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Influence of breed and parasite challenge on the immune response to naturally acquired intestinal nematode infection in sheep

Published online by Cambridge University Press:  18 April 2022

A.C.A. Albuquerque Open the ORCID record for A.C.A. Albuquerque [Opens in a new window] ,
F.A. Almeida Open the ORCID record for F.A. Almeida [Opens in a new window] ,
C.C. Bassetto Open the ORCID record for C.C. Bassetto [Opens in a new window] ,
J.G.G. Lins Open the ORCID record for J.G.G. Lins [Opens in a new window]  and
A.F.T. Amarante Open the ORCID record for A.F.T. Amarante [Opens in a new window]
A.C.A. Albuquerque*
Affiliation:
School of Veterinary Medicine and Animal Science, UNESP – São Paulo State University, Rua Professor Doutor Walter Mauricio Correa s/n, CEP 18618-681, Botucatu, SP, Brazil Institute of Biosciences, UNESP – São Paulo State University, Rua Professor Dr Antônio Celso Wagner Zanin, 250, CEP 18618-689, Botucatu, SP, Brazil
F.A. Almeida
Affiliation:
Institute of Biosciences, UNESP – São Paulo State University, Rua Professor Dr Antônio Celso Wagner Zanin, 250, CEP 18618-689, Botucatu, SP, Brazil
C.C. Bassetto
Affiliation:
Institute of Biosciences, UNESP – São Paulo State University, Rua Professor Dr Antônio Celso Wagner Zanin, 250, CEP 18618-689, Botucatu, SP, Brazil
J.G.G. Lins
Affiliation:
School of Veterinary Medicine and Animal Science, UNESP – São Paulo State University, Rua Professor Doutor Walter Mauricio Correa s/n, CEP 18618-681, Botucatu, SP, Brazil Institute of Biosciences, UNESP – São Paulo State University, Rua Professor Dr Antônio Celso Wagner Zanin, 250, CEP 18618-689, Botucatu, SP, Brazil
A.F.T. Amarante
Affiliation:
Institute of Biosciences, UNESP – São Paulo State University, Rua Professor Dr Antônio Celso Wagner Zanin, 250, CEP 18618-689, Botucatu, SP, Brazil
*
Author for correspondence: A.C.A. Albuquerque, E-mail: [email protected]
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Abstract

Natural infection by intestinal nematodes was assessed in Santa Ines and Ile de France sheep breeds, over a five-month grazing period, with emphasis on the development of the immune response in lambs under two anthelmintic treatment regimens. Nineteen Santa Ines and 19 Ile de France male lambs were allocated into two treatment groups: animals under suppressive treatment with anthelmintics; and animals under targeted selective treatment (TST). The nematodes Trichostrongylus colubriformis and Strongyloides papillosus showed the highest infection intensity in the TST animals in both breeds. Parasite-specific immunoglobulin G levels were significantly higher and more rapidly induced in Santa Ines lambs. Additionally, these lambs had higher levels of parasite-specific immunoglobulin A in intestinal mucus. Animals under TST had higher means of mast cells and globule leukocytes in the intestinal mucosa due to longer and greater parasite challenge in comparison with the suppressive group. A breed effect (P < 0.05) was recorded for mast cells, with Santa Ines lambs presenting the highest counts. Although Santa Ines lambs had lower intestinal nematode counts than Ile de France lambs, they had shown a large variation in T. colubriformis burden, with most of them presenting a marked worm burden, despite showing an earlier and more intense immune response to intestinal nematode infection.

