Sex-specific impact of prenatal stress on growth and reproductive parameters of guinea pigs

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 182, Issue 8, 2012, Pages 1117-1127

  Schöpper, Hanna ^a   Klaus, Teresa ^b   Palme, Rupert ^a   Ruf, Thomas ^a   Huber, Susanne ^a,b  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

Developmental programming; Reproductive maturation; Sex specific

Indexed keywords

PROGESTERONE; TESTOSTERONE;

ANIMAL; ANIMAL BEHAVIOR; ANIMAL DISEASE; ARTICLE; BLOOD; ESTRUS CYCLE; FEMALE; GESTATIONAL AGE; GUINEA PIG; INBRED STRAIN; MALE; MATERNAL BEHAVIOR; MENTAL STRESS; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PHYSIOLOGICAL STRESS; PREGNANCY; PRENATAL EXPOSURE; SEXUAL DEVELOPMENT; SEXUAL MATURATION; WEIGHT GAIN;

ANIMALS; ANIMALS, INBRED STRAINS; BEHAVIOR, ANIMAL; ESTROUS CYCLE; FEMALE; GESTATIONAL AGE; GUINEA PIGS; MALE; MATERNAL BEHAVIOR; PHOTIC STIMULATION; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROGESTERONE; SEX CHARACTERISTICS; SEXUAL MATURATION; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL; TESTOSTERONE; WEIGHT GAIN;

ANIMALIA; CAVIA; CAVIA APEREA;

EID: 84870328395     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-012-0680-9     Document Type: Article

References (69)

