Table of Contents
ISRN Gastroenterology
Volume 2011, Article ID 592404, 11 pages
http://dx.doi.org/10.5402/2011/592404
Review Article

Obesity, Visceral Fat, and NAFLD: Querying the Role of Adipokines in the Progression of Nonalcoholic Fatty Liver Disease

SpR Surgery, Ninewells Hospital, 65 Lister Court, Dundee DD2 1UY, UK

Received 4 April 2011; Accepted 1 May 2011

Academic Editors: K. D. Mullen, C. T. Shun, and W. Vogel

Copyright © 2011 M. S. Mirza. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. C. Seidell, “Epidemiology of obesity,” Seminars in Vascular Medicine, vol. 5, no. 1, pp. 3–14, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. The World Health Organization, “Preventing and managing the global epidemic,” WHO Technical Report Series 894, Geneva, Switzerland, 2000. View at Google Scholar
  3. J. G. Kral, F. Schaffner, R. N. Pierson, and J. Wang, “Body fat topography as an independent predictor of fatty liver,” Metabolism, vol. 42, no. 5, pp. 548–551, 1993. View at Publisher · View at Google Scholar · View at Scopus
  4. G. Ramsey-Stuart, “Hepatic steatosis and morbid obesity,” Obesity Surgery, vol. 3, no. 2, pp. 157–159, 1993. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. W. van Steenbergen and S. Lanckmans, “Liver disturbances in obesity and diabetes mellitus,” International Journal of Obesity, vol. 19, supplement 1, pp. S27–S36, 1995. View at Google Scholar · View at Scopus
  6. A. M. Wolf, B. Busch, H. W. Kuhlmann, and U. Beisiegel, “Histological changes in the liver of morbidly obese patients: correlation with metabolic parameters,” Obesity Surgery, vol. 15, no. 2, pp. 228–237, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. W. I. Youssef and A. J. McCullough, “Steatohepatitis in obese individuals,” Best Practice and Research in Clinical Gastroenterology, vol. 16, no. 5, pp. 733–747, 2002. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Festi, A. Colecchia, T. Sacco, M. Bondi, E. Roda, and G. Marchesini, “Hepatic steatosis in obese patients: clinical aspects and prognostic significance,” Obesity Reviews, vol. 5, no. 1, pp. 27–42, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. C. J. Lyon, R. E. Law, and W. A. Hsueh, “Minireview: adiposity, inflammation, and atherogenesis,” Endocrinology, vol. 144, no. 6, pp. 2195–2200, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Mora and J. E. Pessin, “An adipocentric view of signaling and intracellular trafficking,” Diabetes/Metabolism Research and Reviews, vol. 18, no. 5, pp. 345–356, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. E. M. Brunt, “Nonalcoholic steatohepatitis,” Seminars in Liver Disease, vol. 24, no. 1, pp. 3–20, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. A. Lonardo, “Fatty liver and nonalcoholic steatohepatitis: where do we stand and where are we going?” Digestive Diseases, vol. 17, no. 2, pp. 80–89, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Marchesini, E. Bugianesi, G. Forlani et al., “Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome,” Hepatology, vol. 37, no. 4, pp. 917–923, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  14. P. Marceau, S. Biron, F. S. Hould et al., “Liver pathology and the metabolic syndrome X in severe obesity,” Journal of Clinical Endocrinology and Metabolism, vol. 84, no. 5, pp. 1513–1517, 1999. View at Google Scholar · View at Scopus
  15. K. G. M. M. Alberti, P. Zimmet, and J. Shaw, “The metabolic syndrome—a new worldwide definition,” Lancet, vol. 366, no. 9491, pp. 1059–1062, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. R. H. Eckel, S. M. Grundy, and P. Z. Zimmet, “The metabolic syndrome,” Lancet, vol. 365, no. 9468, pp. 1415–1428, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. Y. Matsuzawa, T. Funahashi, and T. Nakamura, “Molecular mechanism of metabolic syndrome X: contribution of adipocytokines·adipocyte-derived bioactive substances,” Annals of the New York Academy of Sciences, vol. 892, pp. 146–154, 1999. View at Google Scholar · View at Scopus
  18. R. H. Unger, “Lipid overload and overflow: metabolic trauma and the metabolic syndrome,” Trends in Endocrinology and Metabolism, vol. 14, no. 9, pp. 398–403, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. J. A. Cases, I. Gabriely, X. H. Ma et al., “Physiological increase in plasma leptin markedly inhibits insulin secretion in vivo,” Diabetes, vol. 50, no. 2, pp. 348–352, 2001. View at Google Scholar · View at Scopus
