International Journal of Animal Biology
Articles Information
International Journal of Animal Biology, Vol.4, No.2, Jun. 2018, Pub. Date: Aug. 10, 2018
Digestive System and Behavior Disorders Related to Weaning in Mammals
Pages: 19-25 Views: 1526 Downloads: 473
Authors
[01] Mariem Chaâbane, Department of Life Sciences, Sciences Faculty of Sfax, Sfax, Tunisia.
[02] Imen Ghorbel, Department of Life Sciences, Sciences Faculty of Sfax, Sfax, Tunisia.
[03] Awatef Elwej, Department of Life Sciences, Sciences Faculty of Sfax, Sfax, Tunisia.
[04] Najiba Zeghal, Department of Life Sciences, Sciences Faculty of Sfax, Sfax, Tunisia.
[05] Nejla Soudani, Department of Life Sciences, Sciences Faculty of Sfax, Sfax, Tunisia.
Abstract
Weaning is a natural and inevitable phase of mammalian development. In both animals and humans, this process represents a transition from a milk based diet (low carbohydrate content) to a solid diet (relatively rich in carbohydrates). Both, the dietary change and the decline of the mother's attention during this critical period cause a state of stress in the offspring. The present review was designed to analyze the impacts of the weaning procedure on the digestive system and the behavior of mammals such as humans, rodents and pigs. Based on literature data, it appears that weaning is a complex process that requires physiological, microbiological and immunological adjustments in the digestive tract. The physiological changes are manifested by alterations of the intestinal anatomy, the activity of the digestive enzymes and the function of intestinal absorption. The composition of the intestinal flora undergoes changes depending of food and the environment. Weaning results also in the activation of the intestinal immune system following the introduction of new food and microbiological antigens. It involves also behavioral changes which depend largely on the age at which this process is performed. Thus, these data highlight the influence of diet on one of the early stages of mammalian development that may have an effect on the health during adulthood.
Keywords
Weaning, Mammals, Diet, Digestive Tract, Behavior
References
[01] Azara, C. R., Maia, I. C., Rangel, C. N., Silva-Neto, M. A., Serpa, R. F., De Jesus, E. F., Tavares Do Carmo, M. G. and Fialho, E. (2008). Ethanol intake during lactation alters milk nutrient composition and growth and mineral status of rat pups. Biol. Res. 41: 317–330.
[02] Richter, S. H., Kästner, N., Loddenkemper, D. H., Kaiser. S. and Sachser. N. A. (2016). Time to wean? Impact of weaning age on anxiety-like behaviour and stability of behavioural traits in full adulthood. PLoS ONE 11: e0167652.
[03] Farshim, P., Walton, G., Chakrabarti, B., Givens, I., Saddy, D., Kitchen, I. R., Swann, J. and Bailey, A. (2016). Maternal weaning modulates emotional behavior and regulates the gut-brain axis. Sci. Rep. 6: 21958.
[04] Moeser, A. J., Pohl, C. S. and Rajput, M. (2017). Weaning stress and gastrointestinal barrier development: Implications for lifelong gut health in pigs. Anim. Nutr. 3: 313–321.
[05] Lallès, J. P., Bosi, P., Smidt, H. and Stokes, C. R. (2007). Weaning — A challenge to gut physiologists. Livest. Sci. 108: 82–93.
[06] Kikusui, T., Kiyokawa, Y. and Mori, Y. (2007). Deprivation of mother-pup interaction by early weaning alters myelin formation in male, but not female, ICR mice. Brain Res. 1133: 115–122.
[07] Dunphy-Doherty, F., O'Mahony, S. M., Peterson, V. L., O'Sullivan, O., Crispie, F., Cotter, P. D., Wigmore, P., King, M. V., Cryan, J. F. and Fone, K. C. F. (2018). Post-weaning social isolation of rats leads to long-term disruption of the gut microbiota-immune-brain axis. Brain Behav. Immun. 68: 261-273.
[08] Cummins, A. G. and Thompson, F. M. (2002). Effect of breast milk and weaning on epithelial growth of the small intestine in humans. Gut 51: 748−754.
[09] Cummins, A. G., Jones, B. J. and Thompson, F. M. (2006). Postnatal epithelial growth of the small intestine in the rat occurs by both crypt fission and crypt hyperplasia. Dig. Dis. Sci. 51: 718–723.
[10] Hampson, D. J. (1986). Alterations in piglet small intestinal structure at weaning. Res. Vet. Sci. 40: 32–40.
[11] Yang, H., Xiong, X., Wang, X., Tan, B., Li, T. and Yin, Y. (2016). Effects of weaning on intestinal upper villus epithelial cells of piglets. PLoS ONE 11: e0150216.
[12] Pluske, J. R., Williams, I. H. and Aherne, F. X. (1996). Villous height and crypt depth in piglets in response to increases in the intake of cows’ milk after weaning. Anim. Sci. 62: 145–158.
[13] Jiang, Z., Wei, S., Wang, Z., Zhu, C., Hu, S., Zheng, C., Hu, Y., Wang, L., Ma, X. and Yang X. (2015). Effects of different forms of yeast Saccharomyces cerevisiae on growth performance, intestinal development, and systemic immunity in early-weaned piglets. J. Anim. Sci. Biotechnol. 6: 47–54.
[14] Hedemann, M. S., Højsgaard, S. and Jensen, B. B. (2003). Small intestinal morphology and activity of intestinal peptidases in piglets around weaning. J. Anim. Physiol. Anim. Nutr. 87: 32–41.
[15] Hau, J. and Schapiro, S. J. (2010). In: Handbook of laboratory animal science: Vol. I. Essential principles and practices. 3rd ed. Boca Raton, FL: CRC Press.
[16] Kim, J. W. (2017). Lactose intolerance and colorectal cancer. Ann. Coloproctol. 33: 157–158.
[17] O’connor, T. P. and Diamond, J. (1999). Ontogeny of intestinal safety factors: lactase capacities and lactose loads. Am. J. Physiol. 276: 753–765.
[18] Witte, J., Lloyd, M., Lorenzsonn, V., Korsmo, H. and Olson, W. (1990). The biosynthetic basis of adult lactase deficiency. J. Clin. Investig. 86: 1338–1342.
[19] Redman, R. S. and Sweney, L. R. (1976). Change in diet and patterns of feeding activity of developing rats. J. Nutr. 106: 615–626.
[20] Marion, J., Petersen, Y. M., Romé, V., Thomas, F., Sangild, P. T., Le Dividich, J. and Le Huërou-Luron, I. (2005). Early weaning stimulates intestinal brush border enzyme activities in piglets, mainly at the posttranscriptional level. J. Pediatr. Gastroenterol. Nutr. 41: 401–410.
[21] Henning, S. J. (1986). Development of the gastrointestinal tract. Proc. Nutr. Soc. 45: 39–44.
[22] Henning, S. J. (1978). Plasma concentrations of total and free corticosterone during development in the rat. Am. J. Physiol. 235: 451–456.
[23] Ghizoni, H., Figueiredo, P. M., Moisan, M. P., Ogias, D., Osaki, L. H. and Gama, P. (2014). Regulation of corticosterone function during early weaning and effects on gastric cell proliferation. Nutrition 30: 343–349.
[24] Boyle, J. T. and Koldovsky, O. (1980). Critical role of adrenal glands in precocious increase in jejunal sucrase activity following premature weaning in rats: negligible effect of food intake. J. Nutr. 110: 169–177.
[25] Lee, P. C. and Lebenthal, E. (1983). Early weanling and precocious development of small intestine in rats: genetic, dietary or hormonal control. Pediatr. Res. 17: 645–650.
