Delivery by caesarean section, rather than vaginal delivery, promotes hepatic steatosis in piglets

Clinical Science

Volumn 118, Issue 1, 2010, Pages 47-59

  Hyde, Matthew J ^a   Griffin, Julian L ^b   Herrera, Emilio ^c   Byrne, Christopher D ^d   Clarke, Lynne ^a   Kemp, Paul R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSIDAD SAN PABLO CEU   (Spain)

^d UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Birth; Caesarean section; Liver; Metabolic syndrome; Steatosis; Total parenteral nutrition (TPN)

Indexed keywords

APOLIPOPROTEIN A1; CHOLESTEROL; CHOLESTEROL ESTER; FATTY ACID; GALANIN LIKE PEPTIDE; GAMMA INTERFERON; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; HYDROXYMETHYLGLUTARYL COENZYME A SYNTHASE; INTERFERON REGULATORY FACTOR 1; PHOSPHOLIPID; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CESAREAN SECTION; DIETARY INTAKE; ENZYME ACTIVITY; FATTY LIVER; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE HOMEOSTASIS; LIPID METABOLISM; LIVER CELL; METABOLOMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PUERPERIUM; TOTAL PARENTERAL NUTRITION; VAGINAL DELIVERY;

ANIMALS; BLOOD GLUCOSE; CESAREAN SECTION; DELIVERY, OBSTETRIC; FATTY LIVER; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GROWTH; HOMEOSTASIS; LIPID METABOLISM; LIVER; MALE; METABOLOMICS; PHENOTYPE; PREGNANCY; SUS SCROFA; TRIIODOTHYRONINE;

EID: 70549092085     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20090169     Document Type: Article

References (56)

