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Gastrointestinal Helminths in Horses in Serbia and Various Factors Affecting the Prevalence

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Abstract

Purpose

Data on gastrointestinal infections in horses in Southeastern Europe are limited; thus, this study aimed to add to the existing knowledge on this topic by reporting on the prevalence of intestinal parasites of horses in the territory of the Republic of Serbia.

Methods

In the period from April 2017 to December 2018, parasitological examination of 548 samples from horses of different breed, age and sex from four regions and 18 districts of the country was performed. Coprological diagnostic was done by using qualitative methods without concentration and qualitative methods with concentration of parasitic elements. Quantification of the obtained results was performed using semi-qualitative faecal egg count.

Results

Four helminthoses were detected in the examined samples: P. equorum (8.57%), O. equi (3.65%), strongylid eggs (71.17%) and Anoplocephala spp. (0.91%). The total prevalence of helminthoses was 77.19%. Monoinfections were significantly more present 70.07% compared to coinfections (7.12%). The highest prevalence of helminthoses was detected in free-ranging horses (93.10%—27/29), in autumn 86.67% (117/135) and winter 79.71% (165/207), in Šumadija and West Serbia region (100%), and in the youngest category (100%). Significant difference (p < 0.001) was detected in the prevalence of monoinfections by strongylids and O. equi and also coinfections by strongylid/P. equorum between horses of different age categories.

Conclusion

Obtained results are of great contribution to clinical parasitology and pathology, especially from the aspect of animal health, welfare and preservation of horse population.

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References

  1. Đermanović V, Mitrović S, Novaković M, Đorđević N, Ivanov S, Topolac M (2010) Kvalitativna svojstva kopitara gajenih u Centralnoj Srbiji. Zbornik radova XXIV Savetovanja Agronoma, Veterinara i Tehnologa 16:179–188 (UDK:167.7:63)

    Google Scholar 

  2. Mitrović S, Životić V, Ilić P (2004) Stanje i privredni značaj konjarstva u nas. Zbornik naučnih radova 10:95–100

    Google Scholar 

  3. Mitrović S, Đermanović V, Đorđević N, Novaković M, Grubić G (2008) Fenotipska varijabilnost i povezanost telesnih mera posavskog konja gajenog u području Istočne Srbije. Biotechnol Anim Husb 24:253–260 (UDK:636.12+616.007.7)

    Google Scholar 

  4. Ivanov S (2007) Indigenous breeds conservation efforts in the Stara Planina Mt. area. Conference on Native breeds and varieties as part of natural and cultural heritage. Book of Abstracts, Šibenik. pp 113–114.

  5. Kaplan RM, Vidyashankar AN (2012) An inconvenient truth: global worming and anthelmintic resistance. Vet Parasitol 186:70–78. https://doi.org/10.1016/j.vetpar.2011.11.048

    Article  PubMed  Google Scholar 

  6. Dunn AM (1978) Veterinary helminthology, 2nd edn. Butler and Tanner, London

    Google Scholar 

  7. Proudman C, Matthews J (2000) Control of intestinal parasites in horses. Clin Pract 22:90–97. https://doi.org/10.1136/inpract.22.2.90

    Article  Google Scholar 

  8. Herd RP, Gabel AA (1990) Reduced efficacy of anthelmintics in young compared with adult horses. Equine Vet J 22:164–169

    Article  CAS  PubMed  Google Scholar 

  9. ESCCAP Guideline 08 (2019) A Guide to the treatment and control of equine gastrointestinal parasite infections, second edn. Worcestershire, United Kingdom, pp 22–24. ISBN: 978-1-907259-75-3

  10. Ilić T, Dimitrijević S (2005) Helmintoze digestivnog trakta domaćih životinja u nekim delovima Srbije. Vet Glasnik 59:419–425. https://doi.org/10.2298/VETGL0504419I

    Article  Google Scholar 

  11. Božić B, Košak K, Trailović I, Mijatović B, Pavlović I, Trailović D (2016) Prevalenca endoparazita kod balkanskih magaraca u Srbiji. Zbornik radova petog i šestog regionalnog savetovanja, Uzgoj, reprodukcija i zdravstvena zaštita konja“, Beograd, Srbija, str. pp 129–131.