1. Banjanin S, Kapoor A, Matthews SG (2004) Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function and blood pressure in mature male guinea pigs. J Physiol 558: 305-318.
2. Barker DJP (2002) Fetal programming of coronary heart disease. Trends Endocrinol Metab 13: 364-368.
3. Bauer B, Womastek I, Dittami J, Huber S (2008a) The effects of early environmental conditions on reproductive and somatic development of juvenile guinea pigs (Cavia aperea f. porcellus). Gen Comp Endocrinol 155: 680-685.
4. Bauer B, Palme R, Machatschke IH, Dittami J, Huber S (2008b) Non-invasive measurement of adrenocortical and gonadal activity in male and female guinea pigs (Cavia aperea f. porcellus). Gen Comp Endocrinol 156: 482-489.
5. Bauer B, Dittami J, Huber S (2009) Effects of nutritional quality during early development on body weight and reproductive maturation in guinea pigs (Cavia aperea f. porcellus). Gen Comp Endocrinol 161: 384-389.
6. Bertram CE, Hanson MA (2002) Prenatal programming of postnatal endocrine responses by glucocorticoids. Reproduction 124: 459-467.
7. Blatchley FR, Donovan BT, Ter Haar MB (1976) Plasma progesterone and gonadotrophin levels during the estrous cycle of the guinea pig. Biol Reprod 15: 29-38.
8. Chahoud I, Paumgartten FJR (2009) Influence of litter size on postnatal growth of rat pups: is there a rationale for litter-size standardization in toxicity studies? Environ Res 109: 1021-1027.
9. Challis JRG, Heap RB, Illingworth DV (1971) Concentrations of oestrogen and progesterone in the plasma of non-pregnant, pregnant and lactating guinea pigs. J Endocrinol 51: 333-348.
10. Cooper C, Kuh D, Egger P, Wadsworth M, Barker D (1996) Childhood growth and age at menarche. Br J Obstet Gynaecol 103: 814-817.
11. D'mello AP, Liu Y (2006) Effects of maternal immobilization stress on birth weight and glucose homeostasis in the offspring. Psychoneuroendocrinology 31: 395-406.
12. Darnaudéry M, Maccari S (2008) Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57: 571-585.
13. Du M, Tong J, Zha J, Underwood KR, Zhu SP, Ford SP, Nathanielsz PW (2010) Fetal programming of skeletal muscle development in ruminant animals. J Anim Sci 88: E51-E60.
14. Dufty AMJr, Clobert J, Møller AP (2002) Hormones, developmental plasticity and adaptation. Trends Ecol Evol 17: 190-196.
15. Emack J, Kostaki A, Walker CD, Matthews SG (2008) Chronic maternal stress affects growth, behaviour and hypothalamo-pituitary-adrenal function in juvenile offspring. Horm Behav 54: 514-520.
16. Entringer S, Wüst S, Kumsta R, Layes IM, Nelson EL, Hellhammer DH, Wadhwa PD (2008) Prenatal psychological stress exposure is associated with insulin resistance in young adults. Am J Obstet Gynecol 199: 498. e1-498. e7.
17. Feder HH, Resko JA, Goy W (1968) Progesterone concentrations in the arterial plasma of guinea-pigs during the oestrous cycle. J Endocrinol 40: 505-513.
18. Fey K, Trillmich F (2008) Sibling competition in guinea pigs (Cavia aperea f. porcellus): scrambling for mother's teats is stressful. Behav Ecol Sociobiol 62: 321-329.
19. Gluckman PD, Hanson MA (2004) Living with the past; evolution, development, and patterns of disease. Science 305: 1733-1736.
20. Gluckman PD, Hanson MA (2006) Evolution, development and timing of puberty. Trends Endocrinol Metababol 17: 7-12.
21. Gluckman PD, Hanson MA, Cooper C, Thornburg KL (2008a) Effect of in utero and early-life conditions on adult health and disease. N Engl J Med 359: 61-73.
22. Gluckman P, Hanson M, Beedle A, Raubenheimer D (2008b) Fetal and neonatal pathways to obesity. In: Korbonits M (ed) Obesity and metabolism. Front Horm Res, vol 36. Karger, Basel, pp 61-72.
23. Götz AA, Wolf M, Stefanski V (2008) Psychosocial maternal stress during pregnancy: effects on reproduction for F0 and F1 generation laboratory rats. Physiol Behav 93: 1055-1060.
24. Graham JD, Clarke CL (1997) Physiological action of progesterone in target tissues. Endocr Rev 18: 502-519.
25. Harris A, Seckl J (2011) Glucocorticoids, prenatal stress and the programming of disease. Horm Behav 59: 279-289.
26. Hothorn T, Bretz F, Westfall P, Heiberger RM (2008) Multcomp: simultaneous inference in general parametric models. R package version 1. 0-0. http://cran. rproject. org/web/packages/multcomp/vignettes/generalsiminf. pdf.
27. Huizink AC, Bartels M, Rose RJ, Pulkkinen L, Eriksson CJP, Kaprio J (2008) Chernobyl exposure as stressor during pregnancy and hormone levels in adolescent offspring. J Epidemiol Community Health 62: e5.
28. Ikegami M, Jobe AH, Newnham J, Polik DH, Willet KE, Sly P (1997) Repetitive prenatal glucocorticoids improve lung function and decrease growth in preterm lambs. Am J Respir Crit Care Med 156: 178-184.
29. Jeppesen LL, Heller KE (1986) Stress effects on circulating eosinophil leukocytes, breeding performance, and reproductive success of ranch mink. Scientifur 10: 15-18.
30. Kaiser S, Kruijver FPM, Swaab DF, Sachser N (2003) Early social stress in female guinea pigs induces a masculinization of adult behavior and corresponding changes in brain and neuroendocrine function. Behav Brain Res 144: 199-210.
31. Kapoor A, Matthews SG (2005) Short periods of prenatal stress affect growth, behaviour and hypothalamo-pituitary-adrenal axis activity in male guinea pig offspring. JPhysiol 566: 967-977.
32. Kemme K, Kaiser S, Sachser N (2007) Prenatal maternal programming determines testosterone response during social challenge. Horm Behav 51: 387-394.
33. Kemme K, Kaiser S, Sachser N (2008) Prenatal stress does not impair coping with challenge in later life. Physiol Behav 93: 68-75.
34. Klaus T (2010) Effects of gestational stress on maternal performance and offspring growth and behaviour in the guinea pig (Cavia aperea f. porcellus) Diploma thesis, Vienna University.