  20. J. Seufert, “Leptin effects on pancreatic β-cell gene expression and function,” Diabetes, vol. 53, no. 1, pp. 152–158, 2004. View at Google Scholar · View at Scopus
  21. P. Z. Zimmet, K. G. M. M. Alberti, and J. Shaw, “A new IDF worldwide definition of the metabolic syndrome: the rationale and the results,” Diabetes Voice, vol. 50, no. 3, pp. 31–33, 2005. View at Google Scholar
  22. E. S. Ford, W. H. Giles, and W. H. Dietz, “Prevalence of the metabolic syndrome among US adults: findings from the third National Health and Nutrition Examination Survey,” Journal of the American Medical Association, vol. 287, no. 3, pp. 356–359, 2002. View at Google Scholar
  23. P. Arner, “Regional adiposity in man,” Journal of Endocrinology, vol. 155, no. 11, pp. 191–192, 1997. View at Google Scholar
  24. P. Arner, “Differences in lipolysis between human subcutaneous and omental adipose tissues,” Annals of Medicine, vol. 27, no. 4, pp. 435–438, 1995. View at Google Scholar
  25. B. L. Wajchenberg, “Subcutaneous and visceral adipose tissue: Their relation to the metabolic syndrome,” Endocrine Reviews, vol. 21, no. 6, pp. 697–738, 2000. View at Publisher · View at Google Scholar
  26. J. N. Fain, A. K. Madan, M. L. Hiler, P. Cheema, and S. W. Bahouth, “Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans,” Endocrinology, vol. 145, no. 5, pp. 2273–2282, 2004. View at Publisher · View at Google Scholar · View at PubMed
  27. E. Dusserre, P. Moulin, and H. Vidal, “Differences in mRNA expression of the proteins secreted by the adipocytes in human subcutaneous and visceral adipose tissues,” Biochimica Biophysica Acta, vol. 1500, no. 1, pp. 88–96, 2000. View at Publisher · View at Google Scholar
  28. A. S. Lihn, J. M. Bruun, G. He, S. B. Pedersen, P. F. Jensen, and B. Richelsen, “Lower expression of adiponectin mRNA in visceral adipose tissue in lean and obese subjects,” Molecular and Cellular Endocrinology, vol. 219, no. 1-2, pp. 9–15, 2004. View at Publisher · View at Google Scholar · View at PubMed
  29. A. Schaffler, J. Scholmerich, and C. Buchler, “Mechanisms of disease: adipocytokines and visceral adipose tissue—emerging role in nonalcoholic fatty liver disease,” Nature Clinical Practice Gastroenterology and Hepatology, vol. 2, no. 6, pp. 273–280, 2005. View at Publisher · View at Google Scholar · View at PubMed
  30. C. T. Montague, J. B. Prins, L. Sanders et al., “Depot-related gene expression in human subcutaneous and omental adipocytes,” Diabetes, vol. 47, no. 9, pp. 1384–1391, 1998. View at Google Scholar
  31. V. van Harmelen, A. Dicker, M. Rydén et al., “Increased lipolysis and decreased leptin production by human omental as compared with subcutaneous preadipocytes,” Diabetes, vol. 51, no. 7, pp. 2029–2036, 2002. View at Google Scholar
  32. J. M. Bruun, A. S. Lihn, A. K. Madan et al., “Higher production of IL-8 in visceral vs. subcutaneous adipose tissue. implication of nonadipose cells in adipose tissue,” American Journal of Physiology Endocrinology and Metabolism, vol. 286, no. 1, pp. E8–E13, 2004. View at Google Scholar
  33. J. M. Bruun, A. S. Lihn, S. B. Pedersen, and B. Richelsen, “Monocyte chemoattractant protein-1 release is higher in visceral than subcutaneous human adipose tissue (AT): implication of macrophages resident in the AT,” Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 4, pp. 2282–2289, 2005. View at Publisher · View at Google Scholar · View at PubMed
  34. J. K. Sethi and A. Vidal-Puig, “Visfatin: the missing link between intra-abdominal obesity and diabetes?” Trends in Molecular Medicine, vol. 11, no. 8, pp. 344–347, 2005. View at Publisher · View at Google Scholar · View at PubMed
  35. A. M. Lefebvre, M. Laville, N. Vega et al., “Depot-specific differences in adipose tissue gene expression in lean and obese subjects,” Diabetes, vol. 47, no. 1, pp. 98–103, 1998. View at Google Scholar
  36. C. T. Montague, J. B. Prins, L. Sanders, J. E. Digby, and S. O'Rahilly, “Depot- and sex-specific differences in human leptin mRNA expression,” Diabetes, vol. 46, no. 3, pp. 342–347, 1997. View at Google Scholar
  37. R. Z. Yang, M. J. Lee, H. Hu et al., “Identification of omentin as a novel depot-specific adipokine in human adipose tissue: possible role in modulating insulin action,” American Journal of Physiology, vol. 290, no. 6, pp. E1253–E1261, 2006. View at Publisher · View at Google Scholar · View at PubMed