  12. Tarić E, Drašković V, Al-Daghistani V, Tivković S, Pavlović I, Trailović D (2016) Biodiverzitet endoparazita kod domaćih brdskih konja u poluslobodnom sistemu držanja na pašnjacima. Zbornik radova petog i šestog regionalnog savetovanja „Uzgoj, reprodukcija i zdravstvena zaštita konja“, Beograd, Srbija, str. pp 126–128.

  13. Trailović D (2019a) Održivi uzgoj konja i magaraca u planinskim uslovima –tradicionalna i organska proizvodnja. U: Katić V, Trailović R, Tošić A, Trailović D, Organska proizvodnja i zdravstvena zaštita životinja u planinskom stočarstvu, Vrelo, Srbija, str. pp 77–87.

  14. Trailović D (2019b) Najĉešće bolesti životinja u organskom stoĉarstvu. U: Katić V, Trailović R, Tošić A, Trailović D, Organska proizvodnja i zdravstvena zaštita životinja u planinskom stočarstvu, Vrelo, Srbija, str. pp 91–95.

  15. Trailović D, Đoković S, Marković L, Ivanov S (2019) Aktuelna patologija autohtonih rasa konja i magaraca na Staroj planini. Drugi Simpozijum “Zaštita agrobiodiverziteta i očuvanje autohtonih rasa domaćih životinja”, Zbornik radova, Jun 28–30, Dimitrovgrad, Srbija, str. pp 165–173.

  16. Undersander D, Albert B, Cosgrove D, Jonson D, Peterson P (2002) Pastures for profit: a guide to rotational grazing (A3529). Cooperative Extension Publishing University of Winskonsin Extension, Winskonsin., p 43

    Google Scholar 

  17. Republic Hydrometeorological Service of Serbia, Annual Bulletin for Serbia (2017) http://www.hidmet.gov.rs/podaci/meteorologija/latin/2017.pdf (Accessed 06 December 2020).

  18. Republic Hydrometeorological Service of Serbia. Annual Bulletin for Serbia (2018) http://www.hidmet.gov.rs/podaci/meteorologija/latin/2018.pdf (Accessed 06 December 2020).

  19. Euzeby J (1982) Experimental diagnosis of animal helminthiases (domestic animals−laboratory animals−primates), Informations techniques des services vétérinaires, ministère de l’agriculture. Pract Work Vet Helminthol. 2:364

    Google Scholar 

  20. Pittman SJ, Shepherd G, Thacker JB, Myers HG (2010) Modified technique for collecting and processing fecal material for diagnosing intestinal parasites in swine. J Swine Health Prod 18:249–252

    Google Scholar 

  21. Mehfooz A, Masood MZ, Yousaf A, Akhtar N, Zafar MA (2008) Prevalence and anthelmintic efficacy of abamectin against gastro-intestinal parasites in horses. Pakistan Vet J 28:76–78

    Google Scholar 

  22. Singh G, Soodan JS, Singla LD, Khajuria JK (2012) Epidemiological studies on gastrointestinal helminths in horses and mules. Vet Pract 13:23–27

    Google Scholar 

  23. Saeed K, Qadir Z, Ashraf K, Ahmad N (2010) Role of intrinsic and extrinsic epidemiological factors on strongylosis in horses. J Anim Plant Sci 20:277–280

    Google Scholar 

  24. Matto TN, Bharkad GP, Bhat SA (2015) Prevalence of gastrointestinal helminth parasite of equids from organized farms of Mumbai and Pune. J Parasit Dis 39:179–185. https://doi.org/10.1007/s12639-013-0315-4