1. Richardson, A. and Mmata, C. (2007) NHS Maternity Statistics, England: 2005-2006, Information Centre, Government Statistical Service, Leeds
2. Finger, C. (2003) Caesarean section rates skyrocket in Brazil. Many women are opting for caesareans in the belief that it is a practical solution. Lancet 362, 628
3. Cardwell, C. R., Stene, L. C., Joner, G., Cinek, O., Svensson, J., Goldacre, M. J., Parslow, R. C., Pozzilli, P., Brigis, G., Stoyanov, D. et al. (2008) Caesarean section is associated with an increased risk of childhood-onset type 1 diabetes mellitus: a meta-analysis of observational studies. Diabetologia 51, 726-735
4. Hakansson, S. and Kallen, K. (2003) Caesarean section increases the risk of hospital care in childhood for asthma and gastroenteritis. Clin. Exp. Allergy 33, 757-764
5. Renz-Polster, H., David, M. R., Buist, A. S., Vollmer, W. M., O'Connor, E. A., Frazier, E. A. and Wall, M. A. (2005) Caesarean section delivery and the risk of allergic disorders in childhood. Clin. Exp. Allergy 35, 1466-1472
6. Thavagnanam, S., Fleming, J., Bromley, A., Shields, M. D. and Cardwell, C. R. (2008) A meta-analysis of the association between Caesarean section and childhood asthma. Clin. Exp. Allergy 38, 629-633
7. Utz, R. L. (2008) Can prenatal care prevent childhood obesity?Policy Perpectives, vol, 4, April 30 (http://www.imakenews.com/cppa/ e_article001081327.cfm?x=b6Gdd3k)
8. Hagnevik, K., Faxelius, G., Irestedt, L., Lagercrantz, H., Lundell, B. and Persson, B. (1984) Catecholamine surge and metabolic adaptation in the newborn after vaginal delivery and caesarean section. Acta Paediatr. Scand. 73, 602-609
9. Ward Platt, M. and Deshpande, S. (2005) Metabolic adaptation at birth. Semin. Fetal Neonatal Med. 10, 341-350
10. Burcelin, R., Mrejen, C., Decaux, J. F., De Mouzon, S. H., Girard, J. and Charron, M. J. (1998) In vivo and in vitro regulation of hepatic glucagon receptor mRNA concentration by glucose metabolism. J. Biol. Chem. 273, 8088-8093
11. Mitanchez, D. (2007) Glucose regulation in preterm newborn infants. Horm. Res. 68, 265-271
12. Christensson, K., Siles, C., Cabrera, T., Belaustequi, A., Fuente, P., Lagercrantz, H., Puyol, P. and Winberg, J. (1993) Lower body temperatures in infants delivered by caesarean section than in vaginally delivered infants. Acta Paediatr. 82, 128-131
13. Clarke, L., Heasman, L., Firth, K. and Symonds, M. E. (1997) Influence of route of delivery and ambient temperature on thermoregulation in newborn lambs. Am. J. Physiol. 272, R1931-R1939
14. Targher, G. (2007) Non-alcoholic fatty liver disease, the metabolic syndrome and the risk of cardiovascular disease: the plot thickens. Diabetic Med. 24, 1-6
15. Tonkin, A. M. (2004) The metabolic syndrome(s)? Curr. Atheroscler. Rep. 6, 165-166
16. Lavine, J. E. and Schwimmer, J. B. (2005) NAFLD/NASH in children. Fatty Liver Disease: NASH and Related Disorders, 1st edn. (Farrell, G. C., George, J., Hall, P. M. and McCullough, A. J., eds.), pp. 229-240, Blackwell Publishing, Oxford
17. Barker, D. J. P. (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62-67
18. Shibata, M., Kihara, Y., Taguchi, M., Tashiro, M. and Otsuki, M. (2007) Nonalcoholic fatty liver disease is a risk factor for type 2 diabetes in middle-aged Japanese men. Diabetes Care 30, 2940-2944
19. Utzschneider, K. M. and Kahn, S. E. (2006) The role of insulin resistance in nonalcoholic fatty liver disease. J. Clin. Endocrinol. Metab. 91, 4753-4761
20. Klein, S. (1993) Total parenteral nutrition and the liver. In Disease of the Liver 7th edn (Schiff, L. and Schiff, E., eds.), pp. 1505-1516, Lippincott, Philadelphia
21. Hyde, M. J., Amusquivar, E., Laws, J., Corson, A. M., Geering, R. R., Lean, I. J., Putet, G., Dodds, P. F., Herrera, E. and Clarke, L. (2008) Effects of lipid-supplemented total parenteral nutrition on fatty liver disease in a premature neonatal piglet model. Neonatology 93, 77-86
