Effects of inadequate maternal dietary protein: Carbohydrate ratios during pregnancy on offspring immunity in pigs

BMC Veterinary Research

Volumn 8, Issue , 2012, Pages

  Tuchscherer, Margret ^a   Otten, Winfried ^a   Kanitz, Ellen ^a   Gräbner, Maria ^a   Tuchscherer, Armin ^a   Bellmann, Olaf ^a   Rehfeldt, Charlotte ^a   Metges, Cornelia C ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); SUIDAE;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; CARBOHYDRATE DIET; DIET; FEMALE; FETUS DEVELOPMENT; IMMUNOLOGY; MALNUTRITION; MATERNAL NUTRITION; PREGNANCY; PROTEIN INTAKE; SWINE;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; DIET; DIETARY CARBOHYDRATES; DIETARY PROTEINS; FEMALE; FETAL DEVELOPMENT; MALNUTRITION; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; PREGNANCY; SWINE;

EID: 84870056022     PISSN: None     EISSN: 17466148     Source Type: Journal    
DOI: 10.1186/1746-6148-8-232     Document Type: Article

References (60)

1. Shanks N, Lightman SL. The maternal-neonatal neuro-immune interface: are there long-term implications for inflammatory or stress-related disease?. J Clin Invest 2001, 108:1567-1573. 200999, 11733549.
2. Seckl JR, Meaney MJ. Glucocorticoid programming. Ann N Y Acad Sci 2004, 1032:63-84. 10.1196/annals.1314.006, 15677396.
3. Beydoun H, Saftlas AF. Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence. Paediatr Perinat Epidemiol 2009, 22:438-466.
4. Viltart O, Vanbesien-Mailliot CC. Impact of prenatal stress on neuroendocrine programming. Scientific World Journal 2007, 7:1493-1537.
5. Merlot E, Couret D, Otten W. Prenatal stress, fetal imprinting and immunity. Brain Behav Immun 2008, 22:42-51.
6. Kanitz E, Otten W, Tuchscherer M, Manteuffel G. Effects of prenatal stress on corticosteroid receptors and monoamine concentrations in limbic areas of suckling piglets (Sus scrofa). J Vet Med A 2003, 50:132-139.
7. Otten W, Kanitz E, Couret D, Veissier I, Prunier A, Merlot E. Maternal social stress during late pregnancy affects hypothalamic-pituitary-adrenal function and brain neurotransmitter systems in pig offspring. Domest Anim Endocrinol 2010, 38:146-156. 10.1016/j.domaniend.2009.09.002, 19879712.
8. Tuchscherer M, Kanitz E, Otten W, Tuchscherer A. Effects of prenatal stress on cellular and humoral immune responses in neonatal pigs. Vet Immunol Immunopathol 2002, 86:195-203. 10.1016/S0165-2427(02)00035-1, 12007885.
9. Couret D, Jamin A, Kuntz-Simon G, Prunier A, Merlot E. Maternal stress during late gestation has moderate but long-lasting effects on the immune system of the piglets. Vet Immunol Immunopathol 2009, 131:17-24. 10.1016/j.vetimm.2009.03.003, 19362376.
10. Hausmann MF, Carroll JA, Weesner GD, Daniels MJ, Matteri RL, Lay DC. Administration of ACTH to restrained, pregnant sows alters their pigs′ hypothalamic-pituitary-adrenal (HPA) axis. J Anim Sci 2000, 78:2399-2411.
11. Jarvis S, Moinard C, Robson SK, Baxter E, Ormandy E, Douglas AJ, Seckl JR, Russell JA, Lawrence AB. Programming the offspring of the pig by prenatal social stress: neuroendocrine activity and behaviour. Horm Behav 2006, 49:68-80. 10.1016/j.yhbeh.2005.05.004, 15961089.
