Health evaluation of donkeys: parasite control methods and a model for challenge infections

Authors

DOI:

https://doi.org/10.11606/issn.1678-4456.bjvras.2021.174275

Keywords:

Equids, Parasite infections, Milk production, Welfare, Brazil

Abstract

Donkeys, mules, and asses are domestic animals of worldwide distribution, found in all regions of Brazil. Although more health data is needed from these species, some sectors of today’s society are exploring alternatives to use these animals for milk production and the use of donkeys in social events and onotherapy. Donkeys (Equus asinus) are used in many everyday activities, but the animals need better welfare conditions. Although it is well known that endoparasite infections (i.e. cyathostomins, Strongylus spp., Parascaris sp.) can harm the clinical condition of the animals, there are limited clinical and laboratory supporting data, including registered therapeutic drugs for their control. The objective of the present work was to review the existing literature about parasite infections of donkeys, including their clinical implications, and the drug efficacy test to help practitioners improve their health management programs. To assist with that, we have developed a questionnaire to identify the risk factors of donkey farming, which is presented here in English and in Portuguese. Lastly, the present article also includes an original simulation using the susceptible-infected-recovered (SIR) model with low, moderate, and severe scenarios to help visualize the risk of parasite infections. The SIR model was based on the disease condition of donkeys in Brazil, using transient interaction levels from 0.0015 to 0.0025, infectivity levels from 0.10 to 0.40, and distinct recovery rates (R) from 0.01 to 0.08. As milk production is an expanding new activity worldwide, we want to emphasize that the first comprehensive studies must take into account differences in animal age, breed, and body condition score, local climate, pasture quality, day of sampling, and the period of lactation within the lactation curve to measure the health condition of donkeys. These data are considered important and will then be correlated to the parasite egg/oocyst (EPG or OoPG) counts in the feces using coproparasitological protocols (McMaster and Mini-FLOTAC), and even DNA-based techniques, to establish a novel data bank for donkeys. Target selective treatment has been proposed to be used as a routine in horses and will also be implemented in donkeys. This technique aims to reduce the number of anthelmintic treatments and, consequently, lessen parasite selection for resistance. The dynamic variations found by the SIR model are discussed in the text and should be taken into account when deciding the best health management implementation and parasite control programs. We think that more studies are needed to evaluate the basic physiological performance of donkeys in tropical areas to better understand their thermal adaptation, assuming that the animals are kept under acceptable clinical, nutritional, and housing conditions to express their resilient behavior. Cases of neglect and ill-treatment of animals must also be studied in infected conditions as well as their negative impacts. These strategies reinforce the concept of holistic farming with the possibility to improve specific informations, thereby improving the welfare of the donkeys.

Downloads

Download data is not yet available.

References

ABCJPêga. [Internet]. Associação Brasileira de Criadores de Jumento Pegâ: Projeto Social. 2020. [cited 2020 Oct 15]. Available from: https://abcjpega.org.br/servico/projeto-social/.

Animal Welfare Indicators - AWIN. Welfare assessment protocol for donkeys. Rome; 2015. https://doi.org/10.13130/AWIN_donkeys_2015.

Antunes JMAP, Allendorf SD, Appolinário CM, Peres MG, Perotta JH, Neves TB, Deconto I, Barros IR Fo, Biondo AW, Megid J. Serology for Brucella abortus in cart horses from an urban area in Brazil. Braz Arch Vet Med Animal Sci. 2013;65(2):619-21. https://doi.org/10.1590/S0102-09352013000200044.

Araújo AL, Souza GAF, Nóbrega PI No, Souza AP. Tranquilization of donkeys using acepromazine or acepromazine/diazepam. Arq Bras Med Vet Zootec. 2014;66(1):109-15. https://doi.org/10.1590/S0102-09352014000100016.

Aspri M, Souroullas K, Ioannou C, Papademas P. Physico-chemical composition and antimicrobial protein content of early lactation donkey milk. Int J Food Stud. 2019;8(1):68-75. https://doi.org/10.7455/ijfs/8.1.2019.a6.