Keywords

Intestinal nematodesanthelmintic treatmentmast cellsIgA
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e27
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Albuquerque, ACA, Bassetto, CC, de Almeida, FA and Amarante, AFT (2017) Development of Haemonchus contortus resistance in sheep under suppressive or targeted selective treatment with monepantel. Veterinary Parasitology 246(2017), 112–117.CrossRefGoogle ScholarPubMed
Albuquerque, ACA, Bassetto, CC, Almeida, FA, Hildersley, KA, McNeilly, TN, Britton, C and Amarante, AFT (2019) Differences in immune responses to Haemonchus contortus infection in the susceptible Ile de France and the resistant Santa Ines sheep under different anthelmintic treatments regimens. Veterinary Research 50(1), 104.CrossRefGoogle Scholar
Almeida, FA, Garcia, KCOD, Torgerson, PR and Amarante, AFT (2010) Multiple resistance to anthelmintics by Haemonchus contortus and Trichostrongylus colubriformis in sheep in Brazil. Parasitology International 59(4), 622–625.CrossRefGoogle ScholarPubMed
Almeida, FA, Bassetto, CC, Amarante, MRV, Albuquerque, ACA, Starling, RZC and Amarante, AFT (2018) Helminth infections and hybridization between Haemonchus contortus and Haemonchus placei in sheep from Santana do Livramento, Brazil. Revista Brasileira de Parasitologia Veterinaria 27(3), 280–288.Google Scholar
Almeida, FA, Albuquerque, ACA, Bassetto, CC, Starling, RZC, Lins, JGG and Amarante, AFT (2020) Long spelling periods are required for pasture to become free of contamination by infective larvae of Haemonchus contortus in a humid subtropical climate of São Paulo state, Brazil. Veterinary Parasitology 279, 109060.CrossRefGoogle Scholar
Amarante, AFT (2014) Sustainable worm control practices in South America. Small Ruminant Research 118(1–3), 56–62.CrossRefGoogle Scholar
Amarante, AFT and Barbosa, M (1998) Comparison between pasture sampling and tracer lambs to evaluate contamination of sheep pastures by nematode infective larvae. Revista Brasileira de Parasitologia Veterinária 7, 95–100Google Scholar
Amarante, AFT, Bricarello, PA, Rocha, RA and Gennari, SM (2004) Resistance of Santa Ines, Suffolk and Ile de France sheep to naturally acquired gastrointestinal nematode infections. Veterinary Parasitology 120(1–2), 91–106.CrossRefGoogle Scholar
Amarante, AFT, Rocha, RA and Bricarello, PA (2007) Relationship of intestinal histology with the resistance to Trichostrongylus colubriformis infection in three breeds of sheep. Pesquisa Veterinaria Brasileira 27(1), 43–48.CrossRefGoogle Scholar
Amarante, AFT, Susin, I, Rocha, RA, Silva, MB, Mendes, CQ and Pires, AV (2009) Resistance of Santa Ines and crossbred ewes to naturally acquired gastrointestinal nematode infections. Veterinary Parasitology 165(3–4), 273–280.CrossRefGoogle Scholar
Amarante, MRV, Bassetto, CC, Neves, JH and Amarante, AFT (2014) Species-specific PCR for the identification of Cooperia curticei (Nematoda: Trichostrongylidae) in sheep. Journal of Helminthology 88(4), 447–452.CrossRefGoogle ScholarPubMed
Andronicos, N, Hunt, P and Windon, R (2010) Expression of genes in gastrointestinal and lymphatic tissues during parasite infection in sheep genetically resistant or susceptible to Trichostrongylus colubriformis and Haemonchus contortus. International Journal for Parasitology 40(4), 417–429.CrossRefGoogle ScholarPubMed
Bahirathan, M, Miller, JE, Barras, SR and Kearney, MT (1996) Susceptibility of Suffolk and Gulf Coast native suckling lambs to naturally acquired strongylate nematode infection. Veterinary Parasitology 65(3–4), 259–268.CrossRefGoogle ScholarPubMed
Balic, A, Bowles, VM and Meeusen, ENT (2002) Mechanisms of immunity to Haemonchus contortus infection in sheep. Parasite Immunology 24(1), 39–46.CrossRefGoogle ScholarPubMed
Barger, IA (1985) The statistical distribution of trichostrongylid nematodes in grazing lambs. International Journal for Parasitology 15, 645e649.CrossRefGoogle ScholarPubMed