  38. B. A. Neuschwander-Tetri and S. H. Caldwell, “Nonalcoholic steatohepatitis: summary of an AASLD Single topic conference,” Hepatology, vol. 37, no. 5, pp. 1202–1219, 2003. View at Publisher · View at Google Scholar · View at PubMed
  39. E. M. Brunt, C. G. Janney, A. M. Di Bisceglie, B. A. Neuschwander-Tetri, and B. R. Bacon, “Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions,” American Journal of Gastroenterology, vol. 94, no. 9, pp. 2467–2474, 1999. View at Publisher · View at Google Scholar · View at PubMed
  40. C. A. Matteoni, Z. M. Younossi, T. Gramlich, N. Boparai, Y. Chang Liu, and A. J. McCullough, “Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity,” Gastroenterology, vol. 116, no. 6, pp. 1413–1419, 1999. View at Publisher · View at Google Scholar
  41. F. Angelico, M. Del Ben, R. Conti et al., “Non-alcoholic fatty liver syndrome: a hepatic consequence of common metabolic diseases,” Journal of Gastroenterology and Hepatology, vol. 18, no. 5, pp. 588–594, 2003. View at Publisher · View at Google Scholar
  42. G. Pagano, G. Pacini, G. Musso et al., “Nonalcoholic steatohepatitis, insulin resistance, and metabolic syndrome: further evidence for an etiologic association,” Hepatology, vol. 35, no. 2, pp. 367–372, 2002. View at Publisher · View at Google Scholar · View at PubMed
  43. S. Chitturi, S. Abeygunasekera, G. C. Farrell et al., “NASH and insulin resistance: insulin hypersecretion and specific association with the insulin resistance syndrome,” Hepatology, vol. 35, no. 2, pp. 373–379, 2002. View at Publisher · View at Google Scholar · View at PubMed
  44. E. S. Freedland, “Role of a critical visceral adipose tissue threshold (CVATT) in metabolic syndrome: implications for controlling dietary carbohydrates: a review,” Nutrition and Metabolism, vol. 1, no. 12, pp. 1–24, 2004. View at Publisher · View at Google Scholar · View at PubMed
  45. A. H. Kissebah and G. R. Krakower, “Regional adiposity and morbidity,” Physiological Reviews, vol. 74, no. 4, pp. 761–811, 1994. View at Google Scholar
  46. P. Arner, “Not all fat is alike,” Lancet, vol. 351, no. 9112, pp. 1301–1302, 1998. View at Publisher · View at Google Scholar
  47. A. H. Kissebah, N. Vydelingum, R. Murray, D. J. Evans, A. J. Hartz, and R. K. Kalkhoff, “Relation of body fat distribution to metabolic complications of obesitof obesity,” The Journal of Clinical Endocrinology Metabolism, vol. 54, no. 2, pp. 254–260, 1982. View at Google Scholar
  48. S. Nielsen, Z. Guo, C. M. Johnson, D. D. Hensrud, and M. D. Jensen, “Splanchnic lipolysis in human obesity,” Journal of Clinical Investigation, vol. 113, no. 11, pp. 1582–1588, 2004. View at Publisher · View at Google Scholar
  49. E. E. Kershaw and J. S. Flier, “Adipose tissue as an endocrine organ,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 6, pp. 2548–2556, 2004. View at Publisher · View at Google Scholar · View at PubMed
  50. K. S. Park, B. D. Rhee, H. K. Lee, C. S. Koh, and H. K. Min, “Intraabdominal fat is associated with decreased insulin sensitivity in healthy young men,” Metabolism, vol. 40, no. 6, pp. 600–603, 1991. View at Publisher · View at Google Scholar
  51. R. W. Bergstrom, L. L. Newell-Morris, D. L. Leonetti, W. P. Shuman, P. W. Wahl, and W. Y. Fujimoto, “Association of elevated fasting C-peptide level and increased intra-abdominal fat distribution with development of NIDDM in Japanese-American men,” Diabetes, vol. 39, no. 1, pp. 104–111, 1990. View at Google Scholar
  52. C. Couillard, N. Bergeron, D. Prud'Homme et al., “Postprandial triglyceride response in visceral obesity in men,” Diabetes, vol. 47, no. 6, pp. 953–960, 1998. View at Publisher · View at Google Scholar
  53. H. Hauner, “Biology of obesity—secretory factors from human adipose tissue and their functional role,” Proceedings of the Nutrition Society, vol. 64, no. 2, pp. 163–169, 2005. View at Publisher · View at Google Scholar
  54. M. Lundgren, J. Buren, T. Ruge, T. Myrnas, and J. W. Eriksson, “Glucocorticoids down-regulate glucose uptake capacity and insulin-signaling proteins in omental but not subcutaneous human adipocytes,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 6, pp. 2989–2997, 2004. View at Publisher · View at Google Scholar · View at PubMed