35. Laurien-Kehnen C, Trillmich F (2004) Maternal food restriction delays weaning in the guinea pig, Cavia porcellus. Anim Behav 68: 303-312.
36. Lesage J, Del-Favero F, Leonhardt M, Louvart H, Maccari S, Vieau S, Darnaudery M (2004) Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J Endocrinol 181: 291-296.
37. McCabe L, Marash D, Li A, Matthews SG (2001) Repeated antenatal glucocorticoid treatment decreases hypothalamic corticotrophin releasing hormone mRNA but not corticosteroid receptor mRNA expression in the fetal guinea-pig brain. J Neuroendocrinol 13: 425-431.
38. Montano MM, Wang MH, vom Saal FS (1993) Sex differences in plasmacorticosterone in mouse fetuses are mediated by differential placental transport from the mother and eliminated by maternal adrenalectomy or stress. J Reprod Fertil 99: 283-290.
39. Moritz KM, Dodic M, Wintour EM (2003) Kidney development and the fetal programming of adult disease. BioEssays 25: 212-220.
40. Mueller BR, Bale TL (2006) Impact of prenatal stress on long term body weight is dependent on timing and maternal sensitivity. Physiol Behav 88: 605-614.
41. Nathanielsz PW (2006) Animal models that elucidate basic principles of the developmental origins of adult disease. ILAR J 47: 73-82.
42. Nieuwenhuizen AG, Rutters F (2008) The hypothalamic-pituitary-adrenal-axis in the regulation of energy balance. Physiol Behav 94: 169-177.
43. Nyrienda MJ, Seckl JR (1998) Intrauterine events and the programming of adulthood disease: the role of fetal glucocorticoid exposure (review). Int J Mol Med 2: 607-614.
44. Palme R, Möstl E (1994) Biotin-streptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar faeces. In: Görög S (ed) Advances of steroid analysis '93. Akadémiai Kiadó, Budapest, pp 111-117.
45. Palmer AC (2011) Nutritional mediated programming of the developing immune system. Adv Nut 2: 377-395.
46. Phillips DIW, Barker DJP, Fall CHD, Seckl JR, Whorwood CB, Wood PJ, Walker BR (1998) Elevated plasma cortisol concentrations: a link between low birth weight and the insulin resistance syndrome. J Clin Endocinol Metab 83: 757-760.
47. Pinheiro J, Bates D, DebRoy S, Sarkar D, the R core team (2007) Nlme: linear and nonlinear mixed effects models. R package version 3. 1-89. http://CRAN. R-project. org/package=nlme.
48. Politch JA, Herrenkohl LR (1984) Effects of prenatal stress on reproduction in male and female mice. Physiol Behav 32: 95-99.
49. R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0 http://www. R-project. org.
50. Ravelli GP, Stein ZS, Susser MW (1976) Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 295: 349-353.
51. Rhind SM, Rae MT, Brooks AN (2001) Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction 122: 205-214.
52. Rigaudière N, Pelardy G, Robert A, Delost P (1976) Changes in the concentrations of testosterone and androstenedione in the plasma and testis of the guinea-pig from birth to death. J Reprod Fertil 48: 291-300.
53. Rood JP, Weir B (1970) Reproduction in female wild guinea-pigs. Reproduction 23: 393-409.
54. Sachser N, Kaiser S (1996) Prenatal social stress masculinizes the females' behaviour in guinea pigs. Physiol Behav 60: 589-594.
55. Sachser N, Pröve E (1984) Short-term effects of residence on the testosterone responses to fighting in alpha male guinea pigs. Aggr Behav 10: 285-292.
56. Schneider ML, Roughton EC, Koehler A, Lubach GR (1999) Growth and development following prenatal stress in primates: an examination of ontogenetic vulnerability. Child Dev 70: 263-274.
57. Schöpper H, Palme R, Ruf T, Huber S (2011) Chronic stress in pregnant guinea pigs (Cavia aperea f. porcellus) attenuates long-term stress hormone levels and body weight gain, but not reproductive output. J Comp Physiol B 181: 1089-1100.
58. Schöpper H, Palme R, Ruf T, Huber S (2012) Effects of prenatal stress on hypothalamic-pituitary-adrenal (HPA) axis function over two generations of guinea pigs (Cavia aperea f. porcellus) Gen Comp Endocrinol 176: 18-27.
59. Schwarzenberger F, Tomasova K, Holeckova D, Matern B, Möstl E (1996) Measurement of fecal steroids in the black rhinoceros (Diceros bicornis) using group-specific enzyme immunoassay for 20-oxo-pregnanes. Zoo Biol 15: 159-171.
60. Seckl JR (2004) Prenatal glucocorticoids and long-term programming. Eur J Endocrinol 151: U49-U62.
61. Sloboda DM, Hart R, Doherty DA, Pennell CE, Hickey M (2007) Age at menarche: influences of prenatal and postnatal growth. J Clin Endocrinol Metab 92: 46-50.
62. Stockard CR, Papanicolaou GN (1917) The existing of a typical oestrus cycle in the guinea-pig-with a study of histological and physiological changes. Am J Anat 22: 225-283.
63. Symonds ME, Stephenson T, Gardner DS, Budge H (2007) Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reprod Fertil Dev 19: 53-63.
64. Touma C, Palme R, Sachser N (2001) Different types of oestrus cycle in two closely related South American rodents (Cavia aperea and Galea musteloides) with different social and mating systems. Reproduction 121: 791-801.
65. Trillmich F, Laurien-Kehnen C, Adrian A, Linke S (2006) Age at maturity in cavies and guinea-pigs (Cavia aperea and Cavia aperea f. porcellus): influence of social factors. J Zool 268: 285-294.
66. Valencak TG, Tataruch F, Ruf T (2009) Peak energy turnover in lactating European hares: the role of fat reserves. J Exp Biol 212: 231-237.
67. Westfahl PK, Vekasy MS (1988) Changes in serum and ovarian steroids during reproductive development in the female guinea pig. Biol Reprod 39: 1086-1092.
68. Woody CO, First NL, Pope AL (1967) Effect of exogenous progesterone on estrous cycle length. J Anim Sci 26: 139-141.
69. Young WC (1937) The vaginal smear picture, sexual receptivity and the time of ovulation in the guinea pig. Anat Rec 67: 305-325.