Selective Anthelmintic Treatment at Different Physiological Stages in Hair Sheep Under Humid Tropical Conditions
Abstract
Ewes’ genotype and physiological stage are important factors associated with gastrointestinal nematode infection. The aims were to evaluate the parasitic (fecal eggs count, FEC), health (anemia level, FAMACHA; packed cell volume, PCV; hemoglobin, HGB), and productive response (live weight, LW; body condition score, BCS) of hair ewes managed under a selective deworming program with levamisole (7.5 mg/kg of live weight) at reproductive stages (not pregnant, NPW, n=17; ewes between the first and second third of gestation, 1-3PW, n=22; ewes in the last third of gestation and peripartum, 4-5PWN, n=16) and genotype groups (Pelibuey, PB, n=12; Katahdin, KT, n=12; Pelibuey × Katahdin, F1 PB×KT, n=16; and Pelibuey × Dorper F1 PB×DP, n=15). The effects of treatments were studied using analysis of variance, considering the reproductive stages and genotypes as treatments through 4 evaluation periods (days 20, 48, 76, and 104). FEC values were higher (p<0.01) for ewes at 4-5PW than 1-3PW and NPW. FAMACHA, PCV, LW, and BCS were similar in ewes regardless of the reproductive stage. On day 48 post-deworming (levamisole at 7.5 mg/kg of LW), the proportion of ewes with >800 e/g was higher (13.74%) at 4-5PW than at the peripartum stage. On day 76, the accumulated proportion of ewes that were dewormed was higher (p<0.05) at 4-5PW than at the peripartum stage. The accumulated total proportion revealed that the genotype F1 PB×DP ewes had the highest deworming requirement (p<0.05), being dewormed at least once (32.8%). According to the indicators of LW, BCS, FAMACHA, FEC, PCV, HGB, and proportion of dewormed animals, ewes with the F1 PB×KT genotype showed the best performance. Therefore, reproductive stage-orientated management and the use of the best genotype for grazing conditions combined with a selective deworming program can contribute significantly to the control of gastrointestinal nematodes.
References
Aguirre-Serrano, A. M., Ojeda-Robertos, N. F., González-Garduño, R., Peralta-Torres, J. A., Luna-Palomera, C., & Torres-Acosta, J. D. J. (2020). Influence of litter size at birth and weaning on the proportion of Pelibuey ewes treated with an anthelmintic in a targeted selective scheme in the hot humid tropics. Small Ruminant Research, 184, 106049. https://doi.org/10.1016/j.smallrumres.2020.106049
Al-Jbory, W. A. H., & Al-Samarai, F. R. (2016). Some hematological reference values estimated by the reference values advisor in the Iraqi Awassi sheep. Comparative Clinical Pathology, 25, 1155-1162. https://doi.org/10.1007/s00580-016-2320-3
Aleuy, O. A., Serrano, E., Ruckstuhl, K. E., Hoberg, E. P., & Kutz, S. (2020). Parasite intensity drives fetal development and sex allocation in a wild ungulate. Scientific Reports, 10, 1–10. https://doi.org/10.1038/s41598-020-72376-x
Arece-García, J., López-Leyva, Y., González-Garduño, R., & Torres-Hernández, G. (2014). Evaluation of strategic and selective anthelmintic treatments on Pelibuey ewes in Cuba. Revista Colombiana de Ciencias Pecuarias, 27, 273–281. https://doi.org/10.17533/udea.rccp.324901
Atiba, E. M., Zewei, S., & Qingzhen, Z. (2020). Influence of metabolizable protein and minerals supplementation on detrimental effects of endoparasitic nematodes infection in small ruminants. Tropical Animal Health and Production, 52, 2213-2219. https://doi.org/10.1007/s11250-020-02275-w
