Temporary Immunity of Blackbelly Lambs Reinfected with Trichostrongylus colubriformis

Roberto González Garduño, María Eugenia López Arellano, Pedro Mendoza de Gives, Nadia Florencia Ojeda Robertos, Alfonso Juventino Chay Canul

Abstract


Background: Trichostrongylus colubriformis is one of the most prevalent gastrointestinal nematodes of sheep in warm climates. In this nematode species, anthelmintic resistance (AR) has been reported, which has motivated the search for alternative methods to control it. One practice is to increase the immune response level through the selection of animals with natural resistance, such as Blackbelly sheep. The aim of this study was to investigate the response of IgA and IgG in serum and saliva and the level of cells involved in the acquired resistance in Blackbelly lambs after single artificial reinfection with a resistant strain of Trichostrongylus colubriformis.

Materials, Methods & Results: Sixteen weaned lambs grazed for one month in nematode-contaminated grasslands. All the lambs were treated with Albendazole and Levamisole; later, they were stabled for two months. After that, eight lambs were re-infected with 6000 larvae of T. colubriformis and other eight lambs remained naturally infected. In addition, eight nematode-free lambs raised in cages, served as negative control. Blood samples were taken fortnightly to determine packed cell volume (PCV, %), plasmatic protein (g dL-1), as well as absolute and differential leukocytes. The eggs per gram of feces (EPG) were recorded. An indirect ELISA against T. colubriformis Ag was performed to determine the IgG and IgA levels. All data were analyzed by repeated measures. The EPG in the re-infected group increased after 34 days (625 ± 287), while in the naturally infected group it remained close to 200 ± 158 throughout the study. The control lambs did not show any infection. The PCV (29.4 ± 3.4 %), basophils (44 ± 74), lymphocytes (8443 ± 2845) and monocytes (77 ± 91) counts were not affected by infection. The IgA OD against T. colubriformis increased significantly after 15 days post-infection (dpi) in the re-infected lambs (1.69 ± 0.5, 80% with regards to standard). With IgG was not possible to distinguish the effect of infection.

Discussion: Highly persistent infection of T. colubriformis was observed for at least four months in the naturally infected group despite having been treated with anthelmintics. It is a significant problem because this species has a high prevalence in the region of study and shows anthelmintic resistance. For such reason, is important to evaluate the ability of the animal to develop an immune response. In other study, a natural reduction in the fecal egg count (FEC) was indicated at 100 dpi in the same species, but in the present work, the FEC could not be reduced until around 120 days when the naturally infected lambs were evaluated. The larger number of neutrophils and leukocytes in both the naturally infected and re-infected groups implies a sustained response for a long time. While the higher counts of eosinophils only in the re-infected group were produced as an immediate response to infection with T. colubriformis. Similarly, with a single infection of T. colubriformis, in Santa Ines sheep the infected lambs showed significantly higher levels of serum IgA than the control group. In this case, differences in IgA activity were observed between the re-infected lambs and the other groups at fifteen dpi, but the basal levels of IgA in the naturally pre-infected lambs were maintained at least five weeks after infection. In conclusion, an increase in the peripheral immune response in lambs re-infected with T. colubriformis resulted from the increase in IgA levels in serum and saliva, and increase in the number of peripheral eosinophils, total leukocytes and neutrophils. Re-infected lambs had a higher level of IgA than naturally infected lambs and control lambs, making possible to promote the immune response with a single re-infection with Trichostrongylus colubriformis.


Keywords


antibody; gastrointestinal nematodes; serum; sheep; somatic antigen.

Full Text:

PDF

References


Almeida F.A., Garcia K.C.O.D., Torgerson P.R. & Amarante A.F.T. 2010. Multiple resistance to anthelmintics by Haemonchus contortus and Trichostrongylus colubriformis in sheep in Brazil. Parasitology International. 59: 622-625.

Bishop S.C. & Morris C.A. 2007. Genetics of disease resistance in sheep and goats. Small Ruminant Research. 70: 48-59.

Bowdridge S., MacKinnon K., McCann J.C., Zajac A.M. & Notter D.R. 2013. Hair-type sheep generate an accelerated and longer-lived humoral immune response to Haemonchus contortus infection. Veterinary Parasitology. 196: 172-178.

Cardia D.F.F., Rocha-Oliveira R.A., Tsunemi M.H. & Amarante A.F.T.D. 2011. Immune response and performance of growing Santa Ines lambs to artificial Trichostrongylus colubriformis infections. Veterinary Parasitology. 182: 248258.

Craig B.H., Pilkington J.G. & Pemberton J.M. 2006. Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology. 133: 485-496.

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.

Cruz-Rojo M.A., Martínez-Valladares M. & Rojo-Vázquez F.A. 2012. Teladorsagia circumcincta antibodies in serum and milk samples in experimentally infected lactating ewes. Veterinary Parasitology. 188: 386-390.

de la Chevrotière C., Bambou J.C., Arquet R., Jacquiet P. & 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: 337-343.

