Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T05:31:39.988Z Has data issue: false hasContentIssue false
  • English
  • Français

Offspring born to ewes fed high salt during pregnancy have altered responses to oral salt loads

Published online by Cambridge University Press:  03 September 2009

S. N. Digby ,
D. G. Masters ,
D. Blache ,
P. I. Hynd  and
D. K. Revell
S. N. Digby*
Affiliation:
Discipline of Agricultural and Animal Science, School of Agriculture, Food and Wine, The University of Adelaide, Roseworthy, SA 5371, Australia Future Farm Industries Cooperative Research Centre M081, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
D. G. Masters
Affiliation:
CSIRO Livestock Industries, Private Bag 5, Wembley, WA 6913, Australia Future Farm Industries Cooperative Research Centre M081, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
D. Blache
Affiliation:
School of Animal Biology M085, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia Future Farm Industries Cooperative Research Centre M081, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
P. I. Hynd
Affiliation:
Discipline of Agricultural and Animal Science, School of Agriculture, Food and Wine, The University of Adelaide, Roseworthy, SA 5371, Australia
D. K. Revell
Affiliation:
Discipline of Agricultural and Animal Science, School of Agriculture, Food and Wine, The University of Adelaide, Roseworthy, SA 5371, Australia CSIRO Livestock Industries, Private Bag 5, Wembley, WA 6913, Australia Future Farm Industries Cooperative Research Centre M081, Faculty of Natural and Agricultural Sciences, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
Get access

Abstract

Prenatal growth is sensitive to the direct and indirect effects of maternal dietary intake; manipulation can lead to behavioural and physiological changes of the offspring later in life. Here, we report on three aspects of how a high-salt diet during pregnancy (conception to parturition) may affect the offspring’s response to high oral salt loads: (i) dietary preferences for salt; (ii) response to salt and water balance and aldosterone and arginine vasopressin (AVP) concentrations after an oral salt challenge; (iii) concentrations of insulin and leptin after an oral salt challenge. We used two groups of lambs born to ewes fed either a high-salt (13% NaCl) diet during pregnancy (S lambs; n = 12) or control animals born to ewes fed a conventional (0.5% NaCl) diet during pregnancy (C lambs; n = 12). Lambs were subjected to short- (5 min) and long-term (24 h) preference tests for a high-salt (13% NaCl) or control diet, and the response to an oral challenge with either water or 25% NaCl solution were also carried out. Weaned lambs born to ewes fed high salt during pregnancy did not differ in their preference for dietary salt, but they did differ in their physiological responses to an oral salt challenge. Results indicate that these differences reflect an alteration in the regulation of water and salt balance as the metabolic hormones, insulin and leptin, were not affected. During the first 2 h after a single salt dose, S lambs had a 25% lower water intake compared to the C lambs. S lambs had, on average, a 13% lower AVP concentration than the C lambs (P = 0.014). The plasma concentration of aldosterone was higher in the S lambs than in the C lambs (P = 0.013). Results suggest that lambs born to ewes that ingest high amounts of salt during pregnancy are programmed to have an altered thirst threshold, and blunted response in aldosterone to oral salt loads.

Keywords

aldosteronearginine vasopressinfoetal programmingsalt intakewater intake
Type
Full Paper
Information
animal , Volume 4 , Issue 1 , January 2010 , pp. 81 - 88
Copyright
Copyright © The Animal Consortium 2009

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

Arguelles, J, Lopez-Sela, P, Brime, JI, Costales, M, Vijande, M 1996. Changes of blood pressure responsiveness in rats exposed in utero and perinatally to a high-salt environment. Regulatory Peptides 66, 113–115.Google Scholar
Australian Standing Committee on Agriculture and Resource Management 1990. Feeding standards for Australian livestock ruminants. CISRO Victoria, Australia.Google Scholar
Blache, D, Grandison, MJ, Masters, DG, Dynes, RA, Blackberry, MA, Martin, GA 2007. Relationships between metabolic endocrine systems and voluntary feed intake in Merino sheep fed a high salt diet. Australian Journal of Experimental Agriculture 47, 544–550.CrossRefGoogle Scholar
Blache, D, Tellam, RL, Chagas, LM, Blackberry, MA, Vercoe, PE, Martin, GB 2000. Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep. Journal of Endocrinology 165, 625–637.Google Scholar
Butler, DG, Pak, SH, Midgely, A, Nemati, B 2002. AT (1) receptor blockade with losartan during gestation in Wistar rats leads to an increase in thirst and sodium appetite in their adult female offspring. Regulatory Peptides 105, 47–57.Google Scholar
Chadwick, MA, Vercoe, PE, Williams, IH, Revell, DK 2009. Programming sheep production on saltbush: adaptations of offspring from ewes that consumed high amounts of salt during pregnancy. Animal Production Science 49, 311–317.Google Scholar
Curtis, KS, Krause, EG, Wong, DL, Contreras, RJ 2004. Gestational and early postnatal dietary NaCl levels affect NaCl intake, but not stimulated water intake, by adult rats. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 286, R1043–R1050.Google Scholar
Dahlquist, RL, Knoll, JW 1978. Inductively coupled plasma-atomic emission spectrometry: analysis of biological material and soils for major, trace and ultra-trace elements. Applied Spectroscopy 32, 1–29.Google Scholar
Desai, M, Guerra, C, Wang, S, Ross, MG 2003. Programming of hypertonicity in neonatal lambs: resetting of threshold for vasopressin secretion. Endocrinology 144, 4332–4337.Google Scholar
Digby, SN, Masters, DG, Blache, D, Blackberry, MA, Hynd, PI, Revell, DK 2008. Reproductive capacity of Merino ewes fed a high-salt diet. Animal 2, 1353–1360.Google Scholar
Ford, SP, Hess, BW, Schwope, MM, Nijland, MJ, Gilbert, JS, Vonnahme, KA, Means, WJ, Han, H, Nathanielsz, PW 2007. Maternal undernutrition during early to mid-gestation in the ewe results in altered growth, adiposity, and glucose tolerance in male offspring. Journal of Animal Science 85, 1285–1294.CrossRefGoogle ScholarPubMed
Gordon, MS, Majzoub, JA, Williams, GH, Gordon, MB 1997. Sodium balance modulates thirst in normal man. Endocrinology Research 23, 377–392.Google Scholar
James, VHT, Wilson, GA 1976. Determination of aldosterone in biological fluids. In Assay of drugs and other trace compounds in biological fluids (ed. E Reid), pp. 149–158. Elsevier Publishing, Amsterdam.Google Scholar
Lindheimer, MD, Barron, WM, Davison, JM 1989. Osmoregulation of thirst and vasopressin release in pregnancy. American Journal of Physiology – Renal Physiology 257, F159–F169.CrossRefGoogle ScholarPubMed
Luther, J, Aitken, R, Milne, J, Matsuzaki, M, Reynolds, L, Redmer, D, Wallace, J 2007. Maternal and fetal growth, body composition, endocrinology, and metabolic status in undernourished adolescent sheep. Biology of Reproduction 77, 343–350.Google Scholar
Martin-Gronert, MS, Ozanne, SE 2006. Maternal nutrition during pregnancy and health of the offspring. Biochemical Society Transactions 34, 779–782.Google Scholar
Masters, DG, Rintoul, AJ, Dynes, RA, Pearce, KL, Norman, HC 2005. Feed intake and production in sheep fed diets high in sodium and potassium. Australian Journal of Agricultural Research 56, 427–434.Google Scholar
McEwen, BS, Wingfield, JC 2007. Allostasis and allostatic load. In Encyclopaedia of Stress (ed. G Fink), pp. 135–141. Academic Press, New York.Google Scholar
McQuaker, NR, Brown, DF, Kluckner, PD 1979. Digestion of environmental materials for analysis by inductively coupled plasma-atomic emission spectrometry. Analytical Chemistry 51, 1082–1084.Google Scholar
Midkiff, EE, Bernstein, IL 1983. The influence of age and experience on salt preference of the rat. Developmental Psychobiology 16, 385–394.Google Scholar
Miller, DW, Blache, D, Martin, GB 1995. The role of intracerebral insulin in the effect of nutrition on gonadotropin secretion in mature male sheep. Journal of Endocrinology 147, 321–329.Google Scholar
Mistretta, CM, Bradley, RM 1983. Neural basis of developing salt taste sensation: response changes in fetal, postnatal and adult sheep. Journal of Comparative Neurology 215, 199–210.Google Scholar
Mohamed, MO, Phillips, CJC 2003. The effect of increasing salt intake of pregnant dairy cows on the salt appetite and growth of their calves. Animal Science 77, 181–185.Google Scholar
Nicolaidis, S, Galaverna, O, Metzler, CH 1990. Extracellular dehydration during pregnancy increases salt appetite of offspring. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 258, R281–R283.CrossRefGoogle ScholarPubMed
Norman, HC, Dynes, RA, Masters, DG 2002. Nutritive value of plants growing on saline land. In Productive use and rehabilitation of saline land, 8th National Conference, Fremantle, Australia, pp. 59–69. Promaco Conventions Pty Ltd, Perth, Western Australia.Google Scholar
Ryan, EA, Liu, D, Bell, RC, Finegood, DT, Crawford, J 1995. Long-term consequences in offspring of diabetes in pregnancy: studies with syngeneic islet-transplanted streptozotocin-diabetic rats. Endocrinology 136, 5587–5592.Google Scholar
da Silva, AA, de Noronha, IL, de Oliveira, IB, Malheiros, DM, Heimann, JC 2003. Renin-angiotensin system function and blood pressure in adult rats after perinatal salt overload. Nutrition, Metabolism and Cardiovascular Disease 13, 133–139.Google Scholar
Simitzis, PE, Deligeorgis, SG, Bizelis, JA, Fegeros, K 2008. Feeding preferences in lambs influenced by prenatal flavour exposure. Physiology and Behavior 93, 529–536.CrossRefGoogle ScholarPubMed
Smriga, M, Kameishi, M, Torii, K 2002. Brief exposure to NaCl during early postnatal development enhances adult intake of sweet and salty compounds. Neuroreport 13, 2565–2569.CrossRefGoogle ScholarPubMed
Spencer, GSG, Robinson, GM 1993. Stimulation of placental, fetal and neonatal growth by thyroxine administration to pregnant rats. Journal of Endocrinology 139, 275–279.Google Scholar
Thomas, DT, Norman, HC, Rintoul, AJ, Wilnot, MG, Master, DG 2006. Using stable carbon isotopes to measure diet selection in sheep grazing saltland pastures. 26th Biennial Conference of the Australian Society of Animal Production, Burswood, Western Australia, Short communication number 61.Google Scholar
Tindal, JS, Knaggs, GS, Hart, IC, Blake, LA 1978. Release of growth hormone in lactating and non-lactating goats in relation to behaviour, stages of sleep, electroencephalograms, environmental stimuli and levels of prolactin, insulin, glucose and free fatty acids in the circulation. Journal of Endocrinology 76, 333–346.Google Scholar
Wallace, JM 2000. Nutrient partitioning during pregnancy: adverse gestational outcome in overnourished adolescent dams. Proceedings of the Nutrition Society 59, 107–117.CrossRefGoogle ScholarPubMed
Webley, L 2007. Archaeological evidence for pastoralist land-use and settlement in Namaqualand over the last 2000 years. Journal of Arid Environments 70, 629–640.Google Scholar
Zygoyiannis, D 2006. Sheep production in the world and in Greece. Small Ruminant Research 62, 143–147.Google Scholar