  55. F. Giorgino, L. Laviola, and J. W. Eriksson, “Regional differences of insulin action in adipose tissue: insights from in vivo and in vitro studies,” Acta Physiologica Scandinavica, vol. 183, no. 1, pp. 13–30, 2005. View at Publisher · View at Google Scholar · View at PubMed
  56. M. Garaulet, J. J. Hernandez-Morante, J. Lujan, F. J. Tebar, and S. Zamora, “Relationship between fat cell size and number and fatty acid composition in adipose tissue from different fat depots in overweight/obese humans,” International Journal of Obesity, pp. 1–7, 2006. View at Publisher · View at Google Scholar · View at PubMed
  57. S. K. Fried, D. A. Bunkin, and A. S. Greenberg, “Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid,” Journal of Clinical Endocrinology and Metabolism, vol. 83, no. 3, pp. 847–850, 1998. View at Publisher · View at Google Scholar
  58. V. Van Harmelen, S. Reynisdottir, P. Eriksson et al., “Leptin secretion from subcutaneous and visceral adipose tissue in women,” Diabetes, vol. 47, no. 6, pp. 913–917, 1998. View at Publisher · View at Google Scholar
  59. V. Van Harmelen, K. Rohrig, and H. Hauner, “Comparison of proliferation and differentiation capacity of human adipocyte precursor cells from the omental and subcutaneous adipose tissue depot of obese subjectss,” Metabolism, vol. 53, no. 5, pp. 632–637, 2004. View at Publisher · View at Google Scholar
  60. B. L. Wajchenberg, D. Giannella-Neto, M. E. R. da Silva, and R. F. Santos, “Depot-specific hormonal characteristics of subcutaneous and visceral adipose tissue and their relation to the metabolic syndrome,” Hormone and Metabolic Research, vol. 34, no. 11-12, pp. 616–621, 2002. View at Publisher · View at Google Scholar · View at PubMed
  61. V. Mohamed-Ali, J. H. Pinkney, and S. W. Coppack, “Adipose tissue as an endocrine and paracrine organ,” International Journal of Obesity, vol. 22, no. 12, pp. 1145–1158, 1998. View at Google Scholar
  62. P. Arner, “Regulation of lipolysis in fat cells,” Diabetes Reviews, vol. 4, no. 4, pp. 450–463, 1996. View at Google Scholar
  63. M. L. Martin and M. D. Jensen, “Effects of body fat distribution on regional lipolysis in obesity,” Journal of Clinical Investigation, vol. 88, no. 2, pp. 609–613, 1991. View at Google Scholar
  64. P. Marin, B. Andersson, M. Ottosson et al., “The morphology and metabolism of intraabdominal adipose tissue in men,” Metabolism, vol. 41, no. 11, pp. 1242–1248, 1992. View at Publisher · View at Google Scholar
  65. J. Ostman, P. Arner, P. Engfeldt, and L. Kager, “Regional differences in the control of lipolysis in human adipose tissue,” Metabolism, vol. 28, no. 12, pp. 1198–1205, 1979. View at Google Scholar
  66. H. Wahrenberg, F. Lonnqvist, and P. Arner, “Mechanisms underlying regional differences in lipolysis in human adipose tissue,” Journal of Clinical Investigation, vol. 84, no. 2, pp. 458–467, 1989. View at Google Scholar
  67. J. Bolinder, L. Kager, J. Ostman, and P. Arner, “Differences at the receptor and postreceptor levels between human omental and subcutaneous adipose tissue in the action of insulin on lipolysis,” Diabetes, vol. 32, no. 2, pp. 117–123, 1983. View at Google Scholar
  68. B. Richelsen, S. B. Pedersen, T. Moller-Pedersen, and J. F. Bak, “Regional differences in triglyceride breakdown in human adipose tissue: effects of catecholamines, insulin, and prostaglandin e2,” Metabolism, vol. 40, no. 9, pp. 990–996, 1991. View at Publisher · View at Google Scholar
  69. M. Rebuffe-Scrive, M. Bronnegard, A. Nilsson, J. Eldh, J. A. Gustafsson, and P. Bjorntorp, “Steroid hormone receptors in human adipose tissues,” Journal of Clinical Endocrinology and Metabolism, vol. 71, no. 5, pp. 1215–1219, 1990. View at Google Scholar
  70. S. K. Fried, C. D. Russell, N. L. Grauso, and R. E. Brolin, “Lipoprotein lipase regulation by insulin and glucocorticoid in subcutaneous and omental adipose tissues of obese women and men,” Journal of Clinical Investigation, vol. 92, no. 5, pp. 2191–2198, 1993. View at Google Scholar
  71. P. Arner, “Regional differences in protein production by human adipose tissue,” Biochemical Society Transactions, vol. 29, no. 2, pp. 72–75, 2001. View at Publisher · View at Google Scholar