Beasley, AM, Kahn, LP and Windon, RG (2010) The periparturient relaxation of immunity in merino ewes infected with Trichostrongylus colubriformis: parasitological and immunological responses. Veterinary Parasitology 168(1–2), 60–70.CrossRefGoogle ScholarPubMed
Bricarello, PA, Amarante, AFT, Rocha, RA, Cabral Filho, SL, Huntley, JF, Houdijk, JGM, Abdalla, AL and Gennari, SM (2005) Influence of dietary protein supply on resistance to experimental infections with Haemonchus contortus in Ile de France and Santa Ines lambs. Veterinary Parasitology 134(1–2), 99–109.CrossRefGoogle Scholar
Cantacessi, C, Mitreva, M, Campbell, BE, Hall, RS, Young, ND, Jex, AR, Ranganathan, S and Gasser, RB (2010) First transcriptomic analysis of the economically important parasitic nematode, Trichostrongylus colubriformis, using a next-generation sequencing approach. Infection, Genetics and Evolution 10(8), 1199–1207.CrossRefGoogle ScholarPubMed
Cardia, DFF, Rocha-Oliveira, RA, Tsunemi, MH and Amarante, AFT (2011) Immune response and performance of growing Santa Ines lambs to artificial Trichostrongylus colubriformis infections. Veterinary Parasitology 182(2–4), 248–258.CrossRefGoogle Scholar
Cintra, MCR, Teixeira, VN, Nascimento, LV and Sotomaior, CS (2016) Lack of efficacy of monepantel against Trichostrongylus colubriformis in sheep in Brazil. Veterinary Parasitology 216, 4–6.CrossRefGoogle ScholarPubMed
Coop, RL and Kyriazakis, I (1999) Nutrition–parasite interaction. Veterinary Parasitology 84(3–4), 187–204.CrossRefGoogle ScholarPubMed
Costa, RLD, Bueno, MS, Veríssimo, CJ, Cunha, EA, Santos, LE, Oliveira, SM, Spósito Filha, E and Otsuk, IP (2007) Performance and nematode infection of ewe lambs on intensive rotational grazing with two different cultivars of Panicum maximum. Tropical Animal Health and Production 39(4), 255–263.CrossRefGoogle ScholarPubMed
De Chaneet, GC and Dunsmore, JD (1988) Climate and the distribution of intestinal Trichostrongylus spp. of sheep. Veterinary Parasitology 26(3–4), 273–283.CrossRefGoogle ScholarPubMed
de la Chevrotière, C, Bambou, JC, Arquet, R, Jacquiet, P and Mandonnet, N (2012) Genetic analysis of the potential role of IgA and IgE responses against Haemonchus contortus in parasite resistance of creole goats. Veterinary Parasitology 186(3–4), 337–343.CrossRefGoogle ScholarPubMed
Dias-Silva, TP, Filho, ALA, Katiki, LM, Do Amarante, AFT, Abdalla, AL and Louvandini, H (2020) Trichostrongylus Colubriformis infection in Santa Inês lambs: impact on feed digestibility, blood markers, and nitrogen balance. Revista Brasileira de Parasitologia Veterinaria 29(2), 1–7.Google Scholar
Dias-Silva, TP, Louvandini, H and Do Amarante, AFT (2021) Trichostrongylus colubriformis affecting sheep phosphorus metabolism and precision feeding as a mitigating strategy. Revista Brasileira de Parasitologia Veterinaria 30, 1–6.Google ScholarPubMed
Dias-Silva, TP, Ventoso Bompadre, TF, Danasekaran, DK, et al. (2019) Trichostrongylus colubriformis infection: impact on digesta passage rate and lamb performance. Veterinary Parasitology 272, 17–22.CrossRefGoogle Scholar
Dimitrijević, B, Borozan, S, Katić-Radivojević, S and Stojanović, S (2012) Effects of infection intensity with Strongyloides papillosus and albendazole treatment on development of oxidative/nitrosative stress in sheep. Veterinary Parasitology 186(3–4), 364–375.CrossRefGoogle ScholarPubMed
Douch, PGC, Harriston, GBL, Elliott, DC, Buchanan, LL and Greer, KS (1986) Relationship of gastrointestinal histology and mucus antiparasite activity with the development of resistance to trichostrongyle infections in sheep. Veterinary Parasitology 20(4), 315–331.CrossRefGoogle ScholarPubMed
Harrison, GBL, Pulford, HD, Hein, WR, Barber, TK, Shaw, RJ, McNeill, M, Wakefield, SJ and Shoemaker, CB (2003) Immune rejection of Trichostrongylus colubriformis in sheep; a possible role for intestinal mucus antibody against an L3-specific surface antigen. Parasite Immunology 25(1), 45–53.CrossRefGoogle ScholarPubMed
Huntley, JF, Nwelands, GFJ, Jackson, F and Miller, HRP (1992) The influence of challenge dose, duration of immunity, or steroid treatment on mucosal mast cells and on the distribution of sheep mast cell proteinase in Haemonchus-infected sheep. Parasite Immunology 14(4), 429–440.CrossRefGoogle ScholarPubMed
Idika, IK, Chiejina, SN, Mhomga, LI, Ngongeh, LA and Nnadi, PA (2012) Responses of the humid zone ecotype of the Nigerian West African Dwarf sheep to mixed infections with Haemonchus contortus and Trichostrongylus colubriformis. Parasitology Research 110(6), 2521–2527.CrossRefGoogle ScholarPubMed
Inclan-Rico, JM and Siracusa, MC (2018) First responders: innate immunity to helminths. Trends in Parasitology 34(10), 861–880.CrossRefGoogle ScholarPubMed
Kanobana, K, Vervelde, L, van der Veer, M, Eysker, M and Ploeger, HW (2001) Characterisation of host responder types after a single Cooperia oncophora infection: kinetics of the systemic immune response. Parasite Immunology 23, 641–653.CrossRefGoogle Scholar
Kyriazakis, I, Anderson, DH, Oldham, JD, Coop, RL and Jackson, F (1996) Long-term subclinical infection with Trichostrongylus colubriformis: effects on food intake, diet selection and performance of growing lambs. Veterinary Parasitology 61(3–4), 297–313.CrossRefGoogle ScholarPubMed
Makovcová, K, Jankovská, I, Vadlejch, J, Langrová, I, Vejl, P and Lytvynets, A (2009) The contribution to the epidemiology of gastrointestinal nematodes of sheep with special focus on the survival of infective larvae in winter conditions. Parasitology Research 104(4), 795–799.CrossRefGoogle Scholar
McClure, SJ, Emery, DL, Wagland, BM and Jones, WO (1992) A serial study of rejection of Trichostrongylus colubriformis by immune sheep. International Journal for Parasitology 22(2), 227–234.CrossRefGoogle ScholarPubMed
McMahon, C, Gordon, AW, Edgar, HWJ, Hanna, REB, Brennan, GP and Fairweather, I (2012) The effects of climate change on ovine parasitic gastroenteritis determined using veterinary surveillance and meteorological data for Northern Ireland over the period 1999–2009. Veterinary Parasitology 190(1–2), 167–177.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 ScholarPubMed
Mederos, AE, Ramos, Z and Banchero, GE (2014) First report of monepantel Haemonchus contortus resistance on sheep farms in Uruguay. Parasites and Vectors 7(1), 1–4.CrossRefGoogle ScholarPubMed
Medina-Pérez, P, Ojeda-Robertos, NF, Reyes-García, ME, Cámara-Sarmiento, R and Torres-Acosta, JFJ (2015) Evaluation of a targeted selective treatment scheme to control gastrointestinal nematodes of hair sheep under hot humid tropical conditions. Small Ruminant Research 127, 86–91.CrossRefGoogle Scholar
Mowen, KA and Glimcher, LH (2004) Signaling pathways in Th2 development. Immunological Reviews 202, 203–222.CrossRefGoogle ScholarPubMed
Niezen, JH, Miller, CM, Robertson, HA, Wilson, SR and Mackay, AD (1998) Effect of topographical aspect and farm system on the population dynamics of Trichoslongylus larvae on a hill pasture. Veterinary Parasitology 78, 37–48.CrossRefGoogle ScholarPubMed
Pernthaner, A, Cole, SA, Morrison, L, Green, R, Shaw, RJ and Hein, WR (2006) Cytokine and antibody subclass responses in the intestinal lymph of sheep during repeated experimental infections with the nematode parasite Trichostrongylus colubriformis. Veterinary Immunology and Immunopathology 114(1–2), 135–148.CrossRefGoogle ScholarPubMed
Rocha, RA, Bricarello, PA, Silva, MB, Houdijk, JGM, Almeida, FA, Cardia, DFF and Amarante, AFT (2011) Influence of protein supplementation during late pregnancy and lactation on the resistance of Santa Ines and Ile de France ewes to Haemonchus contortus. Veterinary Parasitology 181(2–4), 229–238.CrossRefGoogle Scholar