Beasley, A. M., Kahn, L. P., & Windon, R. G. (2012). The influence of reproductive physiology and nutrient supply on the periparturient relaxation of immunity to the gastrointestinal nematode Trichostrongylus colubriformis in Merino ewes. Veterinary Parasitology, 188, 306–324. https://doi.org/10.1016/j.vetpar.2012.03.022
Calvete, C., González, J. M., Ferrer, L. M., Ramos, J. J., Lacasta, D., Delgado, I., & Uriarte, J. (2020). Assessment of targeted selective treatment criteria to control subclinical gastrointestinal nematode infections on sheep farms Veterinary Parasitology, 277, 109018. https://doi.org/10.1016/j.vetpar.2019.109018
Cunha, S. M. F., Willoughby, O., Schenkel, F., & Cánovas, Á. (2024). Genetic parameter estimation and selection for resistance to gastrointestinal nematode parasites in sheep—A Review. Animals, 14(4), 613. https://doi.org/10.3390/ani14040613
Claerebout, E., De Wilde, N., Van Mael, E., Casaert, S., Velde, F. V., Roeber, F., & Geldhof, P. (2020). Anthelmintic resistance and common worm control practices in sheep farms in Flanders, Belgium Veterinary. Parasitology: Regional Studies and Reports, 100393. https://doi.org/10.1016/j.vprsr.2020.100393
CONAGUA. (2021). Servicio Meteorológico Nacional. Normales climatológicas. https://smn.conagua.gob.mx/es/climatologia/informacion-climatologica/normales-climatologicas-por-estado
Cringoli, G., Rinaldi, L., Veneziano, V., Capelli, G., & Scala, A. (2004). The influence of flotation solution, sample dilution and the choice of McMaster slide area (volume) on the reliability of the McMaster technique in estimating the faecal egg counts of gastrointestinal strongyles and Dicrocoelium dendriticum in sheep. Veterinary Parasitology, 123, 121–131. https://doi.org/10.1016/j.vetpar.2004.05.021
David, C. M. G., Costa, R. L. D., Parren, G. A. E., Rua, M. A. S., Nordi, E. C. P., Paz, C. C. P., Quirino, C. R., Figueiredo, R. S., & Bohland, E. (2020). Hematological, parasitological and biochemical parameters in sheep during the peripartum period. Revista Colombiana De Ciencias Pecuarias, 33(2), 81–95. https://doi.org/10.17533/udea.rccp.v33n1a04
Dey, A. R., Begum, N., Anisuzzaman, Alim, M. A., & Alam, M. Z. (2020). Multiple anthelmintic resistance in gastrointestinal nematodes of small ruminants. Bangladesh Parasitology International, 77, 102105. https://doi.org/10.1016/j.parint.2020.102105
Ferreira, J., Sotomaior, C. S., Bezerra, A. C. D., da Silva, W. E., Leite, J. H. G. M., de Sousa, J. E. R., Viz, de F. F. B. J., & Façanha, D. A. E. (2019). Sensitivity and specificity of the FAMACHA© system in tropical hair sheep. Tropical Animal Health and Production, 51, 1767–1771. https://doi.org/10.1007/s11250-019-01861-x
Gasparina, J. M., Fonseca, L., Loddi, M. M., de Souza Martins, A., & da Rocha, R. A. (2019). Resistance of ewes to gastrointestinal nematode infections during the peripartum and dry periods and the performance of their lambs. Revista Brasileira de Saude e Producao Animal, 20, 1–11. https://doi.org/10.1590/S1519-9940200282019
González-Garduño, R., Arece-García, J., & Torres-Hernández, G. (2021). Physiological, immunological and genetic factors in the resistance and susceptibility to gastrointestinal nematodes of sheep in the peripartum period: A review. Helminthologia (Poland), 58, 134–151. https://doi.org/10.2478/helm-2021-0020
González-Garduño, R., Mendoza-de Gives, P., López-Arellano, M. E., Aguilar-Marcelino, L., Torres-Hernández, G., Ojeda-Robertos, N. F., & Torres-Acosta, J. F. J. (2018). Influence of the physiological stage of Blackbelly sheep on immunological behaviour against gastrointestinal nematodes. Experimental Parasitology, 193, 20–26. https://doi.org/10.1016/j.exppara.2018.08.003