22. Panadero, M., Vidal, H., Herrera, E. and Bocos, C. (2001) Nutritionally induced changes in the peroxisome proliferator-activated receptor-α gene expression in liver of suckling rats are dependent on insulinaemia. Arch Biochem. Biophys. 394, 182-188
23. Ueda, K., Tanizawa, Y., Ishihara, H., Kizuki, N., Ohta, Y., Matsutani, A. and Oka, Y. (1998) Overexpression of mitochondrial FAD-linked glycerol-3-phosphate dehydrogenase does not correct glucose-stimulated insulin secretion from diabetic GK rat pancreatic islets. Diabetologia 41, 649-653
24. Baly, D. L., Keen, C. L. and Hurley, L. S. (1985) Pyruvate carboxylase and phosphoenolpyruvate carboxykinase activity in developing rats: effect of manganese deficiency. J. Nutr. 115, 872-879
25. Munujos, P., Coll-Canti, J., Gonzalez-Sastre, F. and Gella, F. J. (1993) Assay of succinate dehydrogenase activity by a colorimetric-continuous method using iodonitrotetrazolium chloride as electron acceptor. Anal. Biochem. 212, 506-509
26. Luo, C., Wang, X., Long, J. and Liu, J. (2006) An NADH-tetrazolium-coupled sensitive assay for malate dehydrogenase in mitochondria and crude tissue homogenates. J. Biochem. Biophys. Methods 68, 101-111
27. Casado, J., Remesar, X. and Pastor-Anglada, M. (1987) Hepatic uptake of gluconeogenic substrates in late-pregnant and mid-lactating rats. Biosci. Rep. 7, 587-592
28. 1H-NMR spectroscopy- and mass spectrometry-based metabolomic study of the PPAR-α null mutant mouse defines profound systemic changes in metabolism linked to the metabolic syndrome. Physiol. Genomics 27, 178-186
29. Wishart, D. S., Tzur, D., Knox, C., Eisner, R., Guo, A. C., Young, N., Cheng, D., Jewell, K., Arndt, D., Sawhney, S. et al. (2007) HMDB: the human metabolome database. Nucleic Acids Res. 35, D521-D526
30. Ellis, P. D., Smith, C. W. and Kemp, P. (2004) Regulated tissue-specific alternative splicing of enhanced green fluorescent protein transgenes conferred by α-tropomyosin regulatory elements in transgenic mice. J. Biol. Chem. 279, 36660-36669
31. Shiwaku, K., Hashimoto, M., Kitajima, K., Nogi, A., Anuurad, E., Enkhmaa, B., Kim, J.-M., Kim, I.-S., Lee, S.-K., Oyunsuren, T., Shido, O. and Yamane, Y. (2004) Triglyceride levels are ethnic-specifically associated with an index of stearoyl-CoA desaturase activity and n - 3 PUFA levels in Asians. J. Lipid Res. 45, 914-922
32. Daniel, J. A., Carroll, J. A., Keisler, D. H. and Kojima, C. J. (2008) Evaluation of immune system function in neonatal pigs born vaginally or by Cesarean section. Domest. Anim. Endocrinol. 35, 81-87
33. Brown, M. A., Rad, P. Y. and Halonen, M. J. (2003) Method of birth alters interferon-γ and interleukin-12 production by cord blood mononuclear cells. Pediatr. Allergy Immunol. 14, 106-111
34. Chen, H. H., Lin, J. H., Fung, H. P., Ho, L. L., Yang, P. C., Lee, W. C., Lee, Y. P. and Chu, R. M. (2003) Serum acute phase proteins and swine health status. Can. J. Vet. Res. 67, 283-290
35. Reitz, J., Gehrig-Burger, K., Strauss, J. F. and Gimpl, G. (2008) Cholesterol interaction with the related steroidogenic acute regulatory lipid-transfer (START) domains of StAR (STARD1) and MLN64 (STARD3). FEBS J. 275, 1790-1802
36. Nierhoff, D., Levoci, L., Schulte, S., Goeser, T., Rogler, L. E. and Shafritz, D. A. (2007) New cell surface markers for murine fetal hepatic stem cells identified through high density complementary DNA microarrays. Hepatology 46, 535-547
37. Coerver, K. A., Woodruff, T. K., Finegold, M. J., Mather, J., Bradley, A. and Matzuk, M. M. (1996) Activin signaling through activin receptor type II causes the cachexia- like symptoms in inhibin-deficient mice. Mol. Endocrinol. 10, 534-543