Attia MM, Khalifa MM, Atwa MT. The prevalence and intensity of external and internal parasites in working donkeys (Equus asinus) in Egypt. Vet World. 2018;11(9):1298-306. https://doi.org/10.14202/vetworld.2018.1298-1306. PMid:30410237.

Ayo JO, Dzenda T, Olaifa F, Ake SA, Sani I. Diurnal and seasonal fluctuations in rectal temperature, respiration and heart rate of pack donkeys in a tropical savannah zone. J Equine Sci. 2014;25(1):1-6. https://doi.org/10.1294/jes.25.1. PMid:24834007.

Becher AM, Mahling M, Nielsen MK, Pfister K. Selective anthelmintic therapy of horses in the Federal states of Bavaria (Germany) and Salzburg (Austria): an investigation into strongyle egg shedding consistency. Vet Parasitol. 2010;171(1-2):116-22. https://doi.org/10.1016/j.vetpar.2010.03.001. PMid:20356680.

Bevilaqua CML, Rodrigues ML, Concordet D. Identification of infective larvae of some common nematode strongylids of horses. Rev. Med. Vet. 1993;144:989-95.

Bordonaro S, Dimauro C, Criscione A, Marletta D, Macciotta NPP. The mathematical modeling of the lactation curve for dairy traits of the donkey (Equus asinus). J Dairy Sci. 2013;96(6):4005-14. https://doi.org/10.3168/jds.2012-6180. PMid:23587386.

Borioni N, Marinaro P, Celestini S, Del Sole F, Magro R, Zoppi D, Mattei F, Dall’Armi V, Mazzarella F, Cesario A, Bonassi S. Effect of equestrian therapy and onotherapy in physical and psycho-social performances of adults with intellectual disability: a preliminary study of evaluation tools based on the ICF classification. Disabil Rehabil. 2012;34(4):279-87. https://doi.org/10.3109/09638288.2011.605919. PMid:21988646.

Canever RJ, Braga PRC, Boeckh A, Grycajuck M, Bier D, Molento MB. Lack of Cyathostomin sp. reduction after anthelmintic treatment in horses in Brazil. Vet Parasitol. 2013;194(1):9-39. https://doi.org/10.1016/j.vetpar.2012.12.020. PMid:23318166.

Carroccio A, Cavataio F, Montalto G, D’Amico D, Alabrese L, Iacono G. Intolerance to hydrolysed cow’s milk proteins in infants: clinical characteristics and dietary treatment. Clin Exp Allergy. 2000;30(11):1597-603. https://doi.org/10.1046/j.1365-2222.2000.00925.x. PMid:11069569.

Castro LL, Abrahao C, Buzatti A, Molento MB, Bastianetto E, Rodrigues DS, Lopes L, Silva MX, Freitas MG, Conde MH, Borges FA. Comparison of McMaster and Mini-FLOTAC fecal egg counting techniques in cattle and horses. Vet Parasitol Reg Stud Rep. 2017;10(1):132-5. https://doi.org/10.1016/j.vprsr.2017.10.003. PMid:31014585.

Colditz IG, Hine BC. Resilience in farm animals: biology, management, breeding and implications for animal welfare. Anim Prod Sci. 2016;56(1):1961-83. https://doi.org/10.1071/AN15297.

Coles GC, Jackson F, Pomroy WE, Prichard RK, von Samson-Himmelstjerna G, Silvestre A, Taylor MA, Vercruysse J. The detection of anthelmintic resistance in nematodes of veterinary importance. Vet Parasitol. 2006;136(3-4):167-85. https://doi.org/10.1016/j.vetpar.2005.11.019. PMid:16427201.

Costa PWL, Feitosa TF, Vilela VLR. Parasitic profile of traction equids in the semi-arid climate of Paraíba State, Northeastern, Brazil. Rev Bras Parasitol Vet. 2018;27(2):218-22. https://doi.org/10.1590/s1984-296120180035. PMid:29846453.

