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Variation in phenotypic resistance to gastrointestinal nematodes in hair sheep in the humid tropics of Mexico

  • Immunology and Host-Parasite Interactions - Original Paper
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Abstract

The objective of the study was to evaluate phenotypic resistance against gastrointestinal nematodes in Blackbelly, Pelibuey and Katahdin ewes before pregnancy in the humid tropics of Mexico. Individual faecal and blood samples were taken in 59 Pelibuey, 69 Blackbelly and 73 Katahdin ewes. The egg count per gram of faeces (EPG) of gastrointestinal nematodes (GINs) was determined. The percentage of packed cell volume (PCV) and body condition score (BCS) of each animal were also recorded. The ewes were segregated as susceptible, intermediate or resistant based on the EPG using the quartile method. The data were analysed using the general linear method, and the means between breeds were compared by Tukey’s test. The relationships between the EPG, PCV and BCS were evaluated by Spearman correlation. The Katahdin ewes showed the highest EPG counts (3613.6 ± 5649) compared to the Blackbelly and Pelibuey ewes (576.1 ± 1009 and 56.8 ± 187, respectively, P < 0.01). The PCV values between breeds were similar (P > 0.05). The susceptible ewes had the highest EPG counts and the lowest PCV percentage (5069 ± 6404 and 22.8% ± 8.1% respectively) compared to the resistant ewes (P < 0.01). A higher percentage of Katahdin ewes were susceptible compared to the other breeds (P < 0.05). The main GIN species were Haemonchus contortus, Trichostrongylus colubriformis and Cooperia curticei. In conclusion, Katahdin ewes showed susceptibility to GIN compared to Blackbelly and Pelibuey ewes before the pregnancy period in the humid tropics of Mexico.

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References

  • Alba-Hurtado F, Muñoz-Guzmán MA (2013) Immune responses associated with resistance to haemonchosis in sheep. Biomed Res Int 2013:11

    Article  CAS  Google Scholar 

  • Asmare K, Sheferaw D, Aragaw K, Abera M, Sibhat B, Haile A, Kiara H, Szonyi B, Skjerve E, Wieland B (2016) Gastrointestinal nematode infection in small ruminants in Ethiopia: a systematic review and meta-analysis. Acta Trop 160:68–77

    Article  PubMed  Google Scholar 

  • Besier RB, Kahn LP, Sargison ND, Van Wyk JA (2016) The pathophysiology, ecology and epidemiology of Haemonchus contortus infection in small ruminants. Adv Parasitol 93:95–143

    Article  CAS  PubMed  Google Scholar 

  • Bishop SC (2012) Possibilities to breed for resistance to nematode parasite infections in small ruminants in tropical production systems. Animal 6:741–747

    Article  CAS  PubMed  Google Scholar 

  • Bishop SC, Jackson F, Coop RL, Stear MJ (2004) Genetic parameters for resistance to nematode infections in Texel lambs and their utility in breeding programmes. Anim Sci 78:185–194

    Article  Google Scholar 

  • Burke JM, Miller JE (2002) Relative resistance of Dorper crossbred ewes to gastrointestinal nematode infection compared with St. Croix and Katahdin ewes in the southeastern United States. Vet Parasitol 109:265–275

    Article  CAS  PubMed  Google Scholar 

  • Castillo JA, Medina RD, Villalobos JM, Gayosso-Vazquez A, Ulloa-Arvizu R, Rodriguez RA, Ramirez HP, Morales RA (2011) Association between major histocompatibility complex microsatellites, fecal egg count, blood packed cell volume and blood eosinophilia in Pelibuey sheep infected with Haemonchus contortus. Vet Parasitol 177:339–344

    Article  CAS  PubMed  Google Scholar 

  • CONAGUA (2017) Comisión Nacional del Agua. Servicio Meteorológico Nacional. México DF (México)

  • Cornelius MP, Jacobson C, Besier RB (2014) Body condition score as a selection tool for targeted selective treatment-based nematode control strategies in Merino ewes. Vet Parasitol 206:173–181

    Article  CAS  PubMed  Google Scholar 

  • Corticelli B, Lai M (1963) Studies of the technique of culture of infective larvae of gastrointestinal strongyles of cattle. Acta de Medicina Veterinaria, Napoli 9:347–357

    Google Scholar 

  • Encalada-Mena L, Tuyub-Solis H, Ramírez-Vargas G, Mendoza-de-Gives P, Aguilar-Marcelino L, López-Arellano ME (2014) Phenotypic and genotypic characterisation of Haemonchus spp. and other gastrointestinal nematodes resistant to benzimidazole in infected calves from the tropical regions of Campeche State, Mexico. Vet Parasitol 205:246–254