  72. P. Trayhurn and I. S. Wood, “Adipokines: inflammation and the pleiotropic role of white adipose tissue,” British Journal of Nutrition, vol. 92, no. 3, pp. 347–355, 2004. View at Publisher · View at Google Scholar
  73. J. S. Yudkin, C. D. A. Stehouwer, J. J. Emeis, and S. W. Coppack, “C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue?” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 19, no. 4, pp. 972–978, 1999. View at Google Scholar
  74. M. W. Rajala and P. E. Scherer, “Minireview: the adipocyte—at the crossroads of energy homeostasis, inflammation, and atherosclerosis,” Endocrinology, vol. 144, no. 9, pp. 3765–3773, 2003. View at Publisher · View at Google Scholar
  75. P. Trayhurn and I. S. Wood, “Signalling role of adipose tissue: adipokines and inflammation in obesity,” Biochemical Society Transactions, vol. 33, no. 5, pp. 1078–1081, 2005. View at Publisher · View at Google Scholar · View at PubMed
  76. J. S. Yudkin, “Adipose tissue, insulin action and vascular disease: inflammatory signals,” International Journal of Obesity, vol. 27, no. 3, pp. S25–S28, 2003. View at Publisher · View at Google Scholar
  77. S. P. Weisberg, D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante Jr., “Obesity is associated with macrophage accumulation in adipose tissue,” Journal of Clinical Investigation, vol. 112, no. 12, pp. 1796–1808, 2003. View at Publisher · View at Google Scholar · View at PubMed
  78. H. Xu, G. T. Barnes, Q. Yang et al., “Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance,” Journal of Clinical Investigation, vol. 112, no. 12, pp. 1821–1830, 2003. View at Publisher · View at Google Scholar · View at PubMed
  79. P. Haynes, S. Liangpunsakul, and N. Chalasani, “Nonalcoholic fatty liver disease in individuals with severe obesity,” Clinics in Liver Disease, vol. 8, no. 3, pp. 535–547, 2004. View at Publisher · View at Google Scholar · View at PubMed
  80. A. E. Reid, “Nonalcoholic steatohepatitis,” Gastroenterology, vol. 121, no. 3, pp. 710–723, 2001. View at Google Scholar
  81. T. Gramlich, D. E. Kleiner, A. J. McCullough, C. A. Matteoni, N. Boparai, and Z. M. Younossi, “Pathologic features associated with fibrosis in nonalcoholic fatty liver disease,” Human Pathology, vol. 35, no. 2, pp. 196–199, 2004. View at Publisher · View at Google Scholar
  82. M. Charlton, “Nonalcoholic fatty liver disease: a review of current understanding and future impact,” Clinical Gastroenterology and Hepatology, vol. 2, no. 12, pp. 1048–1058, 2004. View at Publisher · View at Google Scholar
  83. G. A. Abrams, S. S. Kunde, A. J. Lazenby, and R. H. Clements, “Portal fibrosis and hepatic steatosis in morbidly obese subjects: a spectrum of nonalcoholic fatty liver disease,” Hepatology, vol. 40, no. 2, pp. 475–483, 2004. View at Publisher · View at Google Scholar · View at PubMed
  84. S. Zelman, “The Liver in obesity,” Archives of Internal Medicine, vol. 90, no. 4, pp. 141–156, 1952. View at Publisher · View at Google Scholar · View at PubMed
  85. M. Adler and F. Schaffner, “Fatty liver hepatitis and cirrhosis in obese patients,” American Journal of Medicine, vol. 67, no. 5, pp. 811–816, 1979. View at Google Scholar
  86. J. M. Campbell, T. K. Hunt, J. H. Karam, and P. H. Forsham, “Jejunoileal bypass as a treatment of morbid obesity,” Archives of Internal Medicine, vol. 137, no. 5, pp. 602–610, 1977. View at Publisher · View at Google Scholar
  87. W. H. Kern, A. H. Heger, and J. H. Payne, “Fatty metamorphosis of the liver in morbid obesity,” Archives of Pathology and Laboratory Medicine, vol. 96, no. 5, pp. 342–346, 1973. View at Google Scholar
  88. T. Andersen and C. Gluud, “Liver morphology in morbid obesity: a literature study,” International Journal of Obesity, vol. 8, no. 2, pp. 97–106, 1984. View at Google Scholar
  89. J. B. Dixon, P. S. Bhathal, and P. E. O'Brien, “Nonalcoholic fatty liver disease: predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obese,” Gastroenterology, vol. 121, no. 1, pp. 91–100, 2001. View at Google Scholar
  90. L. Adamson, E. Bell, P. Kaye, K. Neal, S. D. Ryder, and A. Bennett, “Portal inflammtion in non-alcoholic fatty liver disease—is it a marker of a second hit?” Hepatology, vol. 42, p. 615A, 2005. View at Google Scholar
  91. A. J. Sanyal, “AGA technical review on nonalcoholic fatty liver disease,” Gastroenterology, vol. 123, no. 5, pp. 1705–1725, 2002. View at Google Scholar
