Parascaris spp. eggs in horses of Italy: a large-scale epidemiological analysis of the egg excretion and conditioning factors.
Ascariosis
Epidemiological survey
Horses
Italy
Parascaris
Treatments
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
08 May 2021
08 May 2021
Historique:
received:
01
01
2021
accepted:
26
04
2021
entrez:
9
5
2021
pubmed:
10
5
2021
medline:
9
10
2021
Statut:
epublish
Résumé
Equine ascariosis, caused by Parascaris spp., is a worldwide endoparasitic disease affecting young horses in particular. Despite the great number of horses reared in Italy, large-scale epidemiological surveys dealing with ascariosis prevalence in the country are not reported in the current literature. For this reason, the present survey aims to describe, for the first time, the spread and infestation of Parascaris spp. in a large population of Italian horses (6896 animals) using faecal egg counts, and further to identify risk factors associated with ascarid egg shedding. Individual rectal faecal samples collected during routine veterinary examinations were used and Parascaris spp. prevalence was tested against the animal's age, sex, housing conditions, geographic provenance as well as the respective sampling season. Among the examined stables, 35.8% showed at least one horse to be positive for Parascaris spp. eggs and an overall prevalence of 6.3% was found. Ascariosis rates tended to decrease significantly with age and, proportionally, 80.0% of the recorded Parascaris spp. eggs were found in 0.7% of the examined animals. Statistically significant differences among prevalence rates were found between the different geographic areas of provenance and prevalence was found to be higher in horses reared outdoors compared to those raised indoors. Analysis of data based on sex and season did not show any significant differences. Despite the lower prevalence found compared to other European countries, ascariosis was concluded to represent a significant health challenge for horses reared in Italy, especially foals. Age (foals and yearlings) and outdoor rearing were identified to be significant risk factors for Parascaris spp. egg shedding. Furthermore, the relevance of the infected horses over 6 years of age should not be underestimated as these represent a significant source of contamination for younger animals. The development of improved treatment protocols based on regular faecal examination combined with follow-up assessment of the efficacy of integrated action plans would prove beneficial in regard to animal health and anthelmintic resistance reduction in the field.
Sections du résumé
BACKGROUND
BACKGROUND
Equine ascariosis, caused by Parascaris spp., is a worldwide endoparasitic disease affecting young horses in particular. Despite the great number of horses reared in Italy, large-scale epidemiological surveys dealing with ascariosis prevalence in the country are not reported in the current literature. For this reason, the present survey aims to describe, for the first time, the spread and infestation of Parascaris spp. in a large population of Italian horses (6896 animals) using faecal egg counts, and further to identify risk factors associated with ascarid egg shedding.
METHODS
METHODS
Individual rectal faecal samples collected during routine veterinary examinations were used and Parascaris spp. prevalence was tested against the animal's age, sex, housing conditions, geographic provenance as well as the respective sampling season.
RESULTS
RESULTS
Among the examined stables, 35.8% showed at least one horse to be positive for Parascaris spp. eggs and an overall prevalence of 6.3% was found. Ascariosis rates tended to decrease significantly with age and, proportionally, 80.0% of the recorded Parascaris spp. eggs were found in 0.7% of the examined animals. Statistically significant differences among prevalence rates were found between the different geographic areas of provenance and prevalence was found to be higher in horses reared outdoors compared to those raised indoors. Analysis of data based on sex and season did not show any significant differences. Despite the lower prevalence found compared to other European countries, ascariosis was concluded to represent a significant health challenge for horses reared in Italy, especially foals. Age (foals and yearlings) and outdoor rearing were identified to be significant risk factors for Parascaris spp. egg shedding. Furthermore, the relevance of the infected horses over 6 years of age should not be underestimated as these represent a significant source of contamination for younger animals.
CONCLUSIONS
CONCLUSIONS
The development of improved treatment protocols based on regular faecal examination combined with follow-up assessment of the efficacy of integrated action plans would prove beneficial in regard to animal health and anthelmintic resistance reduction in the field.
Identifiants
pubmed: 33964977
doi: 10.1186/s13071-021-04747-w
pii: 10.1186/s13071-021-04747-w
pmc: PMC8106216
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
246Références
Armstrong SK, Woodgate RG, Gough S, Heller J, Sangster NC, Hughes KJ. The efficacy of ivermectin, pyrantel and fenbendazole against Parascaris equorum infection in foals on farms in Australia. Vet Parasitol. 2014;205:575–80.
pubmed: 25224788
Hautala K, Näreaho A, Kauppinen O, Nielsen MK, Sukura A, Rajala-Schultz PJ. Risk factors for equine intestinal parasite infections and reduced efficacy of pyrantel embonate against Parascaris sp. Vet Parasitol. 2019;273:52–9.
pubmed: 31442894
Laugier C, Sevin C, Menard S, Maillard K. Prevalence of Parascaris equorum infection in foals on French stud farms and first report of ivermectin-resistant P. equorum populations in France. Vet Parasitol. 2012;188:185–9.
pubmed: 22494940
Lyons ET, Tolliver SC. Strongyloides westeri and Parascaris equorum: observations in field studies in thoroughbred foals on some farms in Central Kentucky, USA. Helminthologia. 2014;51:7–12.
Clayton HM, Duncan JL. Clinical signs associated with Parascaris equorum infection in worm-free pony foals and yearlings. Vet Parasitol. 1978;4:69–78.
Cribb NC, Cote NM, Boure LP, Peregrine AS. Acute small intestinal obstruction associated with Parascaris equorum infection in young horses: 25 cases (1985–2004). N Z Vet J. 2006;54:338–43.
pubmed: 17151735
Nielsen MK. Evidence-based considerations for control of Parascaris spp. infections in horses. Equine Vet Educ. 2016;28:224–31.
Jabbar A, Littlewood DTJ, Mohandas N, Briscoe AG, Foster PG, Muller F, et al. The mitochondrial genome of Parascaris univalens - implications for a “forgotten” parasite. Parasit Vectors. 2014;7:428.
pubmed: 25190631
pmcid: 4262126
Nielsen MK, Wang J, Davis R, Bellaw JL, Lyons ET, Lear TL, et al. Parascaris univalens - a victim of large-scale misidentification? Parasitol Res. 2014;113:4485–90.
pubmed: 25231078
Martin F, Hoglund J, Bergstrom TF, Lindsjö OK, Tydén E. Resistance to pyrantel embonate and efficacy of fenbendazole in Parascaris univalens on Swedish stud farms. Vet Parasitol. 2018;264:69–73.
pubmed: 30503095
Goday C, Pimpinelli S. Cytological analysis of chromosomes in the two species Parascaris univalens and P. equorum. Chromosoma. 1986;94:1–10.
Gao JF, Zhang XX, Wang XX, Li Q, Li Y, Xu WW, Gao Y, Wang CR. According to mitochondrial DNA evidence, Parascaris equorum and Parascaris univalens may represent the same species. J Helminthol. 2019;93(3):383–8.
pubmed: 29792237
Reinemeyer CR, Nielsen MK. Control of helminth parasites in juvenile horses. Equine Vet Educ. 2017;29(4):225–32.
Lyons ET, Drudge JH, Tolliver SC. Studies on the development and chemotherapy of larvae of Parascaris equorum (Nematoda: Ascaridoidea) in experimentally and naturally infected foals. J Parasitol. 1976;62(3):453–9.
pubmed: 945338
Fabiani JV, Lyons ET, Nielsen MK. Dynamics of Parascaris and Strongylus spp. parasites in untreated juvenile horses. Vet Parasitol. 2016;230:62–6.
pubmed: 27884444
Anderson RC. Nematode parasites of vertebrates: their development and transmission. Wallingford, Oxon, UK: CABI Publish; 2000.
Di Pietro JA, Todd KS. Chemotherapeutic treatment of larvae and migratory stages of Parascaris equorum. In: Proc. 34th Ann. Conv. Am. Assoc. Equine Prac., San Diego, CA. 1988:611–618.
