Metabolic adaptations in neonatal mother-deprived rabbits


  • Gabriele Brecchia Università degli Studi di Perugia
  • Massimo Zerani Università degli Studi di Camerino
  • Adriana Bonano Università degli Studi di Palermo
  • Cristiano Boiti Università degli Studi di Perugia



maternal separation, thyroid hormones, insulin, leptin, glucose, rabbits


In order to study the metabolic adaptation in response to 48 h transient doe-litter separation (DLS) in young rabbits (5 rabbits/d group) between postnatal 9 and 11 d, plasma concentrations of thyroid hormones T3 and T4, insulin, leptin, glucose, triglycerides (TG), and free fatty acids (FFA) were examined before (6-8 d), during (9-11 d), and after separation (12-16 d). T3 concentrations in newborn control rabbits gradually increased from 0.6 ng/mL at postnatal 6 d to 1.0 ng/mL at postnatal 16 d, whereas those of T4 remained fairly constant (25 ng/mL) up to postnatal 14 d, when T4 gradually declined to 8 ng/mL. T3 values of DLS newborn rabbits did not differ from those of controls at postnatal 10 and 11 d, but were lower (P<0.05) at postnatal 12 d, while T4 concentrations in DLS animals increased, although not significantly, between postnatal 10 and 12 d compared to controls. Insulin concentrations in young control rabbits ranged between 0.6 and 1.0 mg/L in the early postnatal days, whereas those for leptin averaged 2-3 ng/mL. Insulin and leptin values in DLS newborn rabbits were lower (P<0.05) at postnatal 10 and 11 d, but thereafter rebounded to levels close to those of controls. Glycaemia showed a comparable trend in both groups, ranging between 170 and 190 mg/dL up to postnatal 14 d, but thereafter decreased (P<0.05) to values of 120-130 mg/dL independently of treatment. Concentrations of TG varied greatly from day to day around a mean value of 300 mg/dL, whereas those of FFA remained at approximately the same steady-state levels from postnatal 6 to 16 d, averaging 0.8 mM without any significant differences between groups. In conclusion, these findings confirm that newborn rabbits can cope with the metabolic stress of starvation associated with DLS by lowering insulin and leptin concentrations while maintaining those of thyroid hormones, an overall endocrine response which, together with temporary increase of glucorticoids, successfully maintains an adequate energy balance.



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Author Biographies

Gabriele Brecchia, Università degli Studi di Perugia

Dipartimento di Scienze Biopatologiche ed Igiene delle Produzioni Animali e Alimentari. Laboratorio di Biotecnologie Fisiologiche. Sezione di Fisiologia Veterinaria

Massimo Zerani, Università degli Studi di Camerino

Scuola di Scienze Mediche Veterinarie

Adriana Bonano, Università degli Studi di Palermo

Dipartimento di Scienze Entomologiche, Fitopatologiche, Microbiologiche Agrarie e Zootecniche (S.EN.FI.MI.ZO). Sezione di Produzioni Animali

Cristiano Boiti, Università degli Studi di Perugia

Dipartimento di Scienze Biopatologiche ed Igiene delle Produzioni Animali e Alimentari. Laboratorio di Biotecnologie Fisiologiche. Sezione di Fisiologia Veterinaria


Barb C.R. 1999. The brain-pituitary-adipocyte axis: Role of leptin in modulating neuroendocrine function. J. Anim. Sci., 77: 1249-1257.

Blumberg M.S., Sokoloff G. 1998. Thermoregulatory competence and behavioural expression in the young of altricial species – revisited. Dev. Psychobiol., 33: 107-123.

Boelen A., Wiersinga W.M., Fliers E. 2008. Fasting-induced changes in the hypothalamus-pituitary-thyroid axis. Thyroid, 18: 123-129.