[26] Pacha, J. (2000). Development of intestinal transport function in mammals. Physiol. Rev. 80: 1633–1667.
[27] Keelan, M., Clandinin, M. T. and Thomson, A. B. (1997). Refeeding varying fatty acid and cholesterol diets alters phospholipids in rat intestinal brush border membrane. Lipids 32: 895–901.
[28] Wang, B., Rong, X., Duerr, M. A., Hermanson, D. J., Hedde, P. N., Wong, J. S., Vallim, T. Q., Cravatt, B. F., Gratton, E., Ford, D. A. and Tontonoz, P. (2016). Intestinal phospholipid remodeling is required for dietary lipid uptake and survival on a high-fat diet. Cell. Metab. 23: 492–504.
[29] Puchal, A. A. and Buddington, R. K. (1992). Postnatal development of monosaccharide transport in pig intestine. Am. J. Physiol. 262: 895–902.
[30] Toloza, E. M. and Diamond, J. (1992). Ontogenetic development of nutrient transporters in rat intestine. Am. J. Physiol. 263: 593–604.
[31] Mochizuki, K., Sakaguchi, N. and Goda, T. (2007). Triiodothyronine (T3) and fructose coordinately enhance expression of the GLUT5 gene in the small intestine of rats during weaning period. Biosci. Biotechnol. Biochem. 71: 1345–1347.
[32] Boudry, G., Peron, V., Le Huerou-Luron, I., Lalles, J. P. and Seve, B. (2004). Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. J. Nutr. 134: 2256–2262.
[33] Boudry, G., Lalles, J. P., Malbert, C. H., Bobillier, E. and Seve, B. (2002). Diet-related adaptation of the small intestine at weaning in pigs is functional rather than structural. J. Pediatr. Gastroenterol. Nutr. 34: 180–187.
[34] Van Der Meulen, J., Koopmans, S. J., Dekker, R. A. and Hoogendoorn, A. (2010). Increasing weaning age of piglets from 4 to 7 weeks reduces stress, increases post-weaning feed intake but does not improve intestinal functionality. Animal 4: 1653–1661.
[35] Wijtten, P. J., Van Der Meulen, J. and Verstegen, M. W. (2011). Intestinal barrier function and absorption in pigs after weaning: a review. Br. J. Nutr. 105: 967–981.
[36] Mackie, R. I., Sghir, A. and Gaskins, H. R. (1999). Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69: 1035–1045.
[37] Koenig, J. E., Spor, A., Scalfone, N., Fricker, A. D., Stombaugh, J., Knight, R., Angenent, L. T. and Ley, R. E. (2011). Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. U. S. A. 108: 4578–4585.
[38] Davis, M. Y., Zhang, H., Brannan, L. E., Carman, R. J. and Boone, J. H. (2016). Rapid change of fecal microbiome and disappearance of Clostridium difficile in a colonized infant after transition from breast milk to cow milk. Microbiome 4: 53.
[39] Sela, D. A., Chapman, J., Adeuya, A., Kim, J. H., Chen, F., Whitehead, T. R., Lapidusc, A., Rokhsarc, D. S., Lebrillag, C. B., German, J. B., Priced, N. P., Richardsonc, P. M. and Mills, D. A. (2008). The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc. Natl. Acad. Sci. U. S. A. 105: 18964–18969.
[40] Duranti, S., Milani, C., Lugli, G. A., Turroni, F., Mancabelli, L., Sanchez, B., Ferrario, C., Viappiani, A., Mangifesta, M., Mancino, W., Gueimonde, M., Margolles, A., Van Sinderen, D. and Ventura, M. (2015). Insights from genomes of representatives of the human gut commensal Bifidobacterium bifidum. Environ. Microbiol. 17: 2515–2531.