38. Neuschwander-Tetri, B. A. and Caldwell, S. H. (2003) Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference. Hepatology 37, 1202-1219
39. Vestermark, V., Hogdall, C. K., Birch, M., Plenov, G. and Toftager-Larsen, K. (1991) Influence of the mode of delivery on initiation of breast-feeding. Eur. J. Obstet. Gynecol. Reprod. Biol. 38, 33-38
40. Ntambi, J. M., Miyazaki, M., Stoehr, J. P., Lan, H., Kendziorski, C. M., Yandell, B. S., Song, Y., Cohen, P., Friedman, J. M. and Attie, A. D. (2002) Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc. Natl. Acad. Sci. U.S.A. 99, 11482-11486
41. Jiang, H. P. and Serrero, G. (1992) Isolation and characterization of a full-length cDNA coding for an adipose differentiation-related protein. Proc. Natl. Acad. Sci. U.S.A. 89, 7856-7860
42. Gao, J. and Serrero, G. (1999) Adipose differentiation related protein (ADRP) expressed in transfected COS-7 cells selectively stimulates long chain fatty acid uptake. J. Biol. Chem. 274, 16825-16830
43. Imai, Y., Varela, G. M., Jackson, M. B., Graham, M. J., Crooke, R. M. and Ahima, R. S. (2007) Reduction of hepatosteatosis and lipid levels by an adipose differentiation-related protein antisense oligonucleotide. Gastroenterology 132, 1947-1954
44. Toye, A. A., Dumas, M. E., Blancher, C., Rothwell, A. R., Fearnside, J. F., Wilder, S. P., Bihoreau, M. T., Cloarec, O., Azzouzi, I., Young, S. et al. (2007) Subtle metabolic and liver gene transcriptional changes underlie diet-induced fatty liver susceptibility in insulin-resistant mice. Diabetologia 50, 1867-1879
45. Norman, J. E., Bollapragada, S., Yuan, M. and Nelson, S. M. (2007) Inflammatory pathways in the mechanism of parturition. BMC Pregnancy Childbirth 7 (Suppl. 1), S7
46. Haddad, R., Tromp, G., Kuivaniemi, H., Chaiworapongsa, T., Kim, Y. M., Mazor, M. and Romero, R. (2006) Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. Am. J. Obstet. Gynecol. 195, 394 e391-e324
47. Gasparoni, A. (1991) Neutrophil chemotaxis in infants delivered by caesarean section. Eur. J. Pediatr. 150, 481-482
48. Li, Z. and Diehl, A. M. (2003) Innate immunity in the liver. Curr. Opin. Gastroenterol. 19, 565-571
49. Li, Z., Yang, S., Lin, H., Huang, J., Watkins, P. A., Moser, A. B., Desimone, C., Song, X. Y. and Diehl, A. M. (2003) Probiotics and antibodies to TNF inhibit inflammatory activity and improve nonalcoholic fatty liver disease. Hepatology 37, 343-350
50. Yang, S. Q., Lin, H. Z., Lane, M. D., Clemens, M. and Diehl, A. M. (1997) Obesity increases sensitivity to endotoxin liver injury: implications for the pathogenesis of steatohepatitis. Proc. Natl. Acad. Sci. U.S.A. 94, 2557-2562
51. Spengler, R. N., Chensue, S. W., Giacherio, D. A., Blenk, N. and Kunkel, S. L. (1994) Endogenous norepinephrine regulates tumor necrosis factor-α production from macrophages in vitro. J. Immunol. 152, 3024-3031
52. Kageyama, H., Takenoya, F., Kita, T., Hori, T., Guan, J.-L. and Shioda, S. (2005) Galanin-like peptide in the brain: effects on feeding, energy metabolism and reproduction. Regul. Pept. 126, 21-26
53. Abel, R. A., Ronca, A. E. and Alberts, J. R. (1998) Perinatal stimulation facilitates suckling onset in newborn rats. Dev. Psychobiol. 32, 91-99
54. Fowden, A. L., Li, J. and Forhead, A. J. (1998) Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance? Proc. Nutr. Soc. 57, 113-122
55. Dahlquist, G. (1999) Perinatal risk factors for childhood type 1 diabetes in Europe. The Eurodiab Substudy 2 Study Group. Diabetes Care 22, 1698
56. Duee, P. H., Pegorier, J. P., Quant, P. A., Herbin, C., Kohl, C. and Girard, J. (1994) Hepatic ketogenesis in newborn pigs is limited by low mitochondrial 3-hydroxy-3- methylglutaryl-CoA synthase activity. Biochem. J. 298, 207-212