González-Garduño, R., Torres-Acosta, J. F. J., & Chay-Canul, A. J. (2014). Susceptibility of hair sheep ewes to nematode parasitism during pregnancy and lactation in a selective anthelmintic treatment scheme under tropical conditions. Research in Veterinary Science, 96, 487–492. https://doi.org/10.1016/j.rvsc.2014.03.001
Sieuchand, S., Charles, R., Caruth, J., Basu, A., von Samson‐Himmelstjerna, G., & Georges, K. (2020). A field study on the occurrence of gastrointestinal nematodes in sheep over the wet and dry seasons in two West Indian Islands. Transboundary and Emerging Diseases, 67, 193-200. https://doi.org/10.1111/tbed.13521
Hinojosa-Cuéllar, J. A., Oliva-Hernández, J., Torres-Hernández, G., Segura-Correa, J. C. & R. González-Garduño. (2015). Productividad de ovejas F1 Pelibuey x Blackbelly y sus cruces con Dorper y Katahdin en un sistema de producción del trópico húmedo de Tabasco, México. Archivos de Medicina Veterinaria, 47, 167–174. https://doi.org/10.4067/S0301-732X2015000200007
Hodgkinson, J. E., Kaplan, R. M., Kenyon, F., Morgan, E. R., Park, A. W., Paterson, S., Babayan, S. A., Beesley, N. J., Britton, C., Chaudhry, U., Doyle, S. R., Ezenwa, V. O., Fenton, A., Howell, S. B., Laing, R., Mable, B. K., Matthews, L., McIntyre, J., Milne, C. E., Morrison, T. A., Prentice, J. C., Sargison, N. D., Williams, D. J. L., Wolstenholme, A. J., & Devaney, E. (2019). Refugia and anthelmintic resistance: Concepts and challenges. International Journal for Parasitology: Drugs and Drug Resistance, 10, 51–57. https://doi.org/10.1016/j.ijpddr.2019.05.001
Ilangopathy, M., Palavesam, A., Amaresan, S., & Muthusamy, R. (2019). Economic Impact of Gastrointestinal Nematodes in Sheep on Meat Production. International Journal of Livestock Research, 9, 44-48. https://doi.org/10.5455/ijlr.20190331051814
Kuma, B., Abebe, R., Mekbib, B., Sheferaw, D., & Abera, M. (2019). Prevalence and intensity of gastrointestinal nematodes infection in sheep and goats in semi-intensively managed farm, South Ethiopia. Journal of Veterinary Medicine and Animal Health, 11(1), 1-5. https://doi.org/10.5897/JVMAH2018.0705
Leask, R., van Wyk, J. A., Thompson, P. N., & Bath, G. F. (2013). The effect of application of the FAMACHA© system on selected production parameters in sheep. Small Ruminant Research, 110, 1–8. https://doi.org/10.1016/j.smallrumres.2012.07.026
Liddell, C., Morgan, E. R., Bull, K., & Ioannou, C. C. (2020). Response to resources and parasites depends on health status in extensively grazed sheep. Proceedings of the Royal Society B: Biological Sciences, 287 (1920), 20192905. https://doi.org/10.1098/rspb.2019.2905
López-Leyva, Y., González-Garduño, R., Cruz-Tamayo, A. A., Arece-García, J., Huerta-Bravo, M., Ramírez-Valverde, R., Torres-Hernández, G., & López-Arellano, M. E. (2022). Protein supplementation as a nutritional strategy to reduce gastrointestinal nematodiasis in periparturient and lactating pelibuey ewes in a tropical environment. Pathogens, 11(8), 941. https://doi.org/10.3390/pathogens11080941
Luna-Palomera, C., Santamaría-Mayo, E., Berúmen-Alatorre, A., Gómez-Vázquez, A., & Maldonado- García, N. M. (2010). Suplementación energética y proteica en el control de nematodos gastrointestinales en corderas de pelo. Redvet, 11(7),1-13. https://www.redalyc.org/pdf/636/63614251006.pdf
Notter, D. R., Burke, J. M., Miller, J. E., & Morgan, J. L. M. (2017). Factors affecting fecal egg counts in periparturient Katahdin ewes and their lambs. Journal of Animal Science, 95, 103–112. https://doi.org/10.2527/jas.2016.0955
NRC (National Research Council). (2007). Nutrient requirements of small rumanints: sheep, goats, cervids, and new world camelids. National Academy Press.