  92. R. L. Peters, T. Gay, and T. B. Reynolds, “Post jejunoileal bypass hepatic disease. its similarity to alcoholic hepatic disease,” American Journal of Clinical Pathology, vol. 63, no. 3, pp. 318–331, 1975. View at Google Scholar
  93. J. Ludwig, T. R. Viggiano, D. B. McGill, and B. J. Ott, “Nonalcoholic steatohepatitis. mayo clinic experiences with a hitherto unnamed disease,” Mayo Clinic Proceedings, vol. 55, no. 7, pp. 434–438, 1980. View at Google Scholar
  94. K. Seki, Y. Minami, and M. Nishikawa, ““Nonalcoholic steatohepatitis” induced by massive doses of synthetic estrogen,” Gastroenterologia Japonica, vol. 18, no. 3, pp. 197–203, 1983. View at Google Scholar
  95. G. M. Novaro, “Isoniazid and nonalcoholic steatohepatitis,” Journal of Clinical Gastroenterology, vol. 28, no. 2, p. 180, 1999. View at Google Scholar
  96. J. B. Simon, P. N. Manley, J. F. Brien, and P. W. Armstrong, “Amiodarone hepatotoxicity simulating alcoholic liver disease,” New England Journal of Medicine, vol. 311, no. 3, pp. 167–172, 1984. View at Google Scholar
  97. B. R. Bacon, M. J. Farahvash, C. G. Janney, and B. A. Neuschwander-Tetri, “Nonalcoholic steatohepatitis: an expanded clinical entity,” Gastroenterology, vol. 107, no. 4, pp. 1103–1109, 1994. View at Google Scholar
  98. A. J. McCullough, “Update on nonalcoholic fatty liver disease,” Journal of Clinical Gastroenterology, vol. 34, no. 3, pp. 255–262, 2002. View at Publisher · View at Google Scholar
  99. A. Brallion, J. P. Capron, M. A. Herve, C. Degot, and C. Quenum, “Liver in obesity,” Gut, vol. 26, pp. 133–139, 1985. View at Google Scholar
  100. C. Garcia-Monzon, E. Martin-Perez, O. L. Iacono et al., “Characterization of pathogenic and prognostic factors of nonalcoholic steatohepatitis associated obesity,” Journal of Hepatology, vol. 33, no. 5, pp. 716–724, 2000. View at Publisher · View at Google Scholar
  101. F. H. Luyckx, C. Desaive, A. Thiry, W. Dewe, A. J. Scheen, and J. E. Gielen, “Liver abnormalities in severly obese subjects. Effects of drastic weight loss after gastroplasty,” International Journal of Obesity, vol. 22, pp. 222–226, 1998. View at Google Scholar
  102. S. H. Caldwell, D. H. Oelsner, J. C. Iezzoni, E. E. Hespenheide, E. H. Battle, and C. J. Driscoll, “Cryptogenic cirrhosis: clinical characterization and risk factors for underlying disease,” Hepatology, vol. 29, no. 3, pp. 664–669, 1999. View at Google Scholar
  103. A. Poonawala, S. P. Nair, and P. J. Thuluvath, “Prevalence of obesity and diabetes in patients with cryptogenic cirrhosis: a case-control study,” Hepatology, vol. 32, no. 4 I, pp. 689–692, 2000. View at Google Scholar
  104. F. H. Luyckx, P. J. Lefebvre, and A. J. Scheen, “Non-alcoholic steatohepatitis: association with obesity and insulin resistance, and influence of weight loss,” Diabetes and Metabolism, vol. 26, no. 2, pp. 98–106, 2000. View at Google Scholar
  105. C. P. Day and O. F. W. James, “Steatohepatitis: a tale of two 'hits'?” Gastroenterology, vol. 114, no. 4 I, pp. 842–845, 1998. View at Publisher · View at Google Scholar
  106. C. P. Day, “Non-alcoholic steatohepatitis (NASH): where are we now and where are we going?” Gut, vol. 50, no. 5, pp. 585–588, 2002. View at Google Scholar
  107. G. C. Farrell and C. Z. Larter, “Nonalcoholic fatty liver disease: from steatosis to cirrhosis,” Hepatology, vol. 43, no. 2, pp. 99–112, 2006. View at Publisher · View at Google Scholar · View at PubMed
  108. P. Mofrad, M. J. Contos, M. Haque et al., “Clinical and histologic spectrum of nonalcoholic fatty liver disease associated with normal ALT values,” Hepatology, vol. 37, no. 6, pp. 1286–1292, 2003. View at Publisher · View at Google Scholar · View at PubMed
  109. E. E. Powell, W. G. Cooksley, R. Hanson, J. Searle, J. W. Halliday, and L. W. Powell, “The natural history of non-alcoholic steatohepatitis: a followup study of forty-two patients for up to 21 years,” Hepatology, vol. 11, pp. 74–80, 1990. View at Google Scholar
  110. S. G. Sheth, F. D. Gordon, and S. Chopra, “Nonalcoholic steatohepatitis,” Annals of Internal Medicine, vol. 126, no. 2, pp. 137–145, 1997. View at Google Scholar
  111. A. Sonsuz, M. Basaranoglu, and G. Ozbay, “Relationship between aminotransferase levels and histopathological findings in patients with nonalcoholic steatohepatitis,” The American Journal of Gastroenterology, vol. 95, no. 5, pp. 1370–1371, 2000. View at Google Scholar