Rocha, RA, Bricarello, PA, Rocha, GP and Amarante, AFT (2014) Retrieval of Trichostrongylus colubriformis infective larvae from grass contaminated in winter and in spring. Revista Brasileira de Parasitologia Veterinária 23(4), 463–472.CrossRefGoogle Scholar
Santos, MC, Xavier, JK, Amarante, MRV, Bassetto, CC and Amarante, AFT (2014) Immune response to Haemonchus contortus and Haemonchus placei in sheep and its role on parasite specificity. Veterinary Parasitology 203(1-2), 127–138.CrossRefGoogle ScholarPubMed
Shakya, KP, Miller, JE, Lomax, LG and Burnett, DD (2011) Evaluation of immune response to artificial infections of Haemonchus contortus in Gulf Coast native compared with Suffolk lambs. Veterinary Parasitology 181(2–4), 239–247.CrossRefGoogle ScholarPubMed
Sharpe, C, Thornton, DJ and Grencis, RK (2018) A sticky end for gastrointestinal helminths; the role of the mucus barrier. Parasite Immunology 40(4), 1–10.CrossRefGoogle ScholarPubMed
Silva, BF, Amarante, MRV, Kadri, SM, Carrijo-Mauad, JR and Amarante, AFT (2008) Vertical migration of Haemonchus contortus third stage larvae on Brachiaria decumbens grass. Veterinary Parasitology 158(1–2), 85–92.CrossRefGoogle ScholarPubMed
Silva, BF, Bassetto, CC and Amarante, AFT (2012) Immune responses in sheep naturally infected with Oestrus ovis (Diptera: Oestridae) and gastrointestinal nematodes. Veterinary Parasitology 190(1–2), 120–126.CrossRefGoogle ScholarPubMed
Sorobetea, D, Svensson-Frej, M and Grencis, R (2018) Immunity to gastrointestinal nematode infections. Mucosal Immunology 11(2), 304–315.CrossRefGoogle ScholarPubMed
Stear, MJ and Murray, M (1994) Genetic resistance to parasitic disease: particularly of resistance in ruminants to gastrointestinal nematodes. Veterinary Parasitology 54(1–3), 161–176.CrossRefGoogle ScholarPubMed
Taylor, EL (1939) Technique for the estimation of pasture infestation by strongyloid larvae. Parasitology 31(4), 473–478.CrossRefGoogle Scholar
Thomaz-Soccol, V, De Souza, FP, Sotomaior, C, Castro, EA, Milczewski, V, Mocelin, G and Do Carmo Pessoa E Silva, M (2004) Resistance of gastrointestinal nematodes to anthelmintics in sheep (Ovis aries). Brazilian Archives of Biology and Technology 47(1), 41–47.CrossRefGoogle Scholar
Ueno, H and Gonçalves, PC (1998) Manual para diagnóstico das helmintoses de ruminantes. 4th edn. Tokyo, Japan: Japan International Cooperation Agency.Google Scholar
Valcárcel, F, Aguilar, A and Sánchez, M (2015) Field evaluation of targeted selective treatments to control subclinical gastrointestinal nematode infections on small ruminant farms. Veterinary Parasitology 211(1–2), 71–79.CrossRefGoogle ScholarPubMed
van Wyk, JA (2001) Refugia – overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort Journal of Veterinary Research 68, 55–67.Google ScholarPubMed
van Wyk, JA, Malan, FS and Bath, GF (1997) Rampant anthelmintic resistance in sheep in South Africa – what are the options? pp. 51–63 in 16th International Conference of the World Association for the Advancement of Veterinary Parasitology, Workshop on Managing Anthelmintic Resistance in Endoparasites, Sun City, 1997.Google Scholar
van Wyk, JA, Hoste, H, Kaplan, RM and Besier, RB (2006) Targeted selective treatment for worm management-How do we sell rational programs to farmers? Veterinary Parasitology 139(4), 336–346.CrossRefGoogle Scholar
Wilmsen, MO, Silva, BF, Bassetto, CC and Amarante, AFTd (2014) Gastrointestinal nematode infections in sheep raised in Botucatu, state of São Paulo, Brazil. Revista Brasileira de Parasitologia Veterinária 23(3), 348–354.CrossRefGoogle ScholarPubMed
Zajac, AM (2006) Gastrointestinal nematodes of small ruminants: life cycle, anthelmintics, and diagnosis. Veterinary Clinics of North America – Food Animal Practice 22(3), 529–541.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
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