Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T05:46:36.280Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of nutrition in early pregnancy on the periparturient relaxation of immunity to gastro-intestinal parasitism in prolific ewes

Published online by Cambridge University Press:  18 August 2016

J. Valderrábano  and
J. Uriarte
Get access

Abstract

The rôle of body reserves stored during early pregnancy on the periparturient breakdown of resistance to nematode parasites was investigated. From the 35th day of pregnancy, 46 ewes were distributed in four groups and given access to a lucerne pelleted diet. Two groups were given food at maintenance (M and C) and the other two were offered food either ad libitum (H) or at 0·70 their maintenance requirements (L) in order to achieve three well differentiated levels of body reserves by the 90th day of pregnancy when backfat thickness reached a mean value of 10·6, 7·5, 7·4 and 5·0 mm for H, M, C, and L treatments respectively. After the 90th day of pregnancy all animals were given food at 50 g/kg live weight per day. All ewes in groups H, M and L received 5000 infective larvae per week (40% Teladorsagia circumcincta, 40% Trichostrongylus colubriformis, 20% Haemonchus contortus) from 5 weeks before to 3 weeks after lambing. The animals in group C remained as uninfected controls.

Host resistance, as measured by faecal egg counts, was significantly affected by the nutritional treatment established during early pregnancy, showing a mean excretion of 546, 766 and 1007 eggs per gram (e.p.g. ) for H, M, and L treatments, respectively, until 3 weeks post lambing. This response was accompanied by a significant effect on circulating eosinophils and better fed ewes showed a higher concentration with a maximum mean value of 10·1, 6·9, 5·5 and 4·0 cells per mm3 for H, M, L and C treatments, respectively, 2 weeks post infection. The effect of the worm infection per se was evident in that the lambs of the M treatment ewes grew at 0·90 of the rate of those in the control treatment (189 v. 213 g/day). Ad libitum feeding in early pregnancy appeared to sufficiently compensate for this depressive effect, with the H ewes producing lambs that grew at a rate similar to those of the C ewes (213 v. 213 g/day).

The results support the view that fat mass stored by ewes in early pregnancy is involved in the expression of immunity against gastro-intestinal nematode infection around parturition. Furthermore, the depressive effect of ewes’ infection on lambs’ growth rate can be overcome by increasing the plane of nutrition of their dams. These results have clear implications for grazing animals, particularly their nutritional management in early pregnancy and provide a simple management strategy in sustainable management systems.

Keywords

nematodanutrient reservesnutritionsheep
Type
Ruminant nutrition, behaviour and production
Information
Animal Science , Volume 76 , Issue 3 , June 2003 , pp. 481 - 489
Copyright
Copyright © British Society of Animal Science 2003