Austin SM, Foreman JH, Todd KS, Di Pietro JA, Baker GJ. Parascaris equorum infections in horses. Compendium Equine. 1990;12:1110–9.
Clayton HM. Ascarids. Recent advances. Vet Clin North Am Equine Pract. 1986;2(2):313–28.
pubmed: 3527375
Ihler CF. The distribution of Parascaris equorum eggs in the soil profile of bare paddocks in some Norwegian studs. Vet Res Commun. 1995;19:495–501.
pubmed: 8619288
Robert M, Hu W, Nielsen MK, Stowe CJ. Attitude towards implementation of surveillance-based parasite control on Kentucky Thoroughbred farms–current strategies, awareness, and willingness-to-pay. Equine Vet J. 2015;47:694–700.
pubmed: 25196091
Veronesi F, Moretta I, Moretti A, Fioretti DP, Genchi C. Field effectiveness of pyrantel and failure of Parascaris equorum egg count reduction following ivermectin treatment in Italian horse farms. Vet Parasitol. 2009;161:138–41.
pubmed: 19201100
Boersema JH, Eysker M, Nas JW. Apparent resistance of Parascaris equorum to macrocyclic lactones. Vet Rec. 2002;150:279–81.
pubmed: 11924584
Reinemeyer CR. Diagnosis and control of anthelmintic-resistant Parascaris equorum. Parasit Vectors. 2009;2(Suppl. 2):S8.
pubmed: 19778469
pmcid: 2751844
Cooper LG, Caffe G, Cerutti J, Nielsen MK, Anziani OS. Reduced efficacy of ivermectin and moxidectin against Parascaris spp. in foals from Argentina. Vet Parasitol Reg Stud Reports. 2020;20:100388.
pubmed: 32448542
Lyons ET, Tolliver SC, Kuzmina TA, Collins SS. Further evaluation in field tests of the activity of three anthelmintics (fenbendazole, oxibendazole and pyrantel pamoate) against the ascarid Parascaris equorum in horse foals on eight farms in Central Kentucky (2009–2010). Parasitol Res. 2011;109:1193–7.
pubmed: 21499750
Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter? Vet Parasitol. 2014;201:1–8.
pubmed: 24485565
Papini RA, Micol De Bernart F, Sgorbini M. A Questionnaire Survey on Intestinal Worm Control Practices in Horses in Italy. J Equine Vet Sci. 2015;35:70–5.
Veronesi F, Fioretti DP, Genchi C. Are macrocyclic lactones useful drugs for the treatment of Parascaris equorum infections in foals? Vet Parasitol. 2010;172(1–2):164–7.
pubmed: 20471177
Scala A, Tamponi C, Sanna G, Predieri G, Dessì G, Sedda G, et al. Gastrointestinal strongyles egg excretion in relation to age, gender, and management of horses in Italy. Animals. 2020;10(12):2283.
pmcid: 7761647
Raynaud JP. Etude de l’efficacité d’une technique de coproscopie quantitative our le diagnostic de routine et le controle des infestations parasitaires des bovins, ovins, equines et porcins. Ann Parasitol. 1970;45:321–42.
Aromaa M, Hautala K, Oksanen A, Sukura A, Näreaho A. Parasite infections and the risk factors in foals and young horses in Finland. Vet Parasitol Reg Stud Reports. 2018;12:35–8.
pubmed: 31014805
Relf VE, Morgan ER, Hodgkinson JE, Matthews JB. Helminth egg excretion with regard to age, gender and management practices on UK Thoroughbred studs. Parasitology. 2013;140:641–52.
pubmed: 23351718
Lyons ET, Tolliver SC. Prevalence of parasite eggs (Strongyloides westeri, Parascaris equorum, and strongyles) and oocysts (Emeria leuckarti) in the feces of Thoroughbred foals on 14 farms in central Kentucky in 2003. Parasitol Res. 2004;92:400–4.
pubmed: 14760526
Mezgebu T, Tafess K, Tamiru F. Prevalence of gastrointestinal parasites of horses and donkeys in and around Gondar Town, Ethiopia. Open J Vet Med. 2013;3(06):267.