    Article  CAS  PubMed  Google Scholar 

  25. YadavS K, Shukla PC, Gupta DK, Mishra A (2014) Prevalence of gastrointestinal nematodes in horses of Jabalpur region. Res J Vet Pract 2:44–48. https://doi.org/10.14737/journal.rjvp/2014/2.3.44.48

    Article  Google Scholar 

  26. Khan MR, Tunio TM, Hussain I (2020) A study on prevalence of gastro - intestinal parasites and their impact on haematological indices in horses stabled at government farm sargodha, Pakistan. J Agric Res 58:27–34

    Google Scholar 

  27. Umur Ş, Açici M (2009) Survey on helminth infections of equines in the Central Black Sea region, Turkey. Turk J Vet Anim Sci 33:373–378. https://doi.org/10.3906/vet-0712-6

    Article  Google Scholar 

  28. Nielsen MK, Vidyashankar AN, Olsen SN, Monrad J, Thamsborg SM (2012) Strongylus vulgaris associated with usage of selective therapy on Danish horse farms-is it reemerging? Vet Parasitol 189:260–266. https://doi.org/10.1016/j.vetpar.2012.04.039

    Article  CAS  PubMed  Google Scholar 

  29. Eydal M, Gunnarasson E (1994) Helminth infections in a group of Icelandic horses with little exposure to anthelmintics. Búvísindi Icel Agr Sci 8:85–91

    Google Scholar 

  30. Tydén E, Enemark HL, Franko MA, Höglund J, Osterman-Lind E (2019) Prevalence of Strongylus vulgaris in horses after ten years of prescription usage of anthelmintics in Sweden. Vet Parasitol 2:100013. https://doi.org/10.1016/j.vpoa.2019.100013

    Article  CAS  Google Scholar 

  31. Teixeira P, Fabricio W, Gustavo F, Breno CC, Willian GM et al (2014) Endoparasites of horses from the Formiga city, located in center-west region of the state of Minas Gerais, Brazil. Braz J Vet Parasitol Jaboticabal 23:534–538. https://doi.org/10.1590/S1984-29612014072

    Article  Google Scholar 

  32. Pihl TH, Nielsen MK, Olsen SN, Leifsson PS, Jacobsen S (2018) Nonstrangulating intestinal infarctions associated with Strongylus vulgaris: Clinical presentation and treatment outcome of 30 horses (2008–2016). Equine Vet J 50:474–480. https://doi.org/10.1111/evj.12779

    Article  CAS  PubMed  Google Scholar 

  33. Lyons ET, Drudge JH, Tolliver SC (2000) Larval cyathostomiasis. Vet Clin N Am Equine Pract 16:501–513. https://doi.org/10.1016/s0749-0739(17)30092-5

    Article  CAS  Google Scholar 

  34. Kazlauskas J (1958) Helminth fauna of horses in the Lithuanian SSSR. Acta Parasitol Litu 1:85–88 (In Russian)

    Google Scholar 

  35. Pecheur M, Detry-Pouplard M, Gerin G, Tinar R (1979) Les helminthes parasites du systeme digestif de poneys abattusen Belgique. Ann Med Vet 123:103–108

    Google Scholar 

  36. Gawor J (1995) The prevalence and abundance of internal parasites in working horses autopsied in Poland. Vet Parasitol 58:99–108. https://doi.org/10.1016/0304-4017(94)00698-c

    Article  CAS  PubMed  Google Scholar 

  37. Cirak VY, Hermosilla C, Bauer C (1996) Study on the gastrointestinal parasite fauna of ponies in northern Germany. Appl Parasitol 37:239–244

    CAS  PubMed  Google Scholar 

  38. Borgsteede FHM, van Beek G (1998) Parasites of stomach and small intestine of 70 horses slaughtered in the Netherlands. Vet Quart 20:31–34. https://doi.org/10.1080/01652176.1998.9694833

    Article  CAS  Google Scholar 

  39. Laugier C, Sevin C, Ménard S, Maillard K (2012) Prevalence of Parascaris equorum infection in foals on French stud farms and first report of ivermectin-resistant P. equorum populations in France. Vet Parasitol 188:185–189. https://doi.org/10.1016/j.vetpar.2012.02.022

    Article  PubMed  Google Scholar 

  40. Francisco I, Arias M, Cortiñas FJ et al (2009) Intrinsic factors influencing the infection by helminth parasites in horses under an oceanic climate area (NW Spain). J Parasitol Res. https://doi.org/10.1155/2009/616173

    Article  PubMed  PubMed Central  Google Scholar 

  41. Hinney B, Wirtherle NC, Kyule M, Miethe N, Zessin KH, Clausen PH (2011) Prevalence of helminths in horses in the state of Brandenburg, Germany. Parasitol Res 108:1083–1091. https://doi.org/10.1007/s00436-011-2362-z

    Article  PubMed  Google Scholar 

  42. Lyons ET, DrudgeJH STW, Crowe MW, Tolliver SC (1981) Prevalence of Strongylus vulgaris and Parascaris equorum in Kentucky thoroughbreds at necropsy. J Am Vet Med Assoc 179:818–819 (PMID: 7341597)

    CAS  PubMed  Google Scholar 

  43. Slivinska K, Kharchenko V, Wróblewski Z, Gawor J, Kuzmina T (2016) Parasitological survey of Polish primitive horses (Equus caballus gmelini Ant.): influence of age, sex and management strategies on the parasite community. Helminthol 53:233–242. https://doi.org/10.1515/helmin-2016-0023

    Article  CAS  Google Scholar 

  44. Sotiraki ST, Badouvas AG, Himonas CA (1997) A survey on the prevalence of intestinal parasites of equines in Macedonia and Thessalia-Greece. J Equine Vet Sci 17:550–552

    Article  Google Scholar 

  45. Upjohn MM, Shipton K, Lerotholi T, Attwood G, Verheyen KLP (2010) Coprological prevalence and intensity of helminth infection in working horses in Lesotho. Trop Anim Health Prod 42:1655–1661. https://doi.org/10.1007/s11250-010-9617-z

    Article  PubMed  Google Scholar 

  46. Getachew AM, Innocent T, Trawford AF, Feseha G, Reid SJW, Love S (2008) Equine parascarosis under the tropical weather conditions of Ethiopia: a coprological and postmortem study. Vet Rec 162:177–180. https://doi.org/10.4236/ojvm.2013.36043

    Article  CAS  PubMed  Google Scholar 

  47. Khan A, Khan MS, Muhammad A, Mahmood AK, Muhammad I (2010) Prevalence and chemotherapy of Parascaris equorum in equines in Pakistan. J Equine Vet Sci 30:155–158. https://doi.org/10.1016/j.jevs.2010.01.057

    Article  CAS  Google Scholar 

  48. Clayton HM, Duncan JL (1979) The development of immunity to Parascaris equorum infection in the foal. Res Vet Sci 26(3):383–384

    Article  CAS  PubMed  Google Scholar 

  49. Beasley AM, Kotze AC, Barnes T, Coleman GT (2020) Equine helminth prevalence and management practices on Australian properties as shown by coprological survey and written questionnaire. Anim Prod Sci 60(18):2131–2144. https://doi.org/10.1071/AN18378

    Article  Google Scholar 

  50. Clayton HM (1986) Ascarids. recent advances. Vet Clin N Am Equine 2:313–328. https://doi.org/10.1016/s0749-0739(17)30718-6

    Article  CAS  Google Scholar 

  51. Langrova I, Jankovska I, Borovsky M, Fiala T (2003) Effect of climatic influences on the migrations of infective larvae of Cyathostominae. Vet Med 48:18–24. https://doi.org/10.17221/5745-VETMED