Boiti C., Galeati G., Maranesi M., Lilli L., Murgiano L., Brecchia G., Dall’Aglio C., Mercati F., Gobbetti A., Zerani M. 2008. Pituitary gonadotropins and receptors for estrogen and GnRH in fasted does. In Proc: 9th World Rabbit Congress, 10-13 June, Verona, Italy. 285289.

Bonanno A., Alabiso M., Di Grigoli A., Alicata M.L., Leto G. 1999. Effect of a 48h delayed insemination with or without a 48h doelitter separation on performance of non-receptive lactating does. World Rabbit Sci., 7: 171-175.

Bonanno, A., Di Grigoli, A., Alabiso, M., Boiti C. 2002. Parity and number of repeated doe-litter separation treatments affect differently the reproductive performances of lactating does. World Rabbit Sci., 10: 63-70.

Bonanno A., Mazza F., Di Grigoli A., Alabiso M. 2004. Effects of a split 48-hour doe-litter separation on productivity of free nursing does and their litters. Livest. Prod. Sci., 89: 287-295.

Booth P.J., Cosgrove J.R., Foxcroft G.R. 1996. Endocrine and metabolic responses to realimentation in feed-restricted prepubertal gilts: associations among gonadotropins, metabolic hormones, glucose and uteroovarian development. J. Anim. Sci., 74: 840-848.

Brecchia G., Bonanno A., Galeati G., Federici C., Maranesi M., Gobbetti A., Gerani M., Boiti C. 2006. Hormonal and metabolic adaptation to fasting: effects on the hypothalamic-pituitary-ovarian axis and reproductive performance of rabbit does. Domest. Anim. Endocrinol., 31: 105-122.

Brecchia G., Bonanno A., Dall’Aglio C., Mercati F., Zerani M., Di Grigoli A., Boiti C. 2009. Neuroendocrine responses in neonatal mother-deprived rabbits. Brain Res., 1304:105-12.

Breton C., Lukaszewski M.A., Risold P.Y., Enache M., Guillemot J., Rivière G., Delahaye F., Lesage J., Dutriez-Casteloot I., Laborie C., Vieau D. 2009. Maternal prenatal undernutrition alters the response of POMC neurons to energy status variation in adult male rat offspring. Am. J. Physiol. Endocrinol. Metab., 296: E462-472.

Buyse J., Janssens K., Van der Geyten S., Van der As P., Decuypere E., Darras V.M. 2002. Pre- and postprandial change in plasma hormone and metabolite levels and hepatic deiodenase activities in meal-fed broiler chickens. Brit. J. Nutrition., 88: 641-653.

Cassar-Malek I., Kahl S., Jurie C., Picard B. 2001. Influence of feeding level during postweaning growth on circulating concentrations of thyroid hormones and exrtathyroidal 5’-deiodination in steers. Anim. Sci., 79: 2679-2687.

Chilliard Y., Bonnet M., Delavaud C., Faulconnier Y., Leroux C., Djiane J., Bocquier F. 2001. Leptin in ruminants. Gene expression in adipose tissue and mammary gland, and regulation of plasma concentrations. Domest. Anim. Endocrinol., 21: 271-295.

Coureaud G., Schaal B., Coudert P., Rideaud P., Fortun-Lamothe L., Hudson R., Orgeur P. 2000. Immediate postnatal suckling in the rabbits: its influence on pup survival and growth. Reprod. Nutr. Dev., 40: 19-32.

Emery R.S., Liesman J.S., Herdt T.H. 1992. Metabolism of long chain fatty acids in ruminant liver. Anim. Nutr. Phys., 122: 832-837.

Escobar C., Hudson R., Martinez-Gomez M., Aguilar-Roblero R. 2000. Metabolic correlates of the circadian pattern of suckling-associated arousal in young rabbits. J. Comp. Physiol. A, 186: 33-38.

Ferguson E.M., Ashworth C.J., Edwards S.A., Hawkins N., Hepburn N., Hunter M.G. 2003. Effect of different nutritional regimens before ovulation on plasma concentrations of metabolic and reproductive hormones and oocyte maturation in gilts. Reproduction, 126: 61-71.

Forhead A.J., Fowden A.L. 2009. The hungry fetus? Role of leptin as a nutritional signal before birth. J. Physiol., 587: 1145-1152.

González-Mariscal G. 2007. Mother rabbits and their offspring: timing is everything. Dev. Psychobiol., 49: 71-76.

Havel P.J. 2001. Peripheral signals conveying metabolic information to the brain: short-term and long-term regulation of food intake and energy homeostasis. Exp. Biol. Med., 226: 963-977.

Henry B.A., Goding J.W., Tilbrook A.J., Dunshea F.R., Blache D., Clarke I.J. 2004. Leptin-mediated effects of undernutrition or fasting on luteinizing hormone and growth hormone secretion in ovariectomized ewes depends on the duration of metabolic perturbation. J. Neuroendocrinol., 16: 244-255.

Hudson R., Distel H. 1982. The pattern of behaviour of rabbit pups in the nest. Behaviour, 79: 255-272.

Jéquier E. 2002. Leptin signaling, adiposity, and energy balance. Ann. N.Y. Acad. Sci., 967: 379-388.

Mayor F., Cuezva J.M. 1985. Hormonal and metabolic changes in the perinatal period. Biol Neonate, 48:185-196.

Lechan R.M., Fekete C. 2006. The TRH neuron: a hypothalamic integrator of energy metabolism. Prog. Brain Res., 153: 209-235.

Obici S., Rossetti L. 2003. Nutrient sensing and the regulation of insulin action and energy balance. Endocrinology, 144: 5172-5178.

Obregon M.J. 2008. Thyroid hormone and adipocyte differentiation. Thyroid, 18: 185-195.

Rebollar P.G., Espinosa A., Carabaño R. 2004. Transitory disturbances in growing lactating rabbits after transient doe–litter separation. Reprod. Nutr. Dev., 44: 437–447.

Rebollar P.G., Pereda N., Villarroel M., Millán P., Lorenzo P.L. 2006. Oestrus synchronisation of rabbit does at early post-partum by doe–litter separation or eCG injection: effect on kit mortality and growth. Livest. Sci., 103: 13–22.

Rödel H.G., Bautista A., García-Torres E., Martínez-Gómez M., Hudson R. 2008. Why do heavy littermates grow better than lighter ones? A study in wild and domestic European rabbits. Physiol. Behav., 95: 441-448.

Rommers J.M., Boiti C., Brecchia G., Mejerhof R., Noordhuizen J.P.T.M., Decuypere E., Kemp B. 2004. Metabolic adaptation and hormonal regulation in young rabbit does during long-term caloric restriction and subsequent compensatory growth. Anim. Sci., 79: 255-264.

Rukkwamsuk T., Kruip T. A., Wensing T. 1999. Relationship between overfeeding and overconditioning in the dry period and the problems of high producing dairy cows during the postparturient period. Vet. Quart., 21: 71-77.

Silva J.E. 1995. Thyroid hormone control of thermogenesis and energy balance. Thyroid, 5: 481-492.

Theau-Clément M. 2007 Preparation of the rabbit doe to insemination: a review. World Rabbit Sci., 15:61-80.

Theau-Clément M., Castellini C., Maertens L., Boiti C. 1998. Biostimulation applied to rabbit reproduction: theory and practice. World Rabbit Sci., 6: 179-184.

Woods S.C., Seeley R.J., Baskin D.G., Schwarts M.W. 2003. Insulin and the blood-brain barrier. Curr. Pharm. Des., 10: 795-800.

Zarrow M.X., Denenberg V.H., Anderson C.O. 1965. Rabbit: Frequency of suckling in the pup. Science, 150: 1835-1836.

Ziylan Y.Z., Baltaci A.K., Mogulkoc R. 2009. Leptin transport in the central nervous system. Cell Biochem. Funct., 27: 63-70.