Long-term alterations on the physical development of pre- and neonatally undernourished Wistar rats: a functional correlation

Minerva Ortiz-Valladares, Claudia A Salcedo, Mirelta Regalado Ortega, Carmen Torrero Solorio, Manuel Salas Alvarado

Resumen


La restricción temprana de alimento en la rata interfiere en el largo plazo con el desarrollo físico y la función cerebral, aunque los parámetros del sistema esquelético asociados a la desnutrición pre y neonatal han sido poco estudiados. Se Compararon los efectos de la desnutrición gestacional y por la ligadura materna (UL), con los de la desnutrición en una incubadora (UI) asociada a privación sensorial en el desarrollo físico de ratas Wistar hembras y machos F1 y machos adultos F1. Las madres UL F0 recibieron restricción calórica prenatal de alimento. En la lactancia, una de un par de madres se ligó de sus conductos galactóforos intercambiándose entre las camadas (12 h) con otra sin ligadura. Los sujetos con UI permanecieron en una incubadora durante 12 h. Entre los días postnatales (PDs) 5-90 se midieron los ejes longitud del cráneo, bitemporal, naso-cóccix, cola, tarso-metatarso y longitud de falanges, peso corporal, tamaño corporal medio y apertura palpebral. Los sujetos UL y UI mostraron déficits esqueléticos significativos después de una dieta normocalórica desde el PD 25 hasta el 90 vs. sus controles. Además, mostraron pesos corporales significativamente bajos tanto en los sujetos UL hembras o machos, como en los sujetos con UI al compararse ambos grupos. El índice de masa corporal (BMI) en el día PD 90 en hembras con UI mostró un porcentaje mayor vs. sus controles. Se sugiere que la desnutrición perinatal alteró el desarrollo físico de los sujetos F1, afectando su actividad sensoriomotora y las respuestas adaptativas sociales tardías.


Abstract: Early food restriction resulted in long-term consequences on physical and brain development. However, long-term skeletal maturity parameters interacting with sensory deprivation are scarcely described. We compare the effects of gestational undernutrition and postnatal ligature (UL) and neonatal undernutrition by using an incubator (UI) with sensory deprivation on the physical development of suckling and adult F1 female and male Wistar rats. UL F0 subjects were submitted to caloric food restriction during the gestational period and suckling of dams, one with nipple-ligated and interchanged every 12 h. UI subjects were underfed by placing pups into one incubator for 12 h. Skull, nose-coccyx, tail, tarsus-metatarsus, phalange lengths, bitemporal axis, body weight, mean body sizes and eyelid opening were measured on postnatal days (PDs) 5-90. UL and UI subjects resulted with significant skeletal deficits following a normocaloric diet from PD 25 in most of the ages from PDs 5 to 90 of the study compared with their controls. Furthermore, significant low body weights in both female and male UL groups throughout the lactation period, compared to normally feeding rats were obtained. Body Mass Index (BMI) on PD 90 in female UI subjects showed higher percentages than controls. The findings indicated that gestational undernutrition of F0 dams resulted in consistent, long-term altered physical development of F1 subjects that might interfere with their body growth, sensorimotor activity and possibly with the late social adaptive responses.

Keywords: Early undernutrition; physical development; rats; sensory manipulation; growth.


Palabras clave


Desnutrición temprana; desarrollo físico; ratas; manipulación sensorial; crecimiento.

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Referencias


Einstein FH. Multigenerational effects of maternal undernutrition. Cell Metab. 2014 19: 893–894.

Danchin É, Charmantier A, Champagne F,Mesoudi A, Pujol B, Blanchet S. Beyond DNA: integrating inclusive inheritance into an extended theory of evolution. Nat. Rev. Genet. 2011 12: 475–486.

Felix J, Regalado M, Torrero C, Salas M. Retrieval of pups by female rats undernourished during the pre–and neonatal period. J. Behav. Brain Sci. 2014 4:325–333.

Kehoe P, Mallinson K, Bronzino J, McCormick CM. Effects of prenatal protein malnutrition and neonatal stress on CNS responsiveness. Dev. Brain Res. 2001 132:23–31.

Kuhn CM, Butler SR, Schanberg SM. Selective depression of serum growth hormone during maternal deprivation in rat pups. Science. 1978 201: 1034–1036.

Vieau D, Sebaai N, Léonhardt M, Dutriez-Casteloot I, Molendi-Coste O, Laborie C, Breton C, Breton C, Lesage J. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology. 2007 32: 16-20.

Jansson T, Powell TL. Role of placental nutrient sensing in developmental programming. Clin. Obstet. Gynecol. 2013 56: 591–601.

Díaz P, Powell TL, Jansson T. The Role of Placental Nutrient Sensing in Maternal-Fetal Resource Allocation. Biol. Reprod. 2014 91:1-10.

Horton R. Maternal and child undernutrition: an urgent opportunity.Lancet. 2008 371:179.

Belkacemi L, Nelson DM, Desai M, Ross MG. Maternal Undernutrition Influences Placental Fetal Development. Biol. Reprod. 2010 331:325–331.

Anderson GD, Ahokas RA, Lipshitz J, Dilts PVJ. Effect of maternal dietary restriction during pregnancy on maternal weight gain and fetal birth weight in the rat. J. Nutr.1980 110: 883–890.

Molina-Font J. Nutrition and fetal growth. Early Hum. Dev. 1998 53: 51-60.

Reynolds S, Millette A, Devine DP. Sensory and Motor Characterization in the Postnatal Valproate Rat Model of Autism. Dev Neurosci-basel. 2012;34(2-3):258-267.

Harding J E, Johnston BM. Nutrition and fetal growth. Reprod. Fertil. Dev. 1995 7:539–547.

Aláez C, Calvo R, Obregón MJ, Pascual Leone AM. Thyroid hormones and 5’-deiodinase activity in neonatal undernourished rats. Endocrinology. 1992 130: 773–779.

Ayala-Moreno R, Racotta R, Anguiano B, Aceves C, Quevedo L. Perinatal undernutrition programmes thyroid function in the adult rat offspring. Br. J. Nutr. 2013 110: 2207-2215.

Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J. Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur. J. Neurosci. 2006 24:1477–1487.

Mckay JA, Mathers JC. Diet induced epigenetic changes and their implications for health. Acta Physiol. 2011 202:103–118

Jiménez-Chillarón JC, Díaz R, Martínez D, Pentinat T, Ramón-Krauel M, Ribó S, Plösch, T. The role of nutrition on epigenetic modifications and their implications on health. Biochimie. 2012 94:2242–2263.

Zeisel SH. Epigenetic mechanisms for nutrition determinants of later health outcomes. Am. J. Clin. Nutr. 2009 89:1488-1493.

Smart JL, Adlard BPF, Dubbing J. Further studies of body growth and brain development in “small-for-dates” rats. Neonatology. 1974 25: 135–150.

Jaiswal AK, Upadhyay SK, Satyan KS,Bhattacharya SK. Comparative effects of prenatal and postnatal undernutrition on learning and memory in rats. Indian J. Exp. Biol. 1999 37: 17–22.

Rice D, Barone S. Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ. Health Perspect. 2000 3:511-533.

Herlenius E, Lagercrantz H. Development of neurotransmitter systems during critical periods. Exp. Neurol. 2004 190:8–21.

Hardikar A, Satoor S, Karandikar M, Keech A, Jekins A, Yajnik C. Multigenerational undernutrition increases susceptibility to obesity and diabetes that is not reversed after dietary recuperation. Cell Metab. 2015 22: 312–319.

Bedi KS, Birzgalis AR, Mahon M, Smart JL, Wareham AC. Early life undernutrition in rats. 1. Quantitative histology of skeletal muscles from underfed young and refed adult animals. Br. J. Nutr. 1982 47:417–431.

Pucciarelli HM, Oyhenart EE. Effects of maternal food restriction during lactation on craniofacial growth in weanling rats. Am. J. Phys. Anthropol. 1987 72: 67–75

Warren M, Bedi KS. The effects of a lengthy period of undernutrition on food intake and on body and organ growth during rehabilitation. J. Anat. 1985 141:65–75.

Woodall SM, Breier BH, Johnston BM, Gluckman PDA. Model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: Effects on the somatotrophic axis and postnatal growth. J. Endocrinol. 1996 150: 231–242.

Barbeito-Andrés J, Gonzalez P, Hallgrímsson B. Prenatal development of skull and brain in a mouse model of growth restriction. Rev. Argentina Antropol. Biológica. 2016 18: 1–13.

Committee on Guidelines for the Use of Animals in Neuroscience and Behavioral Research (National Research Council). Guidelines for the care and use of mammals in neuroscience and behavioral research. Book (National Academies Press, 2003). doi:https://10.17226/10732.

Khan-Merchant N, Penumetcha M, Meilhac O, Parthasarathy S. Oxidized fatty acids promote atherosclerosis only in the presence of dietary cholesterol in low-density lipoprotein receptor knockout mice. J. Nutr. 2002 132: 3256–3262.

Lynch A. Postnatal undernutrition: an alternative method. Dev. Psychobiol. 1976 9: 39–48.

