Skip to main content Accessibility help
×
Home

Postnatal nutritional restriction affects growth and immune function of piglets with intra-uterine growth restriction

  • Liang Hu (a1), Yan Liu (a1), Chuan Yan (a1), Xie Peng (a1), Qin Xu (a1), Yue Xuan (a1), Fei Han (a1), Gang Tian (a1), Zhengfeng Fang (a1), Yan Lin (a1), Shengyu Xu (a1), Keying Zhang (a1), Daiwen Chen (a1), De Wu (a1) and Lianqiang Che (a1)...

Abstract

Postnatal rapid growth by excess intake of nutrients has been associated with an increased susceptibility to diseases in neonates with intra-uterine growth restricted (IUGR). The aim of the present study was to determine whether postnatal nutritional restriction could improve intestinal development and immune function of neonates with IUGR using piglets as model. A total of twelve pairs of normal-birth weight (NBW) and IUGR piglets (7 d old) were randomly assigned to receive adequate nutrient intake or restricted nutrient intake (RNI) by artificially liquid feeding for a period of 21 d. Blood samples and intestinal tissues were collected at necropsy and were analysed for morphology, digestive enzyme activities, immune cells and expression of innate immunity-related genes. The results indicated that both IUGR and postnatal nutritional restriction delayed the growth rate during the sucking period. Irrespective of nutrient intake, piglets with IUGR had a significantly lower villous height and crypt depth in the ileum than the NBW piglets. Moreover, IUGR decreased alkaline phosphatase activity while enhanced lactase activity in the jejunum and mRNA expressions of Toll-like receptor 9 (TLR-9) and DNA methyltransferase 1 (DNMT1) in the ileum of piglets. Irrespective of body weight, RNI significantly decreased the number and/or percentage of peripheral leucocytes, lymphocytes and monocytes of piglets, whereas the percentage of neutrophils and the ratio of CD4+ to CD8+ were increased. Furthermore, RNI markedly enhanced the mRNA expression of TLR-9 and DNMT1, but decreased the expression of NOD2 and TRAF-6 in the ileum of piglets. In summary, postnatal nutritional restriction led to abnormal cellular and innate immune response, as well as delayed the growth and intestinal development of IUGR piglets.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Postnatal nutritional restriction affects growth and immune function of piglets with intra-uterine growth restriction
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Postnatal nutritional restriction affects growth and immune function of piglets with intra-uterine growth restriction
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Postnatal nutritional restriction affects growth and immune function of piglets with intra-uterine growth restriction
      Available formats
      ×

Copyright

Corresponding author

* Corresponding author: Associate Professor L. Che, fax +86 28 86291256; email clianqiang@hotmail.com