González-Garduño R., López-Arellano M.E., Ojeda-Robertos N., Liébano-Hernández E. & 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: 399-405.

Harrison G.B.L., Pulford H.D., Hein W.R., Barber T.K., Shaw R.J., McNeill M. & Wakefield J. 2003. Immune rejection of Trichostrongylus colubriformis in sheep; a possible role for intestinal mucus antibody against an L3-specific surface Ag. Parasite Immunology. 25: 45-53.

Hunt P.W., Kijas J. & Ingham A. 2013. Understanding parasitic infection in sheep to design more efficient animal selection strategies. The Veterinary Journal. 197: 143-152.

Kemper K.E., Palmer D.G., Liu S.M., Greeff J.C., Bishop S.C. & Karlsson L.J.E. 2010. Reduction of faecal worm egg count, worm numbers and worm fecundity in sheep selected for worm resistance following artificial infection with Teladorsagia circumcincta and Trichostrongylus colubriformis. Veterinary Parasitology. 171: 238-246.

Kottek M., Grieser J., Beck C., Rudolf B. & Rubel F. 2006. World Map of the Köppen-Geiger climate classification updated. Meteorologische Zeitschrift. 15: 259-263.

López-Ruvalcaba O.A., González-Garduño R., Osorio-Arce M.M., Aranda-Ibañez E. & Díaz-Rivera P. 2013. Cargas y especies prevalentes de nematodos gastrointestinales en ovinos de pelo destinados al abasto. Revista Mexicana de Ciencia Pecuaria. 4: 223-234.

Macarthur F.A., Kahn L.P. & Windon R.G. 2013. Immune response of twin-bearing Merino ewes when infected with Haemonchus contortus: Effects of fat score and prepartum supplementation. Livestock Science. 157: 568-576.

Mantovani A., Cassatella M.A., Costantini C. & Jaillon S. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nature Reviews Immunology. 11: 519-531.

Martínez-Valladares M., Vara-Del Río M.P. & Rojo-Vázquez F.A. 2007. Use of a 203 αα fragment of Tc-PDI to detect IgA activity during infection by Teladorsagiacircumcincta in sheep. Parasitology Research. 100: 1213-1220.

Patten T., Good B., Hanrahan J.P., Mulcahy G. & de Waal T. 2011. Gastrointestinal nematode control practices on lowland sheep farms in Ireland with reference to selection for anthelmintic resistance. Irish Veterinary Journal. 64: 4. [doi:10.1186/2046-0481-64-4].

Prada J. de C.J. Matthews L., Mair C., Stefan T. & Stear M.J. 2014. The transfer of IgA from mucus to plasma and the implications for diagnosis and control of nematode infections. Parasitology. 141: 875-879.

SAS Institute. 2004. SAS/STAT User’s Guide, Version 9.2. Cary, NC. SAS Institute.

Scott I., Pomroy W.E., Kenyon P.R., Smith G., Adlington B. & Moss A. 2013. Lack of efficacy of monepantel against Teladorsagia circumcincta and Trichostrongylus colubriformis. Veterinary Parasitology. 198: 166-171.

Shaw R.J., Gatehouse T.K. & McNeill M.M. 1998. Serum IgE responses during primary and challenge infections of sheep with Trichostrongylus colubriformis. International Journal of Parasitology. 28: 293-302.

Shaw R.J., Morris C.A., Wheeler M., Tate M. & Sutherland I.A. 2012. Salivary IgA: a suitable measure of immunity to gastrointestinal nematodes in sheep. Veterinary Parasitology. 186: 109-117.

Terefe G., Lacroux C., Andréoletti O., Grisez C., Prevot F., Bergeaud J.P., Penicaud J., Rouillon V., Gruner L., Brunel J., Francois D., Bouix J., Dorchies P. & Jacquiet P. 2007. Immune response to Haemonchus contortus infection in susceptible (INRA 401) and resistant (Barbados Black Belly) breeds of lambs. Parasite Immunology. 29: 415-424.

Waghorn T.S., Knight J.S. & Leathwick D.M. 2014. The distribution and anthelmintic resistance status of Trichostrongylus colubriformis, T. vitrinus and T. axei in lambs in New Zealand. New Zealand Veterinary Journal. 62: 152-159.

Williams A.R., Palmer D.G., Williams I.H., Vercoe P.E. & Karlsson L.J.E. 2010. Faecal dry matter, inflammatory cells and antibodies in parasite-resistant sheep challenged with either Trichostrongylus colubriformis or Teladorsagia circumcincta. Veterinary Parasitology. 170: 230-237.




DOI: https://doi.org/10.22456/1679-9216.81178

Copyright (c) 2018 Roberto González Garduño, María Eugenia López Arellano, Pedro Mendoza de Gives, Nadia Florencia Ojeda Robertos, Alfonso Juventino Chay Canul

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.