal. Animals 2021;11:155.
- Hotchkiss J.W., Reid S.W.J., Christley R.M.. 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;39:301–308.
- Boelow H., Krücken J., von Samson-Himmelstjerna G.. Epidemiological study on factors influencing the occurrence of helminth eggs in horses in Germany based on sent-in diagnostic samples. Parasitol. Res. 2023;122:749–767.
- Relf V.E., Morgan E.R., Hodgkinson J.E., Matthews J.B.. Helminth egg excretion with regard to age, gender and management practices on UK Thoroughbred studs. Parasitology 2013;140:641–652.
- Elghryani N., McOwan T., Mincher C., Duggan V., de Waal T.. Estimating the Prevalence and Factors Affecting the Shedding of Helminth Eggs in Irish Equine Populations. Animals 2023;13:581.
- Martins A.V., Corrêa L.L., Ribeiro M.S., Lobão L.F., Dib L.V., Palmer J.P.S., de Moura L.C., Knackfuss F.B., Uchôa C.M.A., Molento M.B.. Prevalence, Risk Factors and Diagnosis of Helminths in Thoroughbred Horses Kept at Training Centers in Rio de Janeiro, Brazil. J. Equine Vet. Sci. 2023;127:104536.
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