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

Agricultural Research Council. 1980. The nutrient requierements of ruminant livestock. Commonwealth Agricultural Bureaux, Slough.Google Scholar
Ahima, R. S., Prabakaran, D., Mantzoros, C., Qu, D., Lowell, B., Maratos Flier, E. and Flier, J. S. 1996. Role of leptin in the neuroendocrine response to fasting. Nature 382: 250–252.Google Scholar
Balic, A., Bowles, V. M. and Meeusen, E. N. T. 2000. The immunobiology of gastrointestinal nematode infections in ruminants. Advances in Parasitology 45: 181–241.Google Scholar
Barger, I. A. 1993. Influence of sex and reproductive status on susceptibility of ruminants to nematode parasitism. International Journal for Parasitology 23: 463–469.Google Scholar
Bonnet, M., Gourdou, I., Leroux, C., Chilliard, Y. and Djiane, J. 2002. Leptin expression in the ovine mammary gland: putative sequential involvement of adipose, epithelial, and myoepithelial cells during pregnancy and lactation. Journal of Animal Science 80: 723–728.CrossRefGoogle ScholarPubMed
Brunsdon, R. V. 1966. Importance of the ewe as a source of trichostrongyle infection for lambs: control of the spring-rise phenomenon by single post-lambing anthelmintic treatment. New Zealand Veterinary Journal 14: 118–125.Google Scholar
Brunsdon, R. V. 1970. The spring-rise phenomenon: seasonal changes in the worm burdens of breeding ewes and in the availability of pasture infection. New Zealand Veterinary Journal 18: 47–54.Google Scholar
Campfield, L. A., Smith, F. J., Guisez, Y., Devos, R. and Burn, P. 1995. Recombinant mouse OB protein: evidence for a peripheral signal linking adiposity and central neural networks. Science 269: 546–549.Google Scholar
Delfa, R., Teixeira, A. and Colomer-Rocher, F. 1991. Cold carcass weight, fat thickness, C measurement and longissimus dorsi depth for predicting the carcass composition of Rasa Aragonesa ewes with different body condition score. Options Méditerranéennes 13: 19–24.Google Scholar
Diaz-Torga, G.S, Mejía, M. E., Gonzalez-Iglesias, A., Formía, N., Becú-Villalobos, D. and Lacau-Mengido, I. M. 2001. Metabolic cues for puberty onset in free grazing Holstein heifers naturally infected with nematodes. Theriogenology 56: 111–122.Google Scholar
Donaldson, J., Houtert, M. F. J. van and Sykes, A. R. 1998. The effect of nutrition on the periparturient parasite status of mature ewes. Animal Science 67: 523–533.Google Scholar
Douvres, F. W. 1957. Keys to the identification and differentiation to the immature parasitic stages of gastrointestinal nematodes of cattle. American Journal of Veterinary Research 18: 81–85.Google Scholar
Falcone, F. H., Pritchard, D. I. and Gibbs, B. F. 2001. Do basophils play a role in immunity against parasites? Tr ends in Parasitology 17: 126–129.CrossRefGoogle ScholarPubMed
Ferre, I., Brusa, C. M., Manzanera, E., Rojo-Vazquez, F.A, Buratovich, O. F. and Mantecon, A. R. 1995. Effect of supplementary feeding on the gastrointestinal strongylid eggs shedding in grazing pregnant Merino ewes. Journal of Animal and Feed Sciences 4: 237–245.Google Scholar
Garcia-Perez, A.L, Oregui, L. M., Bravo, M. V., Muñoyerro, A., Povedano, I. and Juste, R. A. 1994. Influencia del nivel de alimentación en el desarrollo de la infestación por nematodos gastrointestinales en ovejas adultas en el periparto y lactación. ITEA 90 A: 139–147.Google Scholar
Gasbarre, L. C. 1987. Recovery of third stage larvae of Ostertagia ostertagi from the abomasa of experimentally inoculated calves by prolonged saline incubation. Proceedings of the Helminthology Society, Washington, vol. 54, pp. 160–161.Google Scholar
Gibbs, H. C. and Barger, I. A. 1986. Haemonchus contortus and other trichostrongylid infections in parturient, lactating and dry ewes. Veterinary Parasitology 22: 57–66.Google Scholar
Houdijk, J. G. M., Kyriazakis, I., Coop, R. L. and Jackson, F. 2001a. The expression of immunity to Teladorsagia circumcincta in ewes and its relationship to protein nutrition depend on body protein reserves. Parasitology 122: 661–672.Google Scholar
Houdijk, J. G. M., Kyriazakis, I., Jackson, F. and Coop, R. L. 2001b. The relationship between protein nutrition, reproductive effort and breakdown in immunity to Teladorsagia circumcincta in periparturient ewes. Animal Science 72: 595–606.Google Scholar