    Article  Google Scholar 

  52. Meana A, Luzon M, Corchero J, Gómez-Bautista M (1998) Reliability of coprological diagnosis of Anoplocephala perfoliata infection. Vet Parasitol 74:79–83. https://doi.org/10.1016/S0304-4017(97)00145-3

    Article  CAS  PubMed  Google Scholar 

  53. Agneessens J, Debever P, Engelen S, Vercruysse J (1998) The prevalence of Anoplocephala perfoliata in horses in Belgium, and evaluation of a diagnostic sedimentation/flotation technique. Vlaams Diergeneeskd Tijdschr 67:27–31

    Google Scholar 

  54. Nielsen MK (2016) Equine tapeworm infections: disease, diagnosis, and control. Equine Vet Educ 28:388–395. https://doi.org/10.1111/eve.12394

    Article  Google Scholar 

  55. Pavone S, Veronesi F, Genchi C, Fioretti DP, Brianti E, Mandara MT (2011) Pathological changes caused by Anoplocephala perfoliata in the mucosa/submucosa and in the enteric nervous system of equine ileocecal junction. Vet Parasitol 176:43–52. https://doi.org/10.1016/j.vetpar.2010.10.041

    Article  PubMed  Google Scholar 

  56. Back H, Nyman A, Osterman Lind E (2013) The association between Anoplocephala perfoliata and colic in Swedish horses–a case control study. Vet Parasitol 197:580–585. https://doi.org/10.1016/j.vetpar.2013.07.020

    Article  CAS  PubMed  Google Scholar 

  57. Tomczuk K, Kostro K, Grzybek M, Szczepaniak K, Studzińska M, Demkowska-Kutrzepa M, Roczeń-Karczmarz M (2015) Seasonal changes of diagnostic potential in the detection of Anoplocephala perfoliata equine infections in the climate of Central Europe. Parasitol Res 114:767–772. https://doi.org/10.1007/s00436-014-4279-9

    Article  PubMed  Google Scholar 

  58. Borgsteede FHM, van Beek G (1996) Data on the prevalence of tape-worm infestations in horses in the Netherlands. Vet Quart 18:110–112. https://doi.org/10.1080/01652176.1996.9694629

    Article  CAS  Google Scholar 

  59. Hedberg-Alm Y, Penell J, Riihimäki M, Osterman-Lind E, Nielsen MK, Tydén E (2020) Parasite occurrence and parasite management in Swedish horses presenting with gastrointestinal disease—a case-control study. Animals. https://doi.org/10.3390/ani10040638

    Article  PubMed  PubMed Central  Google Scholar 

  60. Swann WJ (2006) Improving the welfare of working equine animals in developing countries. Appl Anim Behav Sci 100:148–151. https://doi.org/10.1016/j.applanim.2006.04.001

    Article  Google Scholar 

  61. Krecek RC, Waller PJ (2006) Towards the implementation of the “basket of options” approach to helminth parasite control of livestock: Emphasis on the tropics/subtropics. Vet Parasitol 139:270–282. https://doi.org/10.1016/j.vetpar.2006.04.018

    Article  PubMed  Google Scholar 

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Acknowledgements

The study was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Contract number 451–03-68/2022–14/200143).

Funding

Funding was provided by Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja, 451–03-68/2022–14/200143, Tamara Ilić.

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TI, PM, and SD conceived and designed the study. TI wrote the manuscript. TI, DB, BG, GP, ZK, and PM participated in collecting and analysing the samples. DB, SD, ZK, PM, BG, and KN critically revised the manuscript and made substantial contribution to interpretation of the data. KN performed the statistical analysis. All the authors performed a critical revision of the manuscript and gave final approval of the version to be published.

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Correspondence to Katarina Nenadović.

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Ilić, T., Bogunović, D., Nenadović, K. et al. Gastrointestinal Helminths in Horses in Serbia and Various Factors Affecting the Prevalence. Acta Parasit. 68, 56–69 (2023). https://doi.org/10.1007/s11686-022-00636-z

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