Dai F, Dalla Costa E, Burden F, Judge A, Minero M. The development of guidelines to improve dairy donkey management and welfare. Ital J Anim Sci. 2019;18(1):189-93. https://doi.org/10.1080/1828051X.2018.1503571.

Dai F, Segati G, Costa ED, Burden F, Judge A, Minero M. Management practices and milk production in dairy donkey farms distributed over the Italian territory. Maced Vet Rev. 2017;40(2):131-6. https://doi.org/10.1515/macvetrev-2017-0016.

Disassa H, Alebachew A, Zenebe T, Kebede G. Prevalence of strongyle infection in horses and donkeys in and around Dangila Town, Northwest Ethiopia. Acta Parasitol Global. 2015;6(1):14-9. https://doi.org/10.5829/idosi.apg.2015.6.1.9159.

Elsheikha H. How can vets alleviate anthelmintic resistance in donkeys? [Internet]. Veterinary Practice; Swindon, England; 2019 Aug 1 [cited 2020 Nov 02]. Available from: https://veterinary-practice.com/article/how-can-vets-alleviate-anthelmintic-resistance-in-donkeys

Fantuz F, Ferraro S, Todini L, Piloni R, Mariani P, Salimei E. Donkey milk concentration of calcium, phosphorus, potassium, sodium and magnesium. Int Dairy J. 2012;24(2):143-5. https://doi.org/10.1016/j.idairyj.2011.10.013.

Ferreira GMS, Dutra FAF, Amorim EF Fo, Santos ACG. Gastrointestinal parasitism and hematology in horses and donkeys from the urban área of São Luis, MA, Northeast Brazil. Arch Vet Sci. 2014;19(2):22-30.

Gianfaldoni C, Barlozzari G, Mancini S, Di Domenico E, Maestrini M, Perrucci S. Parasitological investigation in an organic dairy donkey farm. Large Anim Rev. 2020;26(1):25-30.

Gokbulut C, Aksit D, Smaldone G, Mariani U, Veneziano V. Plasma pharmacokinetics, faecal excretion and efficacy of pyrantel pamoate paste and granule formulations following per os administration in donkeys naturally infected with intestinal strongylidae. Vet Parasitol. 2014;205(1-2):186-92. https://doi.org/10.1016/j.vetpar.2014.06.026. PMid:25015542.

Grosenbaugh DA, Reinemeyer CR, Figueiredo MD. Pharmacology and therapeutics in donkeys. Equine Vet Educ. 2011;23(1):523-30. https://doi.org/10.1111/j.2042-3292.2011.00291.x.

Heesterbeek JAP, Roberts MG. Threshold quantities for helminth infections. J Math Biol. 1995;33(4):415-34. https://doi.org/10.1007/BF00176380. PMid:7714416.

Holmes AD, Elman AFSP, Smith CT, Kuzmeski JW. Composition of mares’ milk as compared with that of other species. J Dairy Sci. 1947;30(6):385-95. https://doi.org/10.3168/jds.S0022-0302(47)92363-1.

Imam SMA, Seri HI, Hassan T, Tigani TA, Zolain HB, Abakar AD. Therapeutic efficacy evaluation of anthelmintic activity of albendazole and ivermectin drench formulations in donkeys in Darfur, Sudan. Vet Arh. 2010;80(1):585-95.

Instituto Brasileiro de Geografia e Estatística - IBGE. Sistema IBGE de recuperação automática – SIDRA. Pesquisa da pecuária municipal: acesso online às notícias, publicações, tabelas, bancos de dados e mapas: tabela 73 [Internet]. Brasília; 2012 [cited 2020 Aug 21]. Available from: https://sidra.ibge.gov.br/Tabela/73#resultado

Ishii JB, Arenal A, Felix A, Yoshitani U, Beech R, Molento MB. Diagnosis of resistance alleles in codon 167 of the beta-tubulin (Cya-tbb-1) gene from third-stage larvae of horse cyathostomins. Res Vet Sci. 2017;115(1):92-5. https://doi.org/10.1016/j.rvsc.2017.01.019. PMid:28199900.