Palomo-Couoh, J. G., Aguilar-Caballero, A. J., Torres-Acosta, J. F. J., & González-Garduño, R. (2017). Comparing the phenotypic susceptibility of Pelibuey and Katahdin female lambs against natural gastrointestinal nematode infections under hot humid tropical conditions. Parasitology Research, 116, 1627–1636. https://doi.org/10.1007/s00436-017-5437-7
Pereira, F. C., Longo, C., Castilho, C., Leme, D. P., Seugling, J., Bassetto, C. C., Amarante, A. F. T., & Bricarello, P. A. (2020). Peripartum phenomenon in crioula lanada sheep susceptible and resistant to gastrointestinal nematodes. Frontiers in Veterinary Science, 7, 1–8. https://doi.org/10.1007/s00436-017-5437-7
Ramírez-Rojas, M. del C., Dzib-Can, A. F., Hinojosa-Cuéllar, J. A., González-Garduño, R., Miranda-Jiménez, L., Suárez-Espinosa, J., & Torres-Hernández, G. (2022). Función zootécnica de una población de ovinos Blackbelly en Campeche, México, basada en índices morfométricos. Revista MVZ Cordoba, 27(s), e2850-e2850. https://doi.org/10.21897/rmvz.2850
Romero-Escobedo, E., Torres-Hernández, G., Becerril-Pérez, C. M., Alarcón-Zúñiga, B., Apodaca-Sarabia, C. A., & Díaz-Rivera, P. (2018). A comparison of criollo and suffolk ewes for resistance to haemonchus contortus during the periparturient period. Journal of Applied Animal Research, 46, 17–23. https://doi.org/10.1080/09712119.2016.1252378
Russel, A. (1991). Body condition scoring of sheep. In Practice, 6, 91–94. https://doi.org/10.1136/inpract.6.3.91
Santiago-Figueroa, I., Lara-Bueno, A., González-Garduño, R., López-Arellano, M. E., Rosa-Arana, J. L. de la, & Maldonado-Simán, E. de J. (2019). Anthelmintic resistance in hair sheep farms in a sub-humid tropical climate, in the Huasteca Potosina, Mexico. Veterinary Parasitology: Regional Studies and Reports, 17, 100292. https://doi.org/10.1016/j.vprsr.2019.100292
SAS. (2017). SAS/STAT User´s Guide, Release 6. S. Inst. (ed). SAS Institute.
Sepúlveda-Vázquez, J., Lara-Del Rio, M. J., Vargas-Magaña, J. J., Quintal-Franco, J. A., Alcaraz-Romero, R. A., Ojeda-Chi, M. M., Rodríguez-Vivas, R. I., Mancilla-Montelongo, G., González-Pech, P. G., & Torres-Acosta, J. F. de J. (2021). Frequency of sheep farms with anthelmintic resistant gastrointestinal nematodes in the Mexican Yucatán peninsula. Veterinary Parasitology: Regional Studies and Reports, 24, 1–7. https://doi.org/10.1016/j.vprsr.2021.100549
Sotomaior, C. S., Rosalinski-Moraes, F., da Costa, A. R. B., Maia, D., Monteiro, A. L. G., & van Wyk, J. A. (2012). Sensitivity and specificity of the FAMACHA© system in Suffolk sheep and crossbred Boer goats. Veterinary Parasitology, 190, 114–119. https://doi.org/10.1016/j.vetpar.2012.06.006
Soto-Barrientos, N., Chan-Pérez, J. I., España-España, E., Novelo-Chi, L. K., Palma-Ávila, I., Ceballos-Mendoza, A. C., Sarabia-Hernández, J. A., Santos-Ricalde, R. H., Cámara-Sarmiento, R., & J. F. J. Torres-Acosta. (2018). Comparing body condition score and FAMACHA© to identify hair-sheep ewes with high faecal egg counts of gastrointestinal nematodes in farms under hot tropical conditions. Small Ruminant Research, 167, 92-99. https://doi.org/10.1016/j.smallrumres.2018.08.011
Tariq, K. A. (2015). A review of the epidemiology and control of gastrointestinal nematode infections of small ruminants. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 85, 693-703. https://doi.org/10.1007/s40011-014-0385-9
Torres-Acosta, J. F. J., Pérez-Cruz, M., Canul-Ku, H. L., Soto-Barrientos, N., Cámara-Sarmiento, R., Aguilar-Caballero, A. J., Lozano-Argáes, I., Le-Bigot, C., & Hoste, H. (2014). Building a combined targeted selective treatment scheme against gastrointestinal nematodes in tropical goats. Small Ruminant Research, 121, 27–35. https://doi.org/10.1016/j.smallrumres.2014.01.009
Torres-Chable, O. M., García-Herrera, R. A., González-Garduño, R., Ojeda-Robertos, N. F., Peralta-Torres, J. A., & Chay-Canul, A. J. (2020). Relationships among body condition score, FAMACHA© score and haematological parameters in Pelibuey ewes. Tropical Animal Health and Production, 52, 3403–3408. https://doi.org/10.1007/s11250-020-02373-9
Thorne, J. W. (2023). Characterizing gastrointestinal nematode infection in dorper and rambouillet sheep through genetic analyses (Doctoral dissertation, University of Idaho). https://www.proquest.com/openview/01a76f241bd43b0235b594657cdfbdce/1?pq-origsite=gscholar&cbl=18750&diss=y
Vásquez Hernández, M., González Garduño, R., Torres Hernández, G., Mendoza de Gives, P., & Ruíz Rodríguez, J. M. (2006). Comparison of two grazing systems in the infestation with gastrointestinal nematodes of hair sheep. Veterinaria México, 37, 15–27. https://www.cabidigitallibrary.org/doi/full/10.5555/20063204500
Westers, T., Jones-Bitton, A., Menzies, P., VanLeeuwen, J., Poljak, Z., & Peregrine, A. S. (2017). Comparison of targeted selective and whole flock treatment of periparturient ewes for controlling Haemonchus sp. on sheep farms in Ontario, Canada. Small Ruminant Research, 150, 102–110. https://doi.org/10.1016/j.smallrumres.2017.03.013
Weaver, A. R. (2017). Evaluation of terminal sire breeds for hair sheep production systems (Doctoral dissertation, Virginia Tech). https://vtechworks.lib.vt.edu/items/2fcb1167-559d-4fe1-962f-b31ad5e058d7
Williams, E. G., Davis, C. N., Williams, M., Jones, D. L., Cutress, D., Williams, H. W., Brophy, P. M., Rose, M.T., Stuart, R. B., & Jones, R. A. (2022). Associations between gastrointestinal nematode infection burden and lying behaviour as measured by accelerometers in periparturient ewes. Animals, 12, 1–9. https://doi.org/10.3390/ani12182393
Williams, E. G., Davis, C. N., Williams, M., Jones, D. L., Cutress, D., Williams, H. W., Brophy, P. M., Rose, M. T., Stuart, R. B., & Jones, R. A. (2022). Associations between gastrointestinal nematode infection burden and lying behaviour as measured by accelerometers in periparturient ewes. Animals, 12(18), 2393. https://doi.org/10.3390/ani12182393
Williams, E. G., Brophy, P. M., Williams, H. W., Davies, N., & Jones, R. A. (2021). Gastrointestinal nematode control practices in ewes: Identification of factors associated with application of control methods known to influence anthelmintic resistance development. Veterinary Parasitology: Regional Studies and Reports, 24, 100562. https://doi.org/10.1016/j.vprsr.2021.100562
Williams, E. G. (2023). Design and development of a targeted selective treatment (TST) strategy for gastrointestinal nematodes (GIN) in ewes. (Doctoral dissertation, Aberystwyth University). https://pure.aber.ac.uk/ws/portalfiles/portal/85179805/Williams_Eiry.pdf
Zaragoza-Vera, C.V., González-Garduño, R., Flores-Santiago, E. del J., Chay-Canul, A. J., Zaragoza-Vera, M., Arjona-Jiménez, G., & Torres-Chablé, O. M. (2022). Hematological changes during pregnancy and lactation in Pelibuey ewes infected with gastrointestinal nematodes. Comparative Clinical Pathology, 31, 827–838. https://doi.org/10.1007/s00580-022-03386-6
Zaragoza-Vera, C. V., Aguilar-Caballero, A. J., González-Garduño, R., Arjona-Jiménez, G., Zaragoza-Vera, M., Torres-Acosta, J. F. J., Medina-Reynés, J. U., & Berumen-Alatorre, A. C. (2019). Variation in phenotypic resistance to gastrointestinal nematodes in hair sheep in the humid tropics of Mexico. Parasitology Research, 118, 567-573. https://doi.org/10.1007/s00436-018-06201-w
Zvinorova, P. I., Halimani, T. E., Muchadeyi, F. C., Matika, O., Riggio, V., & Dzama, K. (2016). Breeding for resistance to gastrointestinal nematodes–The potential in low-input/output small ruminant production systems. Veterinary parasitology, 225, 19-28. https://doi.org/10.1016/j.vetpar.2016.05.015
Authors
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Authors submitting manuscripts should understand and agree that copyright of manuscripts of the article shall be assigned/transferred to Tropical Animal Science Journal. The statement to release the copyright to Tropical Animal Science Journal is stated in Form A. This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License (CC BY-SA) where Authors and Readers can copy and redistribute the material in any medium or format, as well as remix, transform, and build upon the material for any purpose, but they must give appropriate credit (cite to the article or content), provide a link to the license, and indicate if changes were made. If you remix, transform, or build upon the material, you must distribute your contributions under the same license as the original.
Article Details
