Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-19T06:39:25.853Z Has data issue: false hasContentIssue false
  • English
  • Français

Artificial Haemonchus contortus infection as a strategy to induce protective immune response to natural infection in Pelibuey lambs

Published online by Cambridge University Press:  20 August 2020

A. Cruz-Tamayo ,
R. González-Garduño Open the ORCID record for R. González-Garduño [Opens in a new window] ,
G. Torres-Hernández ,
C. Becerril-Pérez ,
O. Hernández-Mendo ,
E. Ramírez-Bribiesca ,
M.E. López-Arellano ,
J. Vargas-Magaña  and
E. Hernández-Rueda
A. Cruz-Tamayo
Affiliation:
Colegio de Postgraduados, Campus Montecillo, Montecillo, Estado de México, Mexico Escuela Superior de Ciencias Agropecuarias, Universidad Autónoma de Campeche, Mexico
R. González-Garduño*
Affiliation:
Universidad Autónoma Chapingo, Unidad Regional Universitaria Sursureste, Teapa, Tabasco, Mexico
G. Torres-Hernández
Affiliation:
Colegio de Postgraduados, Campus Montecillo, Montecillo, Estado de México, Mexico
C. Becerril-Pérez
Affiliation:
Colegio de Postgraduados, Campus Montecillo, Montecillo, Estado de México, Mexico
O. Hernández-Mendo
Affiliation:
Colegio de Postgraduados, Campus Montecillo, Montecillo, Estado de México, Mexico
E. Ramírez-Bribiesca
Affiliation:
Colegio de Postgraduados, Campus Montecillo, Montecillo, Estado de México, Mexico
M.E. López-Arellano
Affiliation:
Centro Nacional de Investigación Disciplinaria en Salud Animal e Inocuidad, INIFAP, Mexico
J. Vargas-Magaña
Affiliation:
Escuela Superior de Ciencias Agropecuarias, Universidad Autónoma de Campeche, Mexico
E. Hernández-Rueda
Affiliation:
Escuela Superior de Ciencias Agropecuarias, Universidad Autónoma de Campeche, Mexico
*
Author for correspondence: R. González-Garduño, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The objective of this study was to evaluate the reduction in nematode faecal egg count (FEC) in Pelibuey lambs segregated as resistant (RES), susceptible (SUS) and intermediate (INT) to gastrointestinal nematodes. Twenty-nine weaned Pelibuey lambs, aged five months old, free of nematode infection, were used. Nine lambs were RES, six were SUS and 14 were INT lambs. The study consisted of two phases: in Phase 1 the lambs were infected experimentally with Haemonchus contortus. In Phase 2, the lambs were naturally infected by grazing. Faecal and blood samples were taken every week. The packed cell volume and total protein were quantified. The FEC value (FECmax) per lamb was recorded together with a natural reduction in FEC in the two phases. The data were analysed with a model of measures repeated over time. During Phase 1, the RES lambs showed the lowest FEC (1061 ± 1053) compared to the other groups (INT: 2385 ± 1794 eggs per gram of faeces (EPG); and SUS: 3958 ± 3037 EPG). However, in Phase 2 no significant differences (p > 0.05) were observed between the groups of lambs (RES: 275 ± 498 EPG; SUS: 504 ± 1036 EPG; and INT: 603 ± 1061 EPG). At the end of Phase 1, the FEC of RES lambs was naturally reduced by 75.5% in respect to FECmax (p < 0.05), and at the end of Phase 2 the reduction in FEC was 90% in respect to FECmax (p > 0.05); the same behaviour was observed in RES and SUS lambs. It is concluded that the artificial infection in the lambs induced a more rapid immune response in RES than SUS lambs, and all lambs developed high acquired resistance by continuous infection.