Karatosidi D, Marsico G, Tarricone S. Modern use of donkeys. Iran J Appl Anim Sci. 2013;3(1):13-7.

Lichtenfels JR, Kharchenko VA, Dvojnos GM. Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) of horses, zebras and asses (Equidae). Vet Parasitol. 2008;156(1-2):4-161. https://doi.org/10.1016/j.vetpar.2008.04.026. PMid:18603375.

Love S, Murphy D, Mellor D. Pathogenicity of cyathostome infection. Vet Parasitol. 1999;85(2-3):113-22. https://doi.org/10.1016/S0304-4017(99)00092-8. PMid:10485358.

Love S. Parasite-associated gastrointestinal disease. In: Mair T, Divers T, Ducharme N, editors. Manual of equine gastroenterology. 1st ed. London: WB Saunders Company; 2002. p. 53-60. https://doi.org/10.1016/B978-0-7020-2486-3.50007-0.

Maestrini M, Molento MB, Mancini S, Martini M, Angeletti FGS, Perrucci S. Intestinal strongyle genera in diferente typology of donkey farms in Tuscany, Central Italy. Vet Sci. 2020;7(4):195-204. https://doi.org/10.3390/vetsci7040195. PMid:33276602.

Mansueto P, Iacono G, Taormina G, Seidita A, D’Alcamo A, Adragna F, Randazzo G, Carta M, Rini G, Carroccio A. Ass’s milk in allergy to cow’s milk protein: a review. Acta Med Mediter. 2013;29(1):153-60.

Matthews JB, Burden FA. Common helminth infections of donkeys and their control in temperate regions. Equine Vet Educ. 2013;25(9):461-7. https://doi.org/10.1111/eve.12018.

Molento MB, Antunes J, Novak-Bentes R, Coles GC. Anthelmintic resistant nematodes in Brazilian horses. Vet Rec. 2008;162(12):384-5. https://doi.org/10.1136/vr.162.12.384. PMid:18359933.

Molento MB, Dutra LH, Pritsch IC, Garbin VP, Pereira AM, Gavião A, Gabriel AL, de Sousa RS, Viana JGA. Fasciola hepatica infection in cattle and the use of simulation models for endemic areas. J Helminthol. 2020;94(1):e185. https://doi.org/10.1017/S0022149X2000067X. PMid:32907641.

Molento MB. Parasite control in the age of drug resistance and changing agricultural practices. Vet Parasitol. 2009;163(3):229-34. https://doi.org/10.1016/j.vetpar.2009.06.007. PMid:19560869.

Molento MB. Parasite resistance on helminths of equids and management proposal’s. Cienc Rural. 2005;35(6):1469-77. https://doi.org/10.1590/S0103-84782005000600041.

Naderi Y. Appropriate mathematical models to describe the lactation curves of milk production traits of Iranian Holstein dairy cattle. Acta Sci Anim Sci. 2018;40(1):e37895. https://doi.org/10.4025/actascianimsci.v40i1.37895.

Ogbourne CP, Duncan JL. Strongylus vulgaris in the horse: its biology and veterinary importance. A review. 2nd ed. Slough: Commonwealth Agricultural Bureaux; 1985.

Oryan A, Kish GF, Rajabloo M. Larval cyathostominosis in a working donkey. J Parasit Dis. 2015;39(2):324-7. https://doi.org/10.1007/s12639-013-0313-6. PMid:26064028.

Paiva ALC, Ferreira J, Nunes TL, Mouta AN, Fernandes NS, Cavalcante JM, Barrêto RA Jr, Paula VV. Northeast Brazilian donkeys have little physiological responses influenced by tropical conditions. Biol Rhythm Res. 2019;1(1):1-11. https://doi.org/10.1080/09291016.2019.1629219.