  112. R. G. Lee, “Nonalcoholic steatohepatitis: a study of 49 patients,” Human Pathology, vol. 20, no. 6, pp. 594–598, 1989. View at Google Scholar
  113. A. M. Diehl, Z. Goodman, and K. G. Ishak, “Alcohollike liver disease in nonalcoholics. A clinical and histologic comparison with alcohol-induced liver injury,” Gastroenterology, vol. 95, no. 4, pp. 1056–1062, 1988. View at Google Scholar
  114. S. J. Cotler, K. Kanji, A. Keshavarzian, D. M. Jensen, and S. Jakate, “Prevalence and significance of autoantibodies in patients with non-alcoholic steatohepatitis,” Journal of Clinical Gastroenterology, vol. 38, no. 9, pp. 801–804, 2004. View at Publisher · View at Google Scholar
  115. K. Tajiri, H. Takenawa, K. Yamaoka, M. Yamane, F. Marumo, and C. Sato, “Nonalcoholic steatohepatitis masquerading as autoimmune hepatitis,” Journal of Clinical Gastroenterology, vol. 25, no. 3, pp. 538–540, 1997. View at Publisher · View at Google Scholar
  116. K. J. Mortele and P. R. Ros, “Imaging of diffuse liver disease,” Seminars in Liver Disease, vol. 21, no. 2, pp. 195–212, 2001. View at Publisher · View at Google Scholar · View at PubMed
  117. C. C. Mottin, M. Moretto, A. V. Padoin et al., “The role of ultrasound in the diagnosis of hepatic steatosis in morbidly obese patients,” Obesity Surgery, vol. 14, no. 5, pp. 635–637, 2004. View at Publisher · View at Google Scholar · View at PubMed
  118. H. Ataseven, M. H. Yildirim, M. Yalniz, H. Bahcecioglu, S. Celebi, and I. H. Ozercan, “The vaue of ultrasonography and computerized tomograph in estimating the histopatological severity of nonalcoholic steatohepatitis,” Gastroenterology in Belgium, vol. 68, pp. 221–225, 2005. View at Google Scholar
  119. S. Saadeh, Z. M. Younossi, E. M. Remer et al., “The utility of radiological imaging in nonalcoholic fatty liver disease,” Gastroenterology, vol. 123, no. 3, pp. 745–750, 2002. View at Publisher · View at Google Scholar
  120. P. Angulo, J. C. Keach, K. P. Batts, and K. D. Lindor, “Independent predictors of liver fibrosis in patients with nonalcoholic steatohepatitis,” Hepatology, vol. 30, no. 6, pp. 1356–1362, 1999. View at Google Scholar
  121. D. Joy, V. R. Thava, and B. B. Scott, “Diagnosis of fatty liver disease: is biopsy necessary?” European Journal of Gastroenterology and Hepatology, vol. 15, no. 5, pp. 539–543, 2003. View at Publisher · View at Google Scholar
  122. E. S. Siegelman and M. A. Rosen, “Imaging of hepatic steatosis,” Seminars in Liver Disease, vol. 21, no. 1, pp. 71–80, 2001. View at Google Scholar
  123. E. M. Brunt, “Nonalcoholic steatohepatitis: definition and pathology,” Seminars in Liver Disease, vol. 21, no. 1, pp. 3–16, 2001. View at Google Scholar
  124. B. A. Neuschwander-Tetri, “Nonalcoholic steatohepatitis: an evolving diagnosis,” Canadian Journal of Gastroenterology, vol. 14, no. 4, pp. 321–326, 2000. View at Google Scholar
  125. M. Shimada, E. Hashimoto, M. Taniai, K. Hasegawa, H. Okuda, and Y. Nakanuma, “Hepatocellular carcinoma in patients with non-alcoholic steatohepatitis,” Pathology International, vol. 51, pp. 127–131, 2001. View at Google Scholar
  126. M. Moretto, C. Kupski, C. C. Mottin et al., “Hepatic steatosis in patients undergoing bariatric surgery and its relationship to body mass index and co-morbidities,” Obesity Surgery, vol. 13, no. 4, pp. 622–624, 2003. View at Publisher · View at Google Scholar
  127. S. Shalhub, A. Parsee, S. F. Gallagher et al., “The importance of routine liver biopsy in diagnosing nonalcoholic steatohepatitis in bariatric patients,” Obesity Surgery, vol. 14, no. 1, pp. 54–59, 2004. View at Publisher · View at Google Scholar · View at PubMed
  128. M. S. Campbell and K. R. Reddy, “Review article: the evolving role of liver biopsy,” Alimentary Pharmacology and Therapeutics, vol. 20, no. 3, pp. 249–259, 2004. View at Publisher · View at Google Scholar · View at PubMed
  129. S. G. Hubscher, “Role of liver biopsy in the assessment of non-alcoholic fatty liver disease,” European Journal of Gastroenterology and Hepatology, vol. 16, no. 11, pp. 1107–1115, 2004. View at Publisher · View at Google Scholar
  130. A. A. Bravo, S. G. Sheth, and S. Chopra, “Liver biopsy,” New England Journal of Medicine, vol. 344, no. 7, pp. 495–500, 2001. View at Publisher · View at Google Scholar
  131. R. B. Merriman, L. D. Ferrel, M. G. Patti, J. W. Ostroff, K. Bagetelos, and B. E. Aouizerat, “Histologic correlation of paired right lobe and left lobe liver biopsies in morbidly obese individuals with suspected nonalcoholic fatty liver disease,” Hepatology, vol. 38, supplement 1, p. 230A, 2003. View at Google Scholar
  132. A. Grant and J. Neuberger, “Guidelines on the use of liver biopsy in clinical practice,” Gut, vol. 45, supplement 4, pp. 1–11, 1999. View at Google Scholar
  133. M. Guido and M. Rugge, “Liver biopsy sampling in chronic viral hepatitis,” Seminars in Liver Disease, vol. 24, no. 1, pp. 89–97, 2004. View at Publisher · View at Google Scholar · View at PubMed
  134. S. Geller and M. Pitman, “Morphological diagnostic procedures (liver biopsy),” in Pathology of the Liver, A. D. Burt, B. C. Portmann, and R. N. M. McSween, Eds., pp. 943–960, Churchill Livingston, London, UK, 2002:. View at Google Scholar
  135. S. Seki, H. Sakaguchi, H. Kadoya et al., “Laparoscopic wedge biopsy of the liver with use of an ultrasonically activated scalpel,” Digestive Endoscopy, vol. 13, no. 1, pp. 17–20, 2001. View at Publisher · View at Google Scholar
  136. I. T. Gilmore, A. Burroughs, I. M. Murray-Lyon, R. Williams, D. Jenkins, and A. Hopkins, “Indications, methods, and outcomes of percutaneous liver biopsy in England and Wales: an audit by the British Society of Gastroenterology and the Royal College of Physicians of London,” Gut, vol. 36, no. 3, pp. 437–441, 1995. View at Google Scholar
  137. F. Piccinino, E. Sagnelli, and G. Pasquale, “Complications following percutaneous liver biopsy,” Journal of Hepatology, vol. 2, no. 2, pp. 165–173, 1986. View at Google Scholar
  138. G. Colloredo, M. Guido, A. Sonzogni, and G. Leandro, “Impact of liver biopsy size on histological evaluation of chronic viral hepatitis: the smaller the sample, the milder the disease,” Journal of Hepatology, vol. 39, no. 2, pp. 239–244, 2003. View at Publisher · View at Google Scholar
  139. B. Maharaj, R. J. Maharaj, and W. P. Leary, “Sampling variability and its influence on the diagnostic yield of percutaneous needle biopsy of the liver,” Lancet, vol. 1, no. 8480, pp. 523–525, 1986. View at Google Scholar
  140. S. A. Harrison, S. Torgerson, and P. H. Hayashi, “The natural history of nonalcoholic fatty liver disease: a clinical histopathological study,” American Journal of Gastroenterology, vol. 98, no. 9, pp. 2042–2047, 2003. View at Publisher · View at Google Scholar · View at PubMed
  141. E. Fassio, E. Alvarez, N. Domínguez, G. Landeira, and C. Longo, “Natural history of nonalcoholic steatohepatitis: a longitudinal study of repeat liver biopsies,” Hepatology, vol. 40, no. 4, pp. 820–826, 2004. View at Publisher · View at Google Scholar · View at PubMed
  142. V. Ratziu, P. Giral, F. Charlotte, E. Bruckert, V. Thibault, and I. Theodorou, “Liver fibrosis in over weight patients,” Gastroenterology, vol. 118, pp. 1117–1123, 2000. View at Google Scholar
  143. A. Propst, T. Propst, G. Zangerl, D. Ofner, G. Judmaier, and W. Vogel, “Prognosis and life expectancy in chronic liver disease,” Digestive Diseases and Sciences, vol. 40, no. 8, pp. 1805–1815, 1995. View at Publisher · View at Google Scholar
  144. E. Bugianesi, N. Leone, E. Vanni et al., “Expanding the natural history of nonalcoholic steatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma,” Gastroenterology, vol. 123, no. 1, pp. 134–140, 2002. View at Publisher · View at Google Scholar
  145. J. M. Clark and A. M. Diehl, “Nonalcoholic fatty liver disease. An underrecognized cause of cryptogenic cirrhosis,” Journal of the American Medical Association, vol. 289, no. 22, pp. 300–304, 2003. View at Publisher · View at Google Scholar · View at PubMed
  146. A. J. McCullough, “The clinical features, diagnosis and natural history of nonalcoholic fatty liver disease,” Clinics in Liver Disease, vol. 8, no. 3, pp. 521–533, 2004. View at Publisher · View at Google Scholar · View at PubMed
  147. J. B. Dixon, P. S. Bhathal, N. R. Hughes, and P. E. O'Brien, “Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss,” Hepatology, vol. 39, no. 6, pp. 1647–1654, 2004. View at Publisher · View at Google Scholar · View at PubMed
  148. S. Eriksson, K. F. Eriksson, and L. Bondesson, “Nonalcoholic steatohepatitis in obesity: a reversible