[41] Duranti, S., Turroni, F., Lugli, G. A., Milani, C., Viappiani, A., Mangifesta, M., Gioiosa, L., Palanza, P., Van Sinderen, D. and Ventura, M. (2014). Genomic characterization and transcriptional studies of the starch-utilizing strain Bifidobacterium adolescentis 22 L. Appl. Environ. Microbiol. 80: 6080–6090.
[42] Amarri, S., Benatti, F., Callegari, M. L., Shahkhalili, Y., Chauffard, F., Rochat, F., Shahkhalili, Y., Chauffard, F., Rochat, F., Acheson, K. J., Hager, C., Benyacoub, J., Galli, E., Rebecchi, A. and Morelli, L. (2006). Changes of gut microbiota and immune markers during the complementary feeding period in healthy breast-fed infants. J. Pediatr. Gastroenterol. Nutr. 42: 488–495.
[43] Cummuis, A., Steele, T. W., Labrooy, J. T. and Shearman, D. J. C. (1988). Maturation of the rat small intestine at weaning; changes in epithelial cell kinetics, bacterial flora and mucosal immune activity. Gut 29: 1672-1679.
[44] Luppi, A., Gibellini, M., Gin, T., Vangroenweghe, F., Vandenbroucke, V., Bauerfeind, R., Bonilauri, P., Labarque, G. and Hidalgo, Á. (2016). Prevalence of virulence factors in enterotoxigenic Escherichia coli isolated from pigs with post-weaning diarrhoea in Europe. Porcine Health Manag. 2: 20.
[45] Tsukahara, T. and Ushida, K. (2002). Succinate accumulation in pig large intestine during antibiotic-associated diarrhea and the constitution of succinate-producing flora. J. Gen. Appl. Microbiol. 48: 143–154.
[46] Stokes, C. R., Bailey, M., Haverson, K., Harris, C., Johes, P., Inman, C., Piec, S., Oswaldc, I. P., Williams, B. A., Akkermans, A. D. L., Sowae, E., Rothköttere, H. J., Bevis, G. and Miller, B. G. (2004). Postnatal development of intestinal immune system in piglets: implications for the process of weaning. Anim. Res. 53: 1–10.
[47] Konstantinov, S. R., Awati, A. A., Williams, B. A., Miller, B. G., Jones, P., Stokes, C. R., Akkermans, A. D., Smidt, H. and De Vos, W. M. (2006). Post-natal development of the porcine microbiota composition and activities. Environ. Microbiol. 8: 1191–1199.
[48] Mokoena, M. P. (2017). Lactic acid bacteria and their bacteriocins: classification, biosynthesis and applications against uropathogens: A Mini-Review. Molecules 22: 1255.
[49] Su, Y., Yao, W., Perez-Gutierrez, O. N., Smidt, H. and Zhu, W. Y. (2008). Changes in abundance of Lactobacillus spp. and Streptococcus suis in the stomach, jejunum and ileum of piglets after weaning. FEMS. Microbiol. Ecol. 66: 546–555.
[50] Su, Y. and Zhu, W. Y. (2006). Shifts of total bacterial and lactobacilli community in stomach of sucking and weaned piglets. Par. Ent. Nutr. 13: 1–4.
[51] Hassiotou, F. and Geddes, D. T. (2015). Immune cell–mediated protection of the mammary gland and the infant during breastfeeding. Adv. Nutr. 6: 267–275.
[52] Cacho, N. T. and Lawrence, R. M. (2017). Innate immunity and breast milk. Front. Immunol. 8: 584.
[53] Cummins, A. G., Munro, G. H., Miller, H. R. P. and Ferguson, A. (1988). Association of maturation of the small intestine at weaning with mucosal mast cell activation in the rat. Immunol. Cell Biol. 66: 417-422.
[54] Thompson, F. M., Mayrhofer, G. and Cummins, A. G. (1996). Dependence of epithelial growth of the small intestine on T cell activation during weaning in the rat. Gastroenterology 111: 37–44.
[55] Pie, S., Lalles, J. P. and Blazy, F. (2004). Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. J. Nutr. 134: 641–647.
[56] Villena, J. and Kitazawa, H. (2013). Modulation of intestinal TLR4-inflammatory signalling pathways by probiotic microorganisms: lessons learned from Lactobacillus jensenii TL2937. Front. Immunol. 4: 512.
[57] Henning, S. J. (1981). Postnatal development: coordination of feeding, digestion, and metabolism. Am. J. Physiol. 241: 199–214.
[58] Kikusui, T., Isaka, Y. and Mori, Y. (2005). Early weaning deprives mouse pups of maternal care and decreases their maternal behavior in adulthood. Behav. Brain Res. 162: 200–206.
[59] Fraga, M. C., de Moura, E. G., da Silva Lima, N., Lisboa, P. C., de Oliveira, E., Silva, J. O., Claudio-Neto, S., Filgueiras, C. C., Abreu-Villaça, Y. and Manhães, A. C. (2014). Anxiety-like, novelty-seeking and memory/learning behavioral traits in male Wistar rats submitted to early weaning. Physiol. Behav. 124: 100–106.
[60] Kitchen, I., Leslie, F. M., Kelly, M., Barnes, R., Crook, T. J., Hill, R. G., Borsodi, A., Toth, G., Melchiorri, P. and Negri, L. (1995). Development of delta-opioid receptor subtypes and the regulatory role of weaning: radioligand binding, autoradiography and in situ hybridization studies. J. Pharmacol. Exp. Ther. 275: 1597–1607.
[61] Goody, R. J. and Kitchen, I. (2001). Influence of maternal milk on functional activation of delta-opioid receptors in postnatal rats. J. Pharmacol. Exp. Ther. 296: 744–748.
[62] Neumann, I. D. and Landgraf, R. (2012). Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 35: 649–659.
[63] Curley, J. P., Jordan, E. R., Swaney, W. T., Izraelit, A., Kammel, S. and Champagne, F. A. (2009). The meaning of weaning: influence of the weaning period on behavioral development in mice. Dev. Neurosci. 31: 318–331.
[64] Kikusui, T., Takeuchi, Y. and Mori, Y. (2004). Early weaning induces anxiety and aggression in adult mice. Physiol. Behav. 81: 37–42.
[65] Iwata, E., Kikusui, T., Takeuchi, Y. and Mori, Y. (2007). Fostering and environmental enrichment ameliorate anxious behavior induced by early weaning in Balb/c mice. Physiol. Behav. 91: 318–324.
[66] Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J. and Plotsky, P. M. (2000). Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog. Brain Res. 122: 81–103.
[67] Dallman, M. F., Pecoraro, N., Akana, S. F., La Fleur, S. E., Gomez, F., Houshyar, H., Bell, M. E., Bhatnagar, S., Laugero, K. D. and Manalo, S. (2003). Chronic stress and obesity: a new view of “comfort food”. Proc. Natl. Acad. Sci. U. S. A. 100: 11696–11701.
[68] Jarvis, S., Moinard, C., Robson, S. K., Sumner, B. E. H., Douglas, A. J., Seckl, J. R., Russell, J. and Lawrence, A. B. (2008). Effects of weaning age on the behavioural and neuroendocrine development of piglets. Appl Anim Behav Sci 110: 166–181.
[69] Poletto, R., Steibel, J. P., Siegford, J. M. and Zanella, A. J. (2006). Effects of early weaning and social isolation on the expression of glucocorticoid and mineralocorticoid receptor and 11beta-hydroxysteroid dehydrogenase 1 and 2 mRNAs in the frontal cortex and hippocampus of piglets. Brain Res. 1067: 36–42.
[70] Yuan, Y., Jansen, J., Charles, D. and Zanella, A. J. (2004). The influence of weaning age on post-mixing agonistic interactions in growing pigs. Appl. Anim. Behav. Sci. 88: 39–46.
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