Keywords

Sheepresistancegastrointestinal nematodestotal plasma proteineosinophils
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e181
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Balic, A, Bowles, VM and Meeusen, ENT (2002) Mechanisms of immunity to Haemonchus contortus infection in sheep. Parasite Immunology 24(1), 39–46.CrossRefGoogle Scholar
Bowdridge, SA, Zajac, AM and Notter, DR (2015) St. Croix sheep produce a rapid and greater cellular immune response contributing to reduced establishment of Haemonchus contortus. Veterinary Parasitology 208(3–4), 204–210.CrossRefGoogle Scholar
Byers, SR and Kramer, JW (2010) Normal hematology of sheep and goats. pp. 836–842in Weiss, DJ, Wardrop, KJ (Eds) Schalm's veterinary hematology. 6th edn. Iowa, USA, Wiley-Blackwell.Google Scholar
Castillo, JA, Medina, RD, Villalobos, JM, Gayosso-Vázquez, A, Ulloa-Arvízu, R, Rodríguez, RA, Ramírez, HP and 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. Veterinary Parasitology 177(3–4), 339–344.CrossRefGoogle ScholarPubMed
CONAGUA (2019) Servicio Meteorológico Nacional. Normales climatológicas, https://smn.conagua.gob.mx/es/informacion-climatologica-por-estado?estado=tab (accessed August 13, 2020).Google Scholar
Corticelli, B and Lai, M (1963) Studies on the technique of culture of infective larvae of gastrointestinal strongyles of cattle. Acta de Medicina Veterinaria Napoli 9, 347–357.Google Scholar
Eady, SJ, Woolaston, RR and Barger, IA (2003) Comparison of genetic and nongenetic strategies for control of gastrointestinal nematodes of sheep. Livestock Production Science 81(1), 11–23.CrossRefGoogle Scholar
Emery, DL, Hunt, PW and Le Jambre, LF (2016) Haemonchus contortus: the then and now, and where to from here? International Journal for Parasitology 46, 755–769.CrossRefGoogle Scholar
González-Garduño, R, Gives, PM and Torres-Hernández, G (2013) Variability in the fecal egg count and the parasitic burden of hair sheep after grazing in nematode infected paddocks. Pesquisa Veterinaria Brasileira 33(4), 469-475.CrossRefGoogle Scholar
González-Garduño, R, López-Arellano, ME, Ojeda-Robertos, N, Liébano-Hernández, E and Mendoza-de Gives, P (2014) Diagnóstico in vitro y en campo de resistencia antihelmíntica en nematodos gastrointestinales de pequeños rumiantes. Archivos de Medicina Veterinaria 46(3), 399–405.CrossRefGoogle Scholar
González-Garduño, R, López-Arellano, ME, Mendoza-De-Gives, P, Ojeda-Robertos, NF and Chay-Canul, AJ (2016) Temporary immunity of Blackbelly lambs reinfected with Trichostrongylus colubriformis. Acta Scientiae Veterinariae 44, 1–6.Google Scholar
González Garduño, R, López-Arellano, ME, Torres-Hernández, G, Oliva-Hernández, J and Hinojosa-Cuéllar, JA (2019) Assessment of acquired resistance in previously infected lambs with. Indian Journal of Animal Research 53(9), 1223–1228.Google Scholar
Greer, AW and Hamie, JC (2016) Relative maturity and the development of immunity to gastrointestinal nematodes in sheep: an overlooked paradigm? Parasite Immunology 38(5), 263–272.CrossRefGoogle Scholar
Guo, Z, González, JF, Hernandez, JN, McNelly, TN, Corripio-Miyar, Y, Frew, D, Morrison, T, Yu, P and Li, RW (2016) Possible mechanisms of host resistance to Haemonchus contortus infection in sheep breeds native to the Canary Islands. Scientific Reports 6, 1–14.Google ScholarPubMed
Hodgkinson, JE, Kaplan, RM, Kenyon, F, et al. (2019) Refugia and anthelmintic resistance: concepts and challenges. International journal for parasitology. Drugs and drug resistance 10, 51–57.CrossRefGoogle ScholarPubMed
Jacobs, JR (2013) Characterizing peripheral cellular and humoral immune responses to Haemonchus contortus in sheep. Graduate Theses, Dissertations, and Problem Reports 489. doi:10.33915/etd.489CrossRefGoogle Scholar
Jacobs, JR, Greiner, SP and Bowdridge, SA (2015) Serum interleukin-4 (IL-4) production is associated with lower fecal egg count in parasite-resistant sheep. Veterinary Parasitology 211(1–2), 102–105.CrossRefGoogle ScholarPubMed
Karanu, FN, McGuire, TC, Davis, WC, Besser, TE and Jasmer, DP (1997) CD4+ T lymphocytes contribute to protective immunity induced in sheep and goats by Haemonchus contortus gut antigens. Parasite Immunology 19(10), 435–445.CrossRefGoogle ScholarPubMed
Karrow, NA, Goliboski, K, Stonos, N, Schenkel, F and Peregrine, A (2014) Review: genetics of helminth resistance in sheep. Canadian Journal of Animal Science 94(1), 1–9.CrossRefGoogle Scholar
Kottek, M, Grieser, J, Beck, C, Rudolf, B and Rubel, F (2006) World map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift 15(3), 259–263.CrossRefGoogle Scholar
Lee, CY, Munyard, KA, Gregg, K, Wetherall, JD, Stear, MJ and Groth, DM (2011) The influence of MHC and immunoglobulins A and E on host resistance to gastrointestinal nematodes in sheep. Journal of Parasitology Research 2011, 101848.CrossRefGoogle Scholar
MacKinnon, KM, Zajac, AM, Kooyman, FNJ and Notter, DR (2010) Differences in immune parameters are associated with resistance to Haemonchus contortus in Caribbean hair sheep. Parasite Immunology 32(7), 484–493.CrossRefGoogle ScholarPubMed
McRae, KM, Stear, MJ, Good, B and Keane, OM (2015) The host immune response to gastrointestinal nematode infection in sheep. Parasite Immunology 37(12), 605–613.CrossRefGoogle Scholar
Miller, JE and Horohov, DW (2006) Immunological aspects of nematode parasite control in sheep. Journal of Animal Science 84(Suppl), 124–132.CrossRefGoogle Scholar
Moreno, CR, Sallé, G, Jacquiet, P, et al. (2017) La résistance génétique aux infections par les nématodes gastro-intestinaux chez les petits ruminants: un enjeu de durabilité pour les productions à l'herbe. INRA Productions Animales 30(1), 47–56.CrossRefGoogle Scholar
Morteo-Gómez, R, González-Garduño, R, Torres-Hernández, G, Nuncio-Ochoa, G, Becerril-Pérez, C, Gallegos-Sánchez, J and Aranda-Ibañez, E (2004) Effect of the phenotypic variation in the resistance of Pelibuey lambs to the infestation with gastrointestinal nematodes. Agrociencia 38(4), 395–404.Google Scholar
Mugambi, JM, Bain, RK, Wanyangu, SW, Ihiga, MA, Duncan, JL, Murray, M and Stear, MJ (1997) Resistance of four sheep breeds to natural and subsequent artificial Haemonchus contortus infection. Veterinary Parasitology 69(3–4), 265–273.CrossRefGoogle ScholarPubMed
Notter, DR, Andrew, SA and Zajac, AM (2003) Responses of hair and wool sheep to a single fixed dose of infective larvae of Haemonchus contortus. Small Ruminant Research 47(3), 221–225.CrossRefGoogle Scholar
Ojeda-Robertos, NF, Torres-Acosta, JFJ, González-Garduño, R and Notter, DR (2017) Phenotypic expression of parasite susceptibility to Haemonchus contortus in Pelibuey sheep. Veterinary Parasitology 239, 57–61.CrossRefGoogle ScholarPubMed
Ortolani, EL, do Rego Leal, ML, Minervino, AH, Aires, AR, Coop, RL, Jackson, F and Suttle, NF (2013) Effects of parasitism on cellular immune response in sheep experimentally infected with Haemonchus contortus. Veterinary Parasitology 196(1–2), 230–234.CrossRefGoogle ScholarPubMed
Robinson, N, PIedrafita, D, Snibson, K, Harrison, P and Meeusen, EN (2010) Immune cell kinetics in the ovine abomasal mucosa following hyperimmunization and challenge with Haemonchus contortus. Veterinary Research 41(37), 1–10.CrossRefGoogle ScholarPubMed
Rowe, A, McMaster, K, Emery, D and Sangster, N (2008) Haemonchus contortus infection in sheep: parasite fecundity correlates with worm size and host lymphocyte counts. Veterinary Parasitology 153(3–4), 285–293.CrossRefGoogle ScholarPubMed
Saccareau, M, Sallé, G, Robert-Granié, C, Duchemin, T, Jacquiet, P, Blanchard, A, Cabaret, J and Moreno, CR (2017) Meta-analysis of the parasitic phase traits of Haemonchus contortus infection in sheep. Parasites and Vectors 10(1), 1–14.CrossRefGoogle Scholar
Saddiqi, HA, Iqbal, Z, Khan, MN and Muhammad, G (2010) Comparative resistance of sheep breeds to Haemonchus contortus in a natural pasture infection. International Journal of Agriculture and Biology 12(5), 739–743.Google Scholar