Imani-Baran A, Abdollahi J, Akbari H, Raafat A. Coprological prevalence and the intensity of gastrointestinal nematodes infection in working equines, east Azerbaijan of Iran. J Anim Plant Sci. 2019;29(5):1269–78.
Othman R, Alzuheir I. Prevalence of Parascaris equorum in native horses in West Bank Palestine. Iraqi J Vet Sci. 2019;33(2):433–6.
Salas-Romero J, Gómez-Cabrera KA, Aguilera-Valle LA, Bertot JA, Salas JE, Arenal A, et al. Helminth egg excretion in horses kept under tropical conditions—Prevalence, distribution and risk factors. Vet Parasitol. 2017;243:256–9.
pubmed: 28807303
Rehbein S, Visser M, Winter R. Prevalence, intensity and seasonality of gastrointestinal parasites in abattoir horses in Germany. Parasitol Res. 2013;112:407–13.
pubmed: 23052780
Aboling S, Drotleff AM, Cappai MG, Kamphues J. Contamination with ergot bodies (Claviceps purpurea sensu lato) of two horse pastures in Northern Germany. Mycotoxin Res. 2016;32:207–19.
pubmed: 27495979
Nielsen MK, Mittel L, Grice A, Erskine M, Graves E, Vaala W, et al. AAEP Parasite Control Guidelines. Online at American Association of Equine Practitioners. 2019. https://aaep.org/sites/default/files/Documents/InternalParasiteGuidelinesFinal5.23.19.pdf?fbclid=IwAR1VXsGa19jmLjM5Vwn-3w3tBX-2Ndz-xGdxty0SV-Qv-jUGtMqOgh6Bvrs . Accessed 14 Dec 2020.
Bucknell D, Gasser R, Beveridge I. The prevalence and epidemiology of gastrointestinal parasites of horses in Victoria. Australia Int J Parasitol. 1995;25:711–24.
pubmed: 7657457
Mfitilodze MW, Hutchinson GW. Prevalence and intensity of non-strongyle intestinal parasites of horses in northern Queensland. Aust Vet J. 1989;66:23–6.
pubmed: 2930389
Donoghue EM, Lyons ET, Bellaw JL, Nielsen MK. Biphasic appearance of corticated and decorticated ascarid egg shedding in untreated horse foals. Vet Parasitol. 2015;214:114–7.
pubmed: 26391818
ISPRA, Istituto Superiore per la Protezione e la Ricerca Ambientale. Gli indicatori del Clima in Italia nel. 2015. 2016;5:49.
ISPRA, Istituto Superiore per la Protezione e la Ricerca Ambientale. Gli indicatori del Clima in Italia nel 2016. 2017;3:26.
Nielsen MK, Baptiste KE, Tolliver SC, Collins SS, Lyons ET. Analysis of multiyear studies in horses in Kentucky to ascertain whether counts of eggs and larvae per gram of feces are reliable indicators of numbers of strongyles and ascarids present. Vet Parasitol. 2010;174:77–84.
pubmed: 20850927
Matthews J, Lester H. Control of equine nematodes: making the most of faecal egg counts. Practice. 2015;37(10):540–4.
Anazi ADA, Alyousif MS. Prevalence of non-strongyle gastrointestinal parasites of horses in Riyadh region of Saudi Arabia. Saudi J Biol Sci. 2011;18:299–303.
pubmed: 23961139
Yadav KS, Shukla PC, Gupta DK, Mishra A. Prevalence of gastrointestinal nematodes in horses of Jabalpur region. Res J Vet Pract. 2014;2:44–8.
Singh G, Soodan J, Singla L, Khajuria J. Epidemiological studies on gastrointestinal helminths in horses and mules. Vet Pract. 2012;13:23–7.
Kornaś S, Skalska M, Nowosad B, Gawor J, Labaziewicz I, Babiuch A. Occurrence of tapeworm, roundworm and botfly larvae in horses from southern Poland. Med Wet. 2007;63:1373–6.