Jackson, F., Jackson, E. and Williams, J. T. 1988. Susceptibility of the pre-parturient ewe to infection with Trichostrongylus vitrinus and Ostertagia circumcincta. Research in Veterinary Science 45: 213–218.Google Scholar
Kerboeuf, D. 1979. Le dosage du pepsinogene sanguin element de diagnostic dans les strongyloses gastriques des ruminants. Revue de Médecine Vétérinaire 130: 1365–1370.Google Scholar
Koski, K. G., Su, Z. and Scott, M. E. 1999. Energy deficits suppress both systemic and gut immunity during infection. Biochemical and Biophysical Research Communications 264: 796–801.Google Scholar
Laud, K. I., Gourdou, I., Belair, L., Keisler, D. H. and Djiane, J. 1999. Detection and regulation of leptin receptor mRNA in ovine mammary epithelial cells during pregnancy and lactation. FEBS Letters 463: 194–198.Google Scholar
Leyva, V., Henderson, A. E. and Sykes, A. R. 1982. The effect of daily infection with Ostertagia circumcincta larvae on food intake, milk production and wool growth in sheep. Journal of Agricultural Science, Cambridge 99: 249–259.Google Scholar
Lord, G. M. 2002. Role of leptin in immunology. Nutrition Reviews 60: S35–S38.CrossRefGoogle ScholarPubMed
Lord, G. M., Matarese, G., Howard, J. K., Baker, R. J., Bloom, S. R. and Lechler, R. I. 1998. Leptin modulates the T cell immune response and reverses starvation-induced immunosuppression. Nature 394: 897–901.Google Scholar
McAnulty, R. W., Familton, A. S., Sedcole, R. D. and Sykes, A. R. 2001. Changes in the resistance of the ewe to infection with Teladorsagia circumcincta during late pregnancy and lactation. Animal Science 72: 159–168.Google Scholar
Matarese, G. 2000. Leptin and the immune system: how nutritional status influences the immune response. European Cytokine Network 11: 7–13.Google Scholar
Meeusen, E. N. T. and Balic, A. 2000. Do eosinophils have a role in the killing of helminth parasites? Parasitology Today 16: 95–101.Google Scholar
Mercer, J. G., Mitchell, P. I., Moar, K. M., Bissett, A., Geissler, S., Bruce, K. and Chappell, L. H. 2000. Anorexia in rats infected with the nematode Nippostrongylus brasiliensis: experimental manipulations. Parasitology 120: 641–647.Google Scholar
Ministry of Agriculture, Fisheries and Food. 1971. Manual of veterinary parasitolgical laboratory techniques. Technical bulletin no. 18. Her Majesty’s Stationery Office, London.Google Scholar
Oldham, J. D. and Alderman, G. 1982. Recent advances in understanding protein-energy interrelationships in intermediary metabolism of ruminants. In Protein and energy supply for high production of milk and meat, pp. 33–63. Pergamon Press, Oxford.Google Scholar
O’Sullivan, B. M. and Donald, A. D. 1973. Responses to infection with Haemonchus contortus and Trichostrongylus colubriformis in ewes of different reproductive status. International Journal for Parasitology 3: 521–530.Google Scholar
Raynaud, J. P. 1970. Etude de l’effecacite d’une technique de coproscopie quantitative pour le diagnostique de routine et le controle des infestations de bovins, ovins, equines et porcins. Annales de Parasitologie Humaine et Comparée 45: 321–342.Google Scholar
Roberts, H. C., Hardie, L. J., Chappell, L. H. and Mercer, J. G. 1999. Parasite-induced anorexia: leptin, insulin and corticosterone responses to infection with the nematode, Nippostrongylus bresiliensis. Parasitology 118: 117–123.Google Scholar
Rose, J. H. 1969. The development of the parasitic stages of Ostertagia ostertagi . Journal of Helminthology 43: 173–184.CrossRefGoogle ScholarPubMed
Russel, A. J. F., Doney, J. M. and Gunn, R. G. 1969. Subjective assessment of body fat in live sheep. Journal of Agricultural Science, Cambridge 72: 451–454.Google Scholar
Statistical Analysis Systems Institute. 1998. Statview. SAS Institute Inc., Cary, NC.Google Scholar
Thomas, R. J. and Ali, D. A. 1983. The effect of Haemonchus contortus infection on the pregnant and lactating ewes. International Journal for Parasitology 13: 393–398.Google Scholar
Uriarte, J. and Valderrábano, J. 1990. Grazing management strategies for the control of parasitic diseases in intensive sheep production systems. Veterinary Parasitology 37: 243–255.Google Scholar
Valderrábano, J., Delfa, R. and Uriarte, J. 2002. Effect of level of feed intake on the development of gastrointestinal parasitism in growing lambs. Veterinary Parasitology 104: 327–338.Google Scholar