    Article  CAS  PubMed  Google Scholar 

  • Greer AW, Hamie JC (2016) Relative maturity and the development of immunity to gastrointestinal nematodes in sheep: an overlooked paradigm? Parasite Immunol 38:263–272

    Article  CAS  PubMed  Google Scholar 

  • Gruner L, Aumont G, Getachew T, Brunel JC, Pery C, Cognie Y, Guerin Y (2003) Experimental infection of Black Belly and INRA 401 straight and crossbred sheep with trichostrongyle nematode parasites. Vet Parasitol 116:239–249

    Article  CAS  PubMed  Google Scholar 

  • Herrera-Manzanilla FA, Ojeda-Robertos NF, González-Garduño R, Cámara-Sarmiento R, Torres-Acosta JFJ (2017) Gastrointestinal nematode populations with multiple anthelmintic resistance in sheep farms from the hot humid tropics of Mexico. Veterinary Parasitology: Regional Studies and Reports 9:29–33

    CAS  Google Scholar 

  • Idika IK, Chiejina SN, Mhomga LI, Nnadi PA, Ngongeh LA (2012) Changes in the body condition scores of Nigerian West African Dwarf sheep experimentally infected with mixed infections of Haemonchus contortus and Trichostrongylus colubriformis. Vet Parasitol 188:99–103

    Article  CAS  PubMed  Google Scholar 

  • Keane OM, Zadissa A, Wilson T, Hyndman DL, Greer GJ, Baird DB, McCulloch AF, Crawford AM, McEwan JC (2006) Gene expression profiling of Naïve sheep genetically resistant and susceptible to gastrointestinal nematodes. BMC Genomics 7:42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knox MR, Torres-Acosta JF, Aguilar-Caballero AJ (2006) Exploiting the effect of dietary supplementation of small ruminants on resilience and resistance against gastrointestinal nematodes. Vet Parasitol 139:385–393

    Article  CAS  PubMed  Google Scholar 

  • Lôbo RNB, Vieira LS, de Oliveira AA, Muniz EN, da Silva JM (2009) Genetic parameters for faecal egg count, packed-cell volume and body-weight in Santa Inês lambs. Genet Mol Biol 32:288–294

    PubMed  PubMed Central  Google Scholar 

  • Molento MB, Buzatti A, Sprenger LK (2016) Pasture larval count as a supporting method for parasite epidemiology, population dynamic and control in ruminants. Livest Sci 192:48–54

    Article  Google Scholar 

  • Morgan ER, van Dijk J (2012) Climate and the epidemiology of gastrointestinal nematode infections of sheep in Europe. Vet Parasitol 189:8–14

    Article  CAS  PubMed  Google Scholar 

  • Muñoz-Osorio GA, Aguilar-Caballero AJ, Sarmiento-Franco LA, Wurzinger M, Cámara-Sarmiento R (2016) Technologies and strategies for improving hair lamb fattening systems in tropical regions: a review. Ecosistemas y Recursos Agropecuarios 3:267–277

    Google Scholar 

  • Ngere L, Burke JM, Morgan JLM, Miller JE, Notter DR (2018) Genetic parameters for fecal egg counts and their relationship with body weights in Katahdin lambs. J Anim Sci 96:1590–1599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Notter DR, Burke JM, Miller JE, Morgan JLM (2017) Factors affecting fecal egg counts in periparturient Katahdin ewes and their lambs. J Anim Sci 95:103–112

    CAS  PubMed  Google Scholar 

  • Ojeda-Robertos NF, Torres-Acosta JFJ, González-Garduño R, Notter D (2017) Phenotypic expression of parasite susceptibility to Haemonchus contortus in Pelibuey sheep. Vet Parasitol 239:57–61

    Article  CAS  PubMed  Google Scholar 

  • Palomo-Couoh JG, Aguilar-Caballero AJ, Torres-Acosta JF, Magaña-Monforte JG (2016) Evaluation of different models to segregate Pelibuey and Katahdin ewes into resistant or susceptible to gastrointestinal nematodes. Trop Anim Health Prod 48:1517–1524

    Article  PubMed  Google Scholar 

  • Palomo-Couoh JG, Aguilar-Caballero AJ, Torres-Acosta JFJ, Gonzalez-Garduño R (2017) Comparing the phenotypic susceptibility of Pelibuey and Katahdin female lambs against natural gastrointestinal nematode infections under hot humid tropical conditions. Parasitol Res 116:1627–1636

    Article  CAS  PubMed  Google Scholar 

  • Reynecke DP, van Wyk JA, Gummow B, Dorny P, Boomker J (2011) Validation of the FAMACHA(c) eye colour chart using sensitivity/specificity analysis on two South African sheep farms. Vet Parasitol 177:203–211