Saddiqi, HA, Sarwar, M, Iqbal, Z, Nisa, M and Shahzad, MA (2012) Markers/parameters for the evaluation of natural resistance status of small ruminants against gastrointestinal nematodes. Animal 6(6), 994–1004.CrossRefGoogle ScholarPubMed
SAS (2004) The SAS System for Windows, version 9. SAS Institute. Inc., Cary, North Carolina.Google Scholar
Shakya, KP, Miller, JE and Horohov, DW (2009) A Th2 type of immune response is associated with increased resistance to Haemonchus contortus in naturally infected Gulf Coast native lambs. Veterinary Parasitology 163(1–2), 57–66.CrossRefGoogle ScholarPubMed
Sréter, T, Kassai, T and Takács, E (1994) The heritability and specificity of responsiveness to infection with Haemonchus contortus in sheep. International Journal for Parasitology 24(6), 871–876.CrossRefGoogle Scholar
Stear, MJ, Bairden, K, Duncan, JL and Murray, M (1995) A comparison of the responses to repeated experimental infections with Haemonchus contortus among Scottish Blackface lambs. Veterinary Parasitology 60(1–2), 69–81.CrossRefGoogle ScholarPubMed
Stear, MJ, Strain, S and Bishop, SC (1999) Mechanisms underlying resistance to nematode infection. International Journal for Parasitology 29(1), 51–56.CrossRefGoogle ScholarPubMed
Sweeney, T, Hanrahan, JP, Ryan, MT and Good, B (2016) Immunogenomics of gastrointestinal nematode infection in ruminants – breeding for resistance to produce food sustainably and safely. Parasite Immunology 38(9), 569–586.CrossRefGoogle ScholarPubMed
Terefe, G, Lacroux, C, Andreoletti, O, et al. (2007) Immune response to Haemonchus contortus infection in susceptible (INRA 401) and resistant (Barbados Black Belly) breeds of lambs. Parasite Immunology 29(8), 415–424.CrossRefGoogle ScholarPubMed
Thienpont, D, Rochette, F and Vanparijs, OFJ (2003) Diagnosing helminthiasis by coprological examination. 3rd edn.Beerse, Belgium, Janssen Research Foundation.Google Scholar
Torres-Acosta, JFJ, Mendoza-de-Gives, P, Aguilar-Caballero, AJ and Cuéllar-Ordaz, JA (2012) Anthelmintic resistance in sheep farms: update of the situation in the American continent. Veterinary Parasitology 189(1), 89–96.CrossRefGoogle ScholarPubMed
Valilou, RH, Rafat, SA, Notter, DR, Shojda, D, Moghaddam, G and Nematollahi, A (2015) Fecal egg counts for gastrointestinal nematodes are associated with a polymorphism in the MHC-DRB1 gene in the Iranian Ghezel sheep breed. Frontiers in Genetics 6, 1–11.CrossRefGoogle ScholarPubMed
van Wyk, JA and Mayhew, E (2013) Morphological identification of parasitic nematode infective larvae of small ruminants and cattle: a practical lab guide. Onderstepoort Journal of Veterinary Research 80(1), 1–14.CrossRefGoogle ScholarPubMed
Woolaston, RR, Barger, IA and Piper, LR (1990) Response to helminth infection of sheep selected for resistance to Haemonchus contortus. International Journal for Parasitology 20(8), 1015–1018.CrossRefGoogle ScholarPubMed
Yang, Y, Zhou, QJ, Chen, XQ, Yan, BL, Guo, XL, Zhang, HL and Du, AF (2015) Profiling of differentially expressed genes in sheep T lymphocytes response to an artificial primary Haemonchus contortus infection. Parasites and Vectors 8(1), 235.CrossRefGoogle Scholar
Zaragoza-Vera, CV, Aguilar-Caballero, AJ, González-Garduño, R, Arjona-Jiménez, G, Zaragoza-Vera, M, Torres-Acosta, J, Medina-Reynés, JU and Berumen-Alatorre, AC (2019) Variation in phenotypic resistance to gastrointestinal nematodes in hair sheep in the humid tropics of Mexico. Parasitology Research 118(2), 567–573.CrossRefGoogle Scholar
Zaros, LG, Neves, MRM, Benvenuti, CL, Navarro, AM, Sider, LH, Coutinho, LL and Vieira, LS (2014) Response of resistant and susceptible Brazilian Somalis crossbreed sheep naturally infected by Haemonchus contortus. Parasitology Research 113(3), 1155–1161.CrossRefGoogle ScholarPubMed
Zvinorova, PI, Halimani, TE, Muchadeyi, FC, Matika, O, Riggio, V and Dzama, K (2016) Breeding for resistance to gastrointestinal nematodes – the potential in low-input/output small ruminant production systems. Veterinary Parasitology 225, 19–28.CrossRefGoogle ScholarPubMed