Abstract
This paper addresses the effect of a reduction of uterine blood flow (RUB) on postcranial bone growth in rats. The objectives were: (1) to discover and characterize the changes evoked by growth retardation through a reduction in placental blood flow, (2) to see if the resulting growth retardation is different in each bone, and (3) to analyze any sex-specific features. RUB was induced by the partial bending of uterine vessels at day 1 of pregnancy. Control and sham-operated animals were also included. The animals were X-rayed at birth. The lengths and widths of the humerus, radius, and femur and pelvic length, interischial, interpubic, and pubic widths were measured. Data were analyzed by ANOVA and LSD post hoc tests. The intersubject analysis showed significant differences between groups and non-significant differences between sexes. In males, sham-operated and RUB showed significant differences in pelvic lengths and widths, and humeral, radial, femoral, and tibial widths. In females, there were significant differences only for humeral widths, radial lengths and widths, and femoral and tibial widths. We conclude that reduced blood flow delays appendicular bone growth as observed at birth. Pelvic length was more affected than that of the limbs. The widths of the pelvic and limbs bones, in turn, were more altered than the lengths, and the growth of the males more than that of the females. Partial bending of uterine vessels compromised postcranial growth, though under such disadvantageous circumstances the females proved to be more capable of growing and thus more resilient than the males.
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References
Adams P (1969) The effects of experimental protein deficiency on the growth and development of long bones. In: Jelliffe AM (ed) Symposium Ossium. Livingstone, Edinburgh
Adams P, Berridge FR (1969) Effects of kwashiorkor on cortical and trabecular bone. Arch Dis Child 44:705
Barker DJP (1998) In utero programming of chronic disease. Clin Sci 95:115–128
Beltrand J, Alison M, Nicolescu R, Verkauskiene R, Deghmoun S, Sibony O, Sebag G, Le’Vy Marchal C (2008) Bone mineral content at birth is determined both by birth weight and fetal growth pattern. Pediatr Res 64:1–8
Berdnikovs S, Bernstein M, Metzler A, German RZ (2007) Pelvic growth: ontogeny of size and shape sexual dimorphism in rat pelves. J Morphol 268:12–22
Bernstein P, Crelin ES (2005) Bony pelvic sexual dimorphism in the rat. Anat Rec 157:517–525
Cameron GN, Eshelman BD (1996) Growth and reproduction of hispid cotton rats (Sigmodon hispidus) in response to naturally occurring levels of dietary protein. J Mammal 77:220–231
Cesani MF, Orden AB, Zucchi M, Muñe MC, Oyhenart EE, Pucciarelli HM (2006) Effect of undernutrition on the cranial growth of the rat. An intergenerational study. J Anat 209:137–147
Chaddha V, Viero S, Huppertz B, Kingdom J (2004) Developmental biology of the placenta and the origins of placental insufficiency. Semin Fetal Neonatal Med 9:357–369
Dammrich K (1991) Relationship between nutrition and bone growth in large and giant dogs. J Nutr 121:114–121
Desai M, Crowther NJ, Lucas A, Hales CN (1996) Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 76:591–603
Dressino V, Orden B, Oyhenart EE (2002) Sexual responses to intrauterine stress: body and brain growth. Clin Exp Obstet Gynecol 29:100–102
Gicquel C, Le Bouc Y (2006) Hormonal regulation of fetal growth. Horm Res 65:28–33
Guimarey LM, Oyhenart EE, Quintero FA, Fucini MC (2003) Body weight recovery in intrauterine growth-retarded rats treated with growth hormone. Clin Exp Obstet Gynecol 30:51–56
Huizinga CT, Engelbregt MJT, Rekers-Mombarg LTM, Vaessen SFC, Delemarre-van de Waal HA, Fodor M (2004) Ligation of the uterine artery and early postnatal food restriction—animal models for growth retardation. Horm Res 62:233–240
Loveridge N, Noble BS (1994) Control of longitudinal growth: the role of nutrition. Eur J Clin Nutr 48:75–84
McCance RA (1960) Severe undernutrition in growing and adult animals. 1. Production and general effects. Br J Nutr 14:59–68
McMillen C, Adams MB, Ross JT, Coulter CL, Simonetta G, Owens JA, Robinson JS, Edwards LJ (2001) Fetal growth restriction: adaptations and consequences. Reproduction 122:195–204
Miller JP, German RZ (1999) Protein malnutrition affects the growth trajectories of the craniofacial skeleton in rats. J Nutr 129:2061–2069
Morrison JL (2008) Sheep model of intrauterine growth restriction: fetal adaptations and consequences. Clin Experim Pharmacol Physiol 35:730–743
Mughal MZ, Ross R, Tsang RC (1989) Clearance of calcium across in situ perfused placentas in intrauterine growth-retarded rat fetuses. Pediatr Res 24:420–422
Myatt L (2006) Placental adaptive responses and fetal programming. J Physiol 572:25–30
Nafee TM, Farrell WE, Carroll WD, Fryer AA, Ismail KM (2008) Epigenetic control of fetal gene expression. BJOG 115:158–168
Namgung R, Tsang RC (2000) Factors affecting newborn bone mineral content: in utero effects on newborn bone mineralization. Proc Nutr Soc 59:55–63
Oyhenart EE, Muñe MC, Pucciarelli HM (1998) Influence of intrauterine blood supply on cranial growth and sexual dimorphism at birth. Growth Dev Aging 62:187–198
Oyhenart EE, Guimarey LM, Fucini MC, Quintero FA, Orden B (2002) Effects of bilateral uterine vessel ligation on skeletal growth in rats. Clin Exp Obstet Gynecol 29:121–125
Prader A, Tanner JM, Harnack GAV (1963) Catch-up growth following illness or starvation. An example of developmental canalization in man. J Pediatr 62:646–659
Schreuder MF, Fodor M, van Wijk JA, Delemarre-van de Waal HA (2006) Association of birth weight with cardiovascular parameters in adult rats during baseline and stressed conditions. Pediatr Res 59:126–130
Stewart RJ, Preece RF, Sheppard HG (1975) Twelve generations of marginal protein deficiency. Br J Nutr 33:233–253
Tanner JM (1962) Growth at adolescense. Blackwell, Oxford
Widdowson EM, McCance RA (1963) The effect of finite periods of undernutrition at different ages on the composition and subsequent development of the rat. Proc R Soc Lond B Biol Sci 185:329–342
Wigglesworth JS (1964) Experimental growth retardation of foetal rat. J Pathol Bacteriol 88:1–13
Acknowledgments
This research was supported by grants from the Universidad Nacional de La Plata (UNLP) and the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). The authors are grateful to Dr. Donald F. Haggerty, a native English speaker, for editing the manuscript.
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Oyhenart, E.E., Cesani, M.F., Castro, L.E. et al. Bone growth and sexual dimorphism at birth in intrauterine-growth-retarded rats. Anat Sci Int 86, 119–127 (2011). https://doi.org/10.1007/s12565-010-0098-y
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DOI: https://doi.org/10.1007/s12565-010-0098-y