References

Hide All
1 Wu, G, Bazer, FW, Wallace, JM, et al. (2006) Board-invited review: intrauterine growth retardation: implications for the animal sciences. J Anim Sci 84, 23162337.
2 McMillen, IC & Robinson, JS (2005) Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev 85, 571633.
3 Aucott, SW, Donohue, PK & Northington, FJ (2004) Increased morbidity in severe early intrauterine growth restriction. J Perinatol 24, 435440.
4 Garite, TJ, Clark, R & Thorp, JA (2004) Intrauterine growth restriction increases morbidity and mortality among premature neonates. Am J Obstet Gynecol 191, 481487.
5 Cromi, A, Ghezzi, F, Raffaelli, R, et al. (2009) Ultrasonographic measurement of thymus size in IUGR fetuses: a marker of the fetal immunoendocrine response to malnutrition. Ultrasound Obstet Gynecol 33, 421426.
6 Raqib, R, Alam, DS, Sarker, P, et al. (2007) Low birth weight is associated with altered immune function in rural Bangladeshi children: a birth cohort study. Am J Clin Nutr 85, 845852.
7 Manerikar, SS, Malaviya, AN, Singh, MB, et al. (1976) Immune status and BCG vaccination in newborns with intra-uterine growth retardation. Clin Exp Immunol 26, 173175.
8 Ferguson, AC (1978) Prolonged impairment of cellular immunity in children with intrauterine growth retardation. J Pediatr 93, 5256.
9 Contreras, YM, Yu, X, Hale, MA, et al. (2011) Intrauterine growth restriction alters T-lymphocyte cell number and dual specificity phosphatase 1 levels in the thymus of newborn and juvenile rats. Pediatr Res 70, 123129.
10 Gao, F, Liu, Y, Zhang, C, et al. (2013) Effect of intrauterine growth restriction during late pregnancy on the growth performance, blood components, immunity and anti-oxidation capability of ovine fetus. Livest Sci 155, 435441.
11 Claris, O, Beltrand, J & Levy-Marchal, C (2010) Consequences of intrauterine growth and early neonatal catch-up growth. Semin Perinatol 34, 207210.
12 Shahkhalili, Y, Moulin, J, Zbinden, I, et al. (2010) Comparison of two models of intrauterine growth restriction for early catch-up growth and later development of glucose intolerance and obesity in rats. Am J Physiol Regul Integr Comp Physiol 298, R141R146.
13 Berends, LM, Fernandez-Twinn, DS, Martin-Gronert, MS, et al. (2013) Catch-up growth following intra-uterine growth-restriction programmes an insulin-resistant phenotype in adipose tissue. Int J Obes (Lond) 37, 10511057.
14 Han, F, Hu, L, Xuan, Y, et al. (2013) Effects of high nutrient intake on the growth performance, intestinal morphology and immune function of neonatal intra-uterine growth-retarded pigs. Br J Nutr 110, 18191827.
15 Dai, Y, Thamotharan, S, Garg, M, et al. (2012) Superimposition of postnatal calorie restriction protects the aging male intrauterine growth-restricted offspring from metabolic maladaptations. Endocrinology 153, 42164226.
16 Desai, M, Gayle, D, Babu, J, et al. (2005) Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am J Physiol Regul Integr Comp Physiol 288, R91R96.
17 Guo, Y, Li, W & Chen, J (2010) Influence of nutrient density and lighting regime in broiler chickens: effect on antioxidant status and immune function. Br Poult Sci 51, 222228.
18 Messaoudi, I, Warner, J, Fischer, M, et al. (2006) Delay of T cell senescence by caloric restriction in aged long-lived nonhuman primates. Proc Natl Acad Sci U S A 103, 1944819453.
19 Jolly, CA (2004) Dietary restriction and immune function. J Nutr 134, 18531856.
20 Zhong, X, Li, W, Huang, X, et al. (2012) Impairment of cellular immunity is associated with overexpression of heat shock protein 70 in neonatal pigs with intrauterine growth retardation. Cell Stress Chaperones 17, 495505.
21 Sangild, PT (2006) Gut responses to enteral nutrition in preterm infants and animals. Exp Biol Med (Maywood) 231, 16951711.
22 Ferenc, K, Pietrzak, P, Godlewski, MM, et al. (2014) Intrauterine growth retarded piglet as a model for humans – studies on the perinatal development of the gut structure and function. Reprod Biol 14, 5160.
23 Che, L, Thymann, T, Bering, SB, et al. (2010) IUGR does not predispose to necrotizing enterocolitis or compromise postnatal intestinal adaptation in preterm pigs. Pediatr Res 67, 5459.
24 Chen, Y, Chen, D, Tian, G, et al. (2012) Dietary arginine supplementation alleviates immune challenge induced by Salmonella enterica serovar Choleraesuis bacterin potentially through the Toll-like receptor 4-myeloid differentiation factor 88 signalling pathway in weaned piglets. Br J Nutr 108, 10691076.
25 Livak, KJ & Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔC t method. Methods 25, 402408.
26 D'Inca, R, Gras-Le Guen, C, Che, L, et al. (2011) Intrauterine growth restriction delays feeding-induced gut adaptation in term newborn pigs. Neonatology 99, 208216.
27 Wang, J, Chen, L, Li, D, et al. (2008) Intrauterine growth restriction affects the proteomes of the small intestine, liver, and skeletal muscle in newborn pigs. J Nutr 138, 6066.
28 Morise, A, Seve, B, Mace, K, et al. (2011) Growth, body composition and hormonal status of growing pigs exhibiting a normal or small weight at birth and exposed to a neonatal diet enriched in proteins. Br J Nutr 105, 14711479.
29 Alvarenga, AL, Chiarini-Garcia, H, Cardeal, PC, et al. (2013) Intra-uterine growth retardation affects birthweight and postnatal development in pigs, impairing muscle accretion, duodenal mucosa morphology and carcass traits. Reprod Fertil Dev 25, 387395.
30 Monaghan, P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B Biol Sci 363, 16351645.
31 Maruyama, K & Koizumi, T (2001) Superior mesenteric artery blood flow velocity in small for gestational age infants of very low birth weight during the early neonatal period. J Perinat Med 29, 6470.
32 Xu, RJ, Mellor, DJ, Birtles, MJ, et al. (1994) Impact of intrauterine growth retardation on the gastrointestinal tract and the pancreas in newborn pigs. J Pediatr Gastroenterol Nutr 18, 231240.
33 Wang, T, Huo, YJ, Shi, F, et al. (2005) Effects of intrauterine growth retardation on development of the gastrointestinal tract in neonatal pigs. Biol Neonate 88, 6672.
34 Burrin, DG, Stoll, B, Chang, X, et al. (2003) Parenteral nutrition results in impaired lactose digestion and hexose absorption when enteral feeding is initiated in infant pigs. Am J Clin Nutr 78, 461470.
35 Goldberg, RF, Austen, WG Jr, Zhang, X, et al. (2008) Intestinal alkaline phosphatase is a gut mucosal defense factor maintained by enteral nutrition. Proc Natl Acad Sci U S A 105, 35513556.
36 Qiu, XS, Huang, TT, Shen, ZY, et al. (2005) Effect of early nutrition on intestine development of intrauterine growth retardation in rats and its correlation to leptin. World J Gastroenterol 11, 44194422.
37 Suarez-Souto, MA, Lara-Padilla, E, Reyna-Garfias, H, et al. (2012) Caloric restriction modifies both innate and adaptive immunity in the mouse small intestine. J Physiol Biochem 68, 163173.
38 Fukata, M, Vamadevan, AS & Abreu, MT (2009) Toll-like receptors (TLRs) and Nod-like receptors (NLRs) in inflammatory disorders. Semin Immunol 21, 242253.
39 Athman, R & Philpott, D (2004) Innate immunity via Toll-like receptors and Nod proteins. Curr Opin Microbiol 7, 2532.
40 Garg, M, Thamotharan, M, Dai, Y, et al. (2012) Early postnatal caloric restriction protects adult male intrauterine growth-restricted offspring from obesity. Diabetes 61, 13911398.
41 Pham, TD, MacLennan, NK, Chiu, CT, et al. (2003) Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol 285, R962R970.
42 Comans-Bitter, WM, de Groot, R, van den Beemd, R, et al. (1997) Immunophenotyping of blood lymphocytes in childhood. Reference values for lymphocyte subpopulations. J Pediatr 130, 388393.
43 Deng, Y, Cui, H, Peng, X, et al. (2011) Effect of dietary vanadium on cecal tonsil T cell subsets and IL-2 contents in broilers. Biol Trace Elem Res 144, 647656.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed