Effects of low and high protein:Carbohydrate ratios in the diet of pregnant gilts on maternal cortisol concentrations and the adrenocortical and sympathoadrenal reactivity in their offspring

Journal of Animal Science

Volumn 91, Issue 6, 2013, Pages 2680-2692

  Otten, W ^a   Kanitz, E ^a   Tuchscherer, M ^a   Grabner M ^a   Nurnberg G ^b   Bellmann, O ^c   Hennig, U ^d   Rehfeldt, C ^e   Metges, C C ^d  

^a Behavioral Physiology   (Germany)

^b Research Unit Genetics and Biometry   (Germany)

^c Research Units   (Germany)

^d Leibniz Institute for Farm Animal Biology Institute of Nutritional Physiology 'Oskar Kellner'   (Germany)

^e LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

Author keywords

Catecholamine; Cortisol; Glucocorticoid receptor; Pigs; Pregnancy; Protein intake

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CATECHOLAMINE; GLUCOCORTICOID; HYDROCORTISONE;

ADRENAL MEDULLA; ANIMAL; ANIMAL FOOD; ARTICLE; BLOOD; CARBOHYDRATE DIET; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; FEMALE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; MALE; METABOLISM; PARITY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PREGNANCY; PROTEIN INTAKE; RANDOMIZED CONTROLLED TRIAL; SWINE;

ADRENAL MEDULLA; ANIMAL FEED; ANIMALS; CATECHOLAMINES; DIETARY CARBOHYDRATES; DIETARY PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GLUCOCORTICOIDS; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; NEUROTRANSMITTER AGENTS; PARITY; PITUITARY-ADRENAL SYSTEM; PREGNANCY; STRESS, PHYSIOLOGICAL; SUS SCROFA;

EID: 84882714792     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2012-6080     Document Type: Article

References (46)

1. Allolio, B., J. Hoffmann, E. A. Linton, W. Winkelmann, M. Kusche, and H. M. Schulte. 1990. Diurnal salivary cortisol patterns during pregnancy and after delivery: Relationship to plasma cortiocotrophin-releasing-hormone. Clin. Endocrinol. 33:279-289.
2. Berridge, C. W. 2008. Noradrenergic modulation of arousal. Brain Res. Rev. 58:1-17.
3. Berridge, C. W., and B. D. Waterhouse. 2003. The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Res. Brain Res. Rev. 42:33-84.
4. Bertram, C., A. R. Trowern, N. Copin, A. A. Jackson, and C. B. Whorwood. 2001. The maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11β-hydroxysteroid dehydrogenase: Potential molecular mechanisms underlying the programming of hypertension in utero. Endocrinology 142:2841-2853.
5. Chadio, S. E., B. Kotsampasi, G. Papadomichelakis, S. Deligeorgis, D. Kalogiannis, I. Menegatos, and G. Zervas. 2007. Impact of maternal undernutrition on the hypothalamic-pituitary-adrenal axis responsiveness in sheep at different ages postnatal. J. Endocrinol. 192:495-503.
6. de Kloet, E. R., E. Vreugdenhil, M. S. Oitzl, and M. Joels. 1998. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19:269-301.
7. DeRosa, M. A., and P. E. Cryer. 2004. Hypoglycemia and the sympathoadrenal system: Neurogenic symptoms are largely the result of sympathetic neural, rather than adrenomedullary, activation. Am. J. Physiol. Endocrinol. Metab. 287: E32-E41.
8. Edwards, L. J., and I. C. McMillen. 2001. Maternal undernutrition increases arterial blood pressure in the sheep fetus during late gestation. J. Physiol. 533:561-570.
9. Félix, B., M. E. Léger, and D. Albe-Fessard. 1999. Stereotaxic atlas of the pig brain. Elsevier Science B.V., Amsterdam, The Netherlands.
10. Fernandez-Twinn, D. S., S. Ekizoglou, A. Waymann, C. J. Petry, and S. E. Ozanne. 2006. Maternal low-protein diet programs cardiac β-adrenergic response and signalling in 3-mo-old male offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291:R429-R436.
11. GfE (Gesellschaft für Ernährungsphysiologie). 2006. Empfehlungen zur Energie-und Nährstoffversorgung von Schweinen (Recommendations of energy and nutrient intake in pigs). DLG-Verlags-GmbH, Frankfurt am Main, Germany.
12. Guzik, A. C., J. O. Matthews, B. J. Kerr, T. D. Bidner, and L. L. Southern. 2006. Dietary tryptophan effects on plasma and salivary cortisol and meat quality in pigs. J. Anim. Sci. 84:2251-2259.
13. Hay, M., M. C. Meunier-Salaün, F. Brulaud, M. Monnier, and P. Mormède. 2000. Assessment of hypothalamic-pituitary-adrenal axis and sympathetic nervous system activity in pregnant sows through the measurement of glucocorticoids and catecholamines in urine. J. Anim. Sci. 78:420-428.
14. Henry, Y., B. Sève, A. Mounier, and P. Ganier. 1996. Growth performance and brain neurotransmitters in pigs as affected by tryptophan, protein, and sex. J. Anim. Sci. 74:2700-2710.
15. Herbert, D. C., and A. J. Carrillo. 1982. The hypophyseal-adrenal axis in the protein-calorie malnourished rat. Horm. Metab. Res. 14:205-207.
16. Huizink, A. C., E. J. H. Mulder, and J. K. Buitelaar. 2004. Prenatal stress and risk for psychopathology: Specific effects of induction of general susceptibility? Psychol. Bull. 130:115-142.
17. Jacobson, L., D. Zurakowski, and J. A. Majzoub. 1997. Protein malnutrition increases plasma adrenocorticotropin and anterior pituitary proopiomelanocortin messenger ribonucleic acid in the rat. Endocrinology 138:1048-1057.
18. Kanitz, E., G. Manteuffel, and W. Otten. 1998. Effects of weaning and restraint stress on glucocorticoid receptor binding capacity in limbic areas of domestic pigs. Brain Res. 804:311-315.
19. Kanitz, E., W. Otten, and M. Tuchscherer. 2006. Changes in endocrine and neurochemical profiles in neonatal pigs prenatally exposed to increased maternal cortisol. J. Endocrinol. 191:207-220.
20. Kanitz, E., W. Otten, M. Tuchscherer, M. Gräbner, K. P. Brüssow, C. Rehfeldt, and C. C. Metges. 2012. High and low protein: Carbohydrate dietary ratios during gestation alter materno-fetal cortisol regulation in pigs. PLoS ONE 7:e52748.
21. Kanitz, E., W. Otten, M. Tuchscherer, and G. Manteuffel. 2003. Effects of prenatal stress on corticosteroid receptor binding and monoamine levels in limbic areas of neonatal pigs at different ages. J. Vet. Med. A 50:132-139.
22. Kanitz, E., M. Tuchscherer, A. Tuchscherer, B. Stabenow, and G. Manteuffel. 2002. Neuroendocrine and immune responses to acute endotoxemia in suckling and weaned piglets. Biol. Neonate 81:203-209.
23. Kattesh, H. G. G., G. A. Baumbach, B. E. Gillespie, J. F. Schneider, and J. T. Murai. 1997. Distribution between protein-bound and free forms of plasma cortisol in the gilt and fetal pig near term. Biol. Neonate 72:192-200.
24. Koopmans, S. J., M. Ruis, R. Dekker, H. van Diepen, M. Korte, and Z. Mroz. 2005. Surplus dietary tryptophan reduces plasma cortisol and noradrenaline concentrations and enhances recovery after social stress in pigs. Physiol. Behav. 85:469-478.
25. Laborie, C., O. Molendi-Coste, C. Breton, V. Montel, F. Vandenbulcke, L. Grumolato, Y. Anouar, and D. Vieau. 2011. Maternal perinatal undernutrition has long-term consequences on morphology, function and gene expression of the adrenal medulla in the adult male rat. J. Neuroendocrinol. 23:711-724.
26. Langley-Evans, S. C. 2009. Nutritional programming of disease: Unravelling the mechanism. J. Anat. 215:36-51.
27. Langley-Evans, S. C., D. S. Gardner, and A. A. Jackson. 1996. Maternal protein restriction influences the programming of the rat hypothalamic-pituitary-adrenal axis. J. Nutr. 126:1578-1585.
28. Lesage, J., B. Blondeau, M. Grino, B. Bréant, and J. P. Dupouy. 2001. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology 142:1692-1702.
29. Lesage, J., N. Sebaai, M. Leonhardt, I. Dutriez-Casteloot, C. Breton, S. Deloof, and D. Vieau. 2006. Perinatal maternal undernutrition programs the offspring hypothalamo-pituitary-adrenal (HPA) axis. Stress 9:183-198.
30. Lindsay, J. R., and L. K. Nieman. 2005. The hypothalamic-pituitary-adrenal axis in pregnancy: Challenges in disease detection and treatment. Endocr. Rev. 26:775-799.
31. Lowry, O. H., N. J. Rosebrough, A. L. Farr, and R. J. Randall. 1951. Protein measurement with Folin reagent. J. Biol. Chem. 193:265-275.
32. McMillen, C., and J. S. Robinson. 2005. Developmental origins of the metabolic syndrome: Prediction, plasticity, and programming. Physiol. Rev. 85:571-633.
33. Metges, C. C., I. S. Lang, S. Goers, P. Junghans, U. Hennig, B. Stabenow, F. Schneider, W. Otten, and C. Rehfeldt 2009. Inadequate protein levels during gestation in gilts affect gestation body mass and fatness as well as offspring birth weight and insulin sensitivity at 10 wk of age. J. Anim. Sci. 87(E-Suppl. 2):503-504. (Abstr.)
34. Metges, C. C., I. S. Lang, U. Hennig, K. P. Brüssow, E. Kanitz, M. Tuchscherer, F. Schneider, J. M. Weitzel, A. Steinhoff-Ooster, H. Sauerwein, O. Bellmann, G. Nürnberg, C. Rehfeldt, and W. Otten. 2012. Intrauterine growth retarded progeny of pregnant sows fed high protein:low carbohydrate diet is related to metabolic energy deficit. PLoS ONE 7:e31390.
35. Metges, C. C., K. J. Petzke, G. Backes, U. Hennig, A. Elsner, M. Derno, P. Junghans, and G. Nürnberg. 2005. Response to lysine in a wheat gluten diet in adult minipigs after short-and long-term dietary adaptation as assessed with an indicator amino acid oxidation and balance technique. J. Anim. Sci. 83:833-841.
36. Metzler-Zebeli, B. U., I. S. Lang, S. Görs, K. P. Brüssow, U. Hennig, G. Nürnberg, C. Rehfeldt, W. Otten, and C. C. Metges. 2012. High protein-low carbohydrate diet during pregnancy alters maternal plasma amino acid concentration and placental amino acid extraction but not fetal plasma amino acids in pigs. Brit. J. Nutr. 108:2176-2189.
37. Mokler, D. J., O. I. Torres, J. R. Galler, and P. J. Morgane. 2007. Stress-induced changes in extracellular dopamine and serotonin in the medial prefrontal cortex and dorsal hippocampus of prenatally malnourished rats. Brain Res. 1148:226-233.
38. Molendi-Coste, O., L. Grumolato, C. Laborie, J. Lesage, E. Maubert, H. Ghzili, H. Vaudry, Y. Anouar, C. Breton, and D. Vieau. 2006. Maternal perinatal undernutrition alters neuronal and neuroendocrine differentiation in the rat adrenal medulla at weaning. Endocrinology 147:3050-3059.
39. Molendi-Coste, O., C. Laborie, M. C. Scarpa, V. Montel, D. Vieau, and C. Breton. 2009. Maternal perinatal undernutrition alters postnatal development of chromaffin cells in the male rat adrenal medulla. Neuroendocrinology 90:54-66.
40. Otten, W., E. Kanitz, D. Couret, I. Veissier, A. Prunier, and E. Merlot. 2010. Maternal social stress during late pregnancy affects hypothalamic-pituitary-adrenal function and brain neurotransmitter systems in pig offspring. Domest. Anim. Endocrinol. 38:146-156.
41. Pastuszewska, B., D. Tomaszewska-Zaremba, L. Buraczewska, E. Świech, and M. Taciak. 2007. Effects of supplementing pig diets with tryptophan and acidifier on protein digestion and deposition, and on brain serotonin concentrations in young pigs. Anim. Feed Sci. Technol. 132:49-65.
42. Petry, C. J., M. W. Dorling, C. L. Wang, D. B. Pawlak, and S. E. Ozanne. 2000. Catecholamine levels and receptor expression in low protein rat offspring. Diabet. Med. 17:848-853.
43. Rehfeldt, C., I. S. Lang, S. Görs, U. Hennig, C. Kalbe, B. Stabenow, K. P. Brüssow, R. Pfuhl, O. Bellmann, G. Nürnberg, W. Otten, and C. C. Metges. 2011. Limited and excess dietary protein during gestation affects growth and compositional traits in gilts and impairs offspring fetal growth. J. Anim. Sci. 89:329-341.
44. Rehfeldt, C., L. Lefaucheur, J. Block, B. Stabenow, R. Pfuhl, W. Otten, C. C. Metges, and C. Kalbe. 2012. Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets. Eur. J. Nutr. 51:151-165.
45. Takahashi, L. K., J. G. Turner, and N. H. Kalin. 1992. Prenatal stress alters brain catecholaminergic activity and potentiates stress-induced behavior in adult rats. Brain Res. 574:131-137.
46. Valentino, R. J., and E. Van Bockstaele. 2008. Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur. J. Pharmacol. 583:194-203.