Altman J, Bayer SA. Atlas of prenatal rat brain development. CRC Press, Boca Raton, Florida 1995 pp. 1-589.

Hughes PC, Tanner, JMA. longitudinal study of the growth of the black-hooded rat: methods of measurement and rates of growth for skull, limbs, pelvis, nose-rump and tail lengths. J. Anat. 1970 106: 349–370.

Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of In Utero and Early-Life Conditions on Adult Health and Disease. N. Engl. J. Med. 2008 359: 61–73.

Belkacemi L, Nelson DM, Desai M, Ross M G. Maternal undernutrition influences placental-fetal development. Biol. Reprod. 2010 83: 325–331.

Florian ML, Nunes ML. Effects of intra-uterine and early extra-uterine malnutrition on seizure threshold and hippocampal morphometry of pup rats. Nutr. Neurosci. 2011 14: 151–158.

Wu G, Bazer FW, Cudd TA, Meininger CJ, Spencer TE. Maternal nutrition and fetal development. J. Nutr. 2004 134: 2169–2172.

Salas M, Torrero C, Regalado M, Rubio L. Effects of perinatal undernutrition on the basilar dendritic arbor of the anterior cingulate pyramidal neurons in lactating dams. Acta Neurobiol. Exp. (Wars). 2015 75: 372–380.

Kennedy GC, Mitra J. Body weight and food intake as initiating factors for puberty in the rat. J. Physiol. 1963 166: 408–418.

Larsson K, Carlsson SG, Sourander P, Forrsstrom B, Hansen S, Henriksson B, Lindquist A. Delayed Onset of Sexual Activity of Male Rats Subjected to Pre and Postnatal Undernutrition. Physiol. Behav. 1974 3: 307–311.

Salas M, Torrero C, Regalado M, Perez E. Retrieving of pups by neonatally stressed mothers. Nutr. Neurosci. 2002 5: 399–405.

Curtis G, Sung J, Rogers J. Maternal influences on epigenetic programming of the developing hypothalamic-pituitary-adrenal axis. Birth Defects Res A Clin Mol Teratol. 2011 91: 797–805.

Batista TH, Veronesi VB, Ribeiro ACAF, Giusti-Paiva A, Vilela FC. Protein malnutrition during pregnancy alters maternal behavior and anxiety-like behavior in offspring. Nutr. Neurosci. 2017 20: 437–442.

Purves D, Augustine GJ, Fitzpatrick D, Hall WC, LaMantia AS, McNamara JO, White LE. En: Movement and its central control. Neuroscience Sinauer Ass. 5th edition 2012 pp. 353-435.

Altman J, Sudarshan K, Mccormick N. Neural and Behavioral Development : III. Development of Some Motor, Particularly Locomotor Patterns During Infancy. Dev. Psychobiol. 1971 4: 97–114.

Salas, M. Effects of early malnutrition on the development of swimming ability in the rat. Physiol. Behav. 1972 8: 119–122.

Harrison AP, Tivey, DR, Clausen T, Duchamp C, Dauncey MJ. Role of thyroid hormones in early postnatal development of skeletal muscle and its implications for undernutrition. Br. J. Nutr. 1996 76: 841–855.

Loranca A, Torrero C, Salas M. Development of play behavior in neonatally undernourished rats. Physiol. Behav. 1999 66: 3–10.

Salcedo C, Torrero C, Regalado M, Rubio L, Salas M. Effects of pre- and neonatal undernutrition on the kyphotic response and c-Fos activity in the caudal periaqueductal gray of primiparous lactating Wistar rats. Physiol. Behav. 2018 185: 87–94.

Raju NV. Effect of early malnutrition on muscle function and metabolism in rats. Life Sci. 1974 15 949–960.

Ravelli GP, Stein, ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N. Engl. J. Med. 1976 295: 349–353.

Faust IM, Johnson PR, Hirsch J. Long-term effects of early nutritional experience on the development of obesity in the rat. J. Nutr. 1980 110: 2027–2034.

Björntorp P, Holm G, Rosmond R. Hypothalamic arousal, insulin resistance and Type 2 diabetes mellitus. Diabet. Med. 1999 16:373–383.

Barness LA, Opitz JM, Gilbert-Barness E. Obesity: Genetic, molecular, and environmental aspects. in American Journal of Medical Genetics, Part A. 2007 143: 3016–3034

Clarke KA, Parker AJ, Smart JL. Analysis of walking locomotion in adult female rats undernourished as sucklings. Physiol. Behav. 1992 52: 823–826.




DOI: https://doi.org/10.25009/eb.v10i25.2567

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