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Vivas RI, Cob-Galera L (2005) Técnicas Diagnósticas en Parasitología Veterinaria Segunda edición. Universidad Autónoma de Yucatán. Mérida, México. ISBN: 970–698–045-8

  • Roeber F, Jex AR, Gasser RB (2013) Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance - an Australian perspective. Parasit Vectors 6:153–153

    Article  PubMed  PubMed Central  Google Scholar 

  • Russel A (1984) Body condition scoring of sheep. In Practice 6:91–93

    Article  CAS  PubMed  Google Scholar 

  • Saddiqi HA, Sarwar M, Iqbal Z, Nisa M, Shahzad MA (2012) Markers/parameters for the evaluation of natural resistance status of small ruminants against gastrointestinal nematodes. Animal 6:994–1004

    Article  CAS  PubMed  Google Scholar 

  • SAS (2004) Statistical Analysis System, SAS Institute Inc. SAS/ACCESS® 9.1 for windows. Cary, N. C. SAS Institute, Inc.

  • Soto-Barrientos N, Chan-Pérez JI, España-España E, Novelo-Chib LK, Palma-Ávila I, Ceballos-Mendoza AC, Sarabia-Hernández JA, Santos-Ricalde RH, Cámara-Sarmiento R, Torres-Acosta JFJ (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 Rumin Res 167:92–99

    Article  Google Scholar 

  • Torres-Acosta JFJ, Mendoza-de-Gives P, Aguilar-Caballero AJ, Cuellar-Ordaz JA (2012) Anthelmintic resistance in sheep farms: update of the situation in the American continent. Vet Parasitol 189:89–96

    Article  CAS  PubMed  Google Scholar 

  • Van Wyk JA, Mayhew E (2013) Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical lab guide. Onderstepoort J Vet Res 80:539

    PubMed  Google Scholar 

  • Vanimisetti HB, Greiner SP, Zajac AM, Notter DR (2004) Performance of hair sheep composite breeds: resistance of lambs to Haemonchus contortus. J Anim Sci 82:595–604

    Article  CAS  PubMed  Google Scholar 

  • Yazwinski TA, Goode L, Moncol DJ, Morgan GW, Linnerud AC (1979) Parasite resistance in straightbred and crossbred Barbados Blackbelly sheep 1, 2. J Anim Sci 49(4):919–926

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the Centre for Training and Reproduction of Minor Species (CECAREM) of Tabasco, Government, the Santa Martha and San Francisco farms for the facilities and animals granted. Claudia Virginia Zaragoza Vera received a scholarship from SEP-MEXICO (DSA/103.5/16/5835) to carry out her PhD studies at the Autonomous University of Yucatan, Mexico.

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Authors and Affiliations

  1. Facultad de Medicina Veterinaria y Zootecnia, Campus de Ciencias Biológicas y Agropecuarias, Universidad Autónoma de Yucatán, Km. 15.5, Carretera Mérida-Xmatkuil, Apdo. Postal 4-116, 97100, Mérida, Yucatán, México

    Claudia V. Zaragoza-Vera, Armando J. Aguilar-Caballero & Juan Felipe J. Torres-Acosta

  2. Unidad Regional Universitaria Sursureste, Universidad Autónoma Chapingo, Km 7.5 Carretera Teapa-Vicente Guerrero, Teapa, Tabasco, México

    Roberto González-Garduño

  3. División Académica de Ciencias Agropecuarias, Universidad Juárez Autónoma de Tabasco, Km. 25, Carretera Villahermosa-Teapa, R/a La Huasteca 2ª. Sección, 86298, Villahermosa, Tabasco, México

    Guadalupe Arjona-Jiménez, Maritza Zaragoza-Vera, José U. Medina-Reynés & Alma C. Berumen-Alatorre

Authors
  1. Claudia V. Zaragoza-Vera
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  2. Armando J. Aguilar-Caballero
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  3. Roberto González-Garduño
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  4. Guadalupe Arjona-Jiménez
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  5. Maritza Zaragoza-Vera
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  6. Juan Felipe J. Torres-Acosta
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  7. José U. Medina-Reynés
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  8. Alma C. Berumen-Alatorre
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Correspondence to Armando J. Aguilar-Caballero.

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Statement on the welfare of animals

The Bioethics Committee of the Campus of Biological and Agricultural Sciences of the Autonomous University of Yucatan, Mexico, approved the development of the present study under authorisation number CB-CCBA-D-2017-001.

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Zaragoza-Vera, C.V., Aguilar-Caballero, A.J., González-Garduño, R. et al. Variation in phenotypic resistance to gastrointestinal nematodes in hair sheep in the humid tropics of Mexico. Parasitol Res 118, 567–573 (2019). https://doi.org/10.1007/s00436-018-06201-w

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  • DOI: https://doi.org/10.1007/s00436-018-06201-w

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