Papini RA, Orsetti C, Sgorbini M. A controlled study on efficacy and egg reappearance period of ivermectin in donkeys naturally infected with small strongyles. Helminthologia. 2020;57(2):163-70. https://doi.org/10.2478/helm-2020-0017. PMid:32518493.

Passantino A. Welfare issues of donkey (Equus asinus): a checklist based on the five freedoms. J Verbrauch Lebensm. 2011;6(2):215-6. https://doi.org/10.1007/s00003-010-0638-3.

Paz CFR, Paganela JC, Oliveira DP, Feijó LS, Nogueira CEW. Biometric standard of traction horses in Pelotas, state of Rio Grande do Sul. Ciênc Anim. 2013;14(2):159-63. https://doi.org/10.5216/cab.v14i2.13078.

Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter? Vet Parasitol. 2014;201(1-2):1-8. https://doi.org/10.1016/j.vetpar.2014.01.004. PMid:24485565.

Ragona G, Corrias F, Benedetti M, Paladini I, Salari F, Altomonte I, Martini M. Amiata donkey milk chain: animal health evaluation and milk. Ital J Food Saf. 2016;5(3):5951. https://doi.org/10.4081/ijfs.2016.5951. PMid:27853717.

Rangel AHN, Galvão JGB Jr, Simplício AA, Freire RMB, Novaes LP. Aspectos composicionais e nutricionais do leite de jumenta: uma revisão. Rev Inst Laticínios Cândido Tostes. 2015;70(3):160-71. https://doi.org/10.14295/2238-6416.v70i3.395.

Santos DW, Madeira de Carvalho LM, Molento MB. Identification of third stage larval types of cyathostomins of equids: an improved perspective. Vet Parasitol. 2018;260(1):49-52. https://doi.org/10.1016/j.vetpar.2018.08.007. PMid:30197013.

Svendsen ED. The professional handbook of the donkey. 3rd ed. London: Whittet Books; 2000.

Tavassoli M, Arjmand Yamchi J, Hajipour N. A survey on the prevalence of strongyles species in working donkeys in North-West of Iran. J Parasit Dis. 2016;40(4):1210-2. https://doi.org/10.1007/s12639-015-0651-7. PMid:27876916.

Trawford AF, Tremlett JG. Efficacy of triclabendazole against Fasciola hepatica in the donkey (Equus asinus). Vet Rec. 1996;139(6):142-3. https://doi.org/10.1136/vr.139.6.142. PMid:8863404.

Upjohn MM, Pfeiffer DU, Verheyen KL. Helping working Equidae and their owners in developing countries: monitoring and evaluation of evidence-based interventions. Vet J. 2014;199(2):210-6. https://doi.org/10.1016/j.tvjl.2013.09.065. PMid:24269105.

Valle E, Raspa F, Giribaldi M, Barbero R, Bergagna S, Antoniazzi S, McLean AK, Minero M, Cavallarin L. Afunctional approach to the body condition assessment of lactating donkeys as a tool for welfare evaluation. PeerJ. 2017;5:e3001. https://doi.org/10.7717/peerj.3001. PMid:28367363.

Vercruysse J, Claerebout E. Treatment vs non-treatment of helminth infections in cattle: defining the threshold. Vet Parasitol. 2001;98(1-3):195-214. https://doi.org/10.1016/S0304-4017(01)00431-9. PMid:11516586.

Vynnycky E, White R. Introduction to infectious disease modelling. 1st ed. Oxford: Oxford University Press; 2010.

Wise D. [Internet]. Donkey Therapy Italy - For people who love donkeys. 2020.[cited 2020 Dec 18]. Available from: https://donkeywise.org/donkey-therapy/italy/.

Downloads

Published

2021-04-01

How to Cite

1.
Molento MB, Vilela VLR. Health evaluation of donkeys: parasite control methods and a model for challenge infections. Braz. J. Vet. Res. Anim. Sci. [Internet]. 2021 Apr. 1 [cited 2024 Apr. 24];58:e174275. Available from: https://www.revistas.usp.br/bjvras/article/view/174275