12. de Groot J, Kranendonk G, Fillerup M, Hopster H, Boersma W, Hodgson D, van Reenen K, Taverne M. Response to LPS in female offspring from sows treated with cortisol during pregnancy. Physiol Behav 2007, 90:612-618. 10.1016/j.physbeh.2006.11.013, 17261319.
13. Collier CT, Williams PN, Carroll JA, Welsh TH, Laurenz JC. Effect of maternal restraint stress during gestation on temporal lipopolysaccharide-induced neuroendocrine and immune responses of progeny. Domest Anim Endocrinol 2011, 40:40-50. 10.1016/j.domaniend.2010.08.005, 2996048, 20932703.
14. Pond WG, Maurer RR, Mersmann HJ, Cummins S. Response of fetal and newborn piglets to maternal protein restriction during early or late pregnancy. Growth Dev Aging 1992, 56:115-127.
15. Rehfeldt C, Lang IS, Görs S, Hennig U, Kalbe C, Stabenow B, Brüssow KP, Pfuhl R, Bellmann O, Nürnberg G, Otten W, Metges CC. Limited and excess dietary protein during gestation affects growth and compositional traits in gilts and impairs offspring fetal growth. J Anim Sci 2011, 89:329-341. 10.2527/jas.2010-2970, 20889684.
16. Rehfeldt C, Lefaucheur L, Block J, Stabenow B, Pfuhl R, Otten W, Metges CC, Kalbe C. 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 2012, 51:151-165. 10.1007/s00394-011-0201-8, 21559991.
17. Metges CC, Lang IS, Hennig U, Brüssow KP, Kanitz E, Tuchscherer M, Schneider F, Weitzel JM, Steinhoff-Ooster A, Sauerwein H, Bellmann O, Nürnberg G, Rehfeldt C, Otten W. Intrauterine growth retarded progeny of pregnant sows fed high protein: carbohydrate diet is related to metabolic energy deficit. PLoS One 2012, 7:e31390. 10.1371/journal.pone.0031390, 3273459, 22328932.
18. Varela P, Muñoz-Martínez E, Marcos A, Unzaga MT. Influence of dietary protein levels on the electrophoretic pattern and plasma IgG and IgM levels in pregnant rats and their offspring. Arch Latinoam Nutr 1988, 38:219-228.
19. Calder PC, Yaqoob P. The level of protein and type of fat in the diet of pregnant rats both affect lymphocyte function on the offspring. Nutr Res 2000, 20:995-1005.
20. Wu G, Bazer FW, Wallace JM, Spencer TE. Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci 2006, 84:2316-2337. 10.2527/jas.2006-156, 16908634.
21. Tuchscherer M, Puppe B, Tuchscherer A, Tiemann U. Early identification of neonates at risk: traits of newborn piglets with respect to survival. Theriogenology 2000, 54:371-388. 10.1016/S0093-691X(00)00355-1, 11051321.
22. Foisnet A, Farmer C, David C, Quesnel H. Relationships between colostrum production by primiparous sows and sow physiology around parturition. J Anim Sci 2010, 88:1672-1683. 10.2527/jas.2009-2562, 20118422.
23. Barker DJ. A new model for the origins of chronic disease. Med Health Care Philos 2001, 4:31-35. 10.1023/A:1009934412988, 11315417.
24. Langley-Evans SC. Nutritional programming of disease: unravelling the mechanism. J Anat 2009, 215:36-51. 10.1111/j.1469-7580.2008.00977.x, 2714637, 19175805.
25. Langley-Evans SC. Developmental programming of health and disease. Proc Nutr Soc 2006, 65:97-105. 10.1079/PNS2005478, 1885472, 16441949.
26. Daenzer M, Ortmann S, Klaus S, Metges CC. Prenatal high protein exposure decreases energy expenditure and increases adiposity in young rats. J Nutr 2002, 132:142-144.
27. GfE (Gesellschaft für Ernährungsphysiologie) Empfehlungen zur Energie- und Nährstoffversorgung von Schweinen (Recommendations of energy and nutrient intake in pigs) 2006, Frankfurt am Main: DLG-Verlags-GmbH, GfE (Gesellschaft für Ernährungsphysiologie).
28. Tuchscherer M, Kanitz E, Puppe B, Tuchscherer A, Viergutz T. Changes in endocrine and immune responses of neonatal pigs exposed to a psychosocial stressor. Res Vet Sci 2009, 87:380-388. 10.1016/j.rvsc.2009.04.010, 19433330.
29. Löhrke B, Derno M, Krüger B, Viergutz T, Matthes HD, Jentsch W. Expression of sulphonylurea receptors in bovine monocytes from animals with a different metabolic rate. Eur J Physiol 1997, 434:712-720.
30. SAS Institute Inc SAS/STAT® 9.2 User's Guide 2009, NC: SAS Institute Inc, Cary, SAS Institute Inc.
31. Chandra RK. Nutrition and the immune system from birth to old age. Eur J Clin Nutr 2002, 56(Suppl 3):73-76.
32. Calder PC, Jackson AA. Undernutrition, infection and immune function. Nutr Res Rev 2000, 13:3-29. 10.1079/095442200108728981, 19087431.
33. Atinmo T, Baldijao C, Pond WG, Barnes RH. Prenatal and postnatal protein malnutrition in pigs: effects on growth rate, serum protein and albumin. J Anim Sci 1976, 43:606-612.
34. Chandra RK, Kumari S. Nutrition and immunity: an overview. J Nutr 1994, 124(Suppl 8):1433-1435.
35. Klobasa F, Habe F, Werhahn E, Butler JE. Changes in the concentrations of serum IgG, IgA and IgM of sows throughout the reproductive cycle. Vet Immunol Immunopathol 1985, 10:341-353. 10.1016/0165-2427(85)90023-6, 3832574.
36. Le Dividich J, Rooke JA, Herpin P. Nutritional and immunological importance of colostrum for the new-born pig. J Agric Sci 2005, 143:469-485.
37. Butler JE, Zhao Y, Sinkora M, Wertz N, Kacskovics I. Immunoglobulins, antibody repertoire and B cell development. Dev Comp Immunol 2009, 33:321-333. 10.1016/j.dci.2008.06.015, 18804488.
38. Lay DC, Kattesh HG, Cunnick JE, Daniels MJ, McMunn KA, Toscano MJ, Roberts MP. Prenatal stress effects on pig development and response to weaning. J Anim Sci 2008, 86:1316-1324. 10.2527/jas.2007-0812, 18272847.
39. Machado-Neto R, Graves CN, Curtis SE. Immunglobulins in piglets from sows heat-stressed prepartum. J Anim Sci 1987, 65:445-455.
40. Bate LA, Ireland W, Connell BJ, Grimmelt B. Development of the small intestine of piglets in response to prenatal elevation of glucocorticoids. Histol Histopath 1991, 6:207-216.
41. Kanitz E, Gräbner M, Tuchscherer M, Brüssow KP, Stabenow B, Rehfeldt C, Metges CC, Otten W. An inadequate maternal protein diet during pregnancy in pigs alters the expression of corticosteroid receptors and 11β-hydroxysteroid dehydrogenase isoforms in the placenta and fetal brain [abstract]. Endocr Abstr 2010, 22:P261.
42. Edwards SA. Perinatal mortality in the pig: environmental or physiological solutions?. Livest Prod Sci 2002, 78:3-12.
43. Salmon H, Berri M, Gerdts V, Meurens F. Humoral and cellular factors of maternal immunity in swine. Dev Comp Immunol 2009, 33:384-393. 10.1016/j.dci.2008.07.007, 18761034.
44. Levast B, de Monte M, Chevaleyre C, Melo S, Berri M, Mangin F, Zanello G, Lantier I, Salmon H, Meurens F. Ultra-early weaning in piglets results in low serum IgA concentration and IL17 mRNA expression. Vet Immunol Immunopathol 2010, 137:261-268. 10.1016/j.vetimm.2010.06.004, 20591504.
45. Coe CL, Kramer M, Kirschbaum C, Netter P, Fuchs E. Prenatal stress diminishes the cytokine response of leukocytes to endotoxin stimulation in juvenile rhesus monkeys. J Clin Endocrinol Metab 2002, 87:675-681. 10.1210/jc.87.2.675, 11836303.
46. Otten W, Kanitz E, Tuchscherer M, Puppe B, Nürnberg G. Repeated administrations of adrenocorticotropic hormone during gestation in gilts: effects on growth, behaviour and immune responses of their piglets. Livest Sci 2007, 106:261-270.
47. Becker BA, Misfeldt ML. Evaluation of the mitogen-induced proliferation and cell surface differentiation antigens of lymphocytes from pigs 1 to 30 days of age. J Anim Sci 1993, 71:2073-2078.
48. Bauer ME, Perks P, Lightman SL, Shanks N. Restraint stress is associated with changes in glucocorticoid immunoregulation. Physiol Behav 2001, 73:525-532. 10.1016/S0031-9384(01)00503-0, 11495656.
49. Stowell JR, Kiecolt-Glaser JK, Glaser R. Perceived stress and cellular immunity: when coping counts. J Behav Med 2001, 24:323-339. 10.1023/A:1010630801589, 11523331.
50. Lo DY, Lee WM, Chien MS, Lin CC, Lee WC. Effects of dexamethasone on peripheral blood mononuclear cell phenotype in weanling piglets. Comp Immunol Microbiol Infect Dis 2005, 28:251-258. 10.1016/j.cimid.2005.03.001, 15896844.
51. Degabriele R, Fell LR. Changes in behaviour, cortisol and lymphocyte types during isolation and group confinement of sheep. Immunol Cell Biol 2001, 79:583-589. 10.1046/j.1440-1711.2001.01040.x, 11903617.
52. Herbert TB, Cohen S. Stress and immunity in humans: a meta-analytic review. Psychosom Med 1993, 55:364-379.
53. Zorrilla EP, Luborsky L, McKay JR, Rosenthal R, Houldin A, Tax A, McCorkle R, Seligman DA, Schmidt K. The relationship of depression and stressors to immunological assays: a meta-analytic review. Brain Behav Immun 2001, 15:199-226. 10.1006/brbi.2000.0597, 11566046.
54. Webel DM, Fink BN, Baker DH, Johnson RW. Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. J Anim Sci 1997, 75:1514-1520.
55. Williams PN, Collier CT, Carroll JA, Welsh TH, Laurenz JC. Temporal pattern and effect of sex on lipopolysaccharide-induced stress hormone and cytokine response in pigs. Dom Anim Endocrinol 2009, 37:139-147.
56. Blume J, Douglas SD, Evans DL. Immune suppression and immune activation in depression. Brain Behav Immun 2011, 25:221-229. 10.1016/j.bbi.2010.10.008, 3025086, 20955778.
57. Saxton KB, John-Henderson N, Reid MW, Francis DD. The social environment and IL-6 in rats and humans. Brain Behav Immun 2011, 25:1617-1625. 10.1016/j.bbi.2011.05.010, 3191259, 21640816.
58. Hack CE, Aarden LA, Thijs LG. Role of cytokines in sepsis. Adv Immunol 1997, 66:101-195.
59. Moore KW, De Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annnu Rev Immunol 2001, 19:683-765.
60. Schippers EF, Van't Veer C, Van Voorden S, Martina CAE, Huizinga TWJ, Le Cessie S, Van Dissel JT. IL-10 and toll-like receptor-4 polymorphisms and in vivo and ex vivo response to endotoxin. Cytokine 2005, 29:215-228. 10.1016/j.cyto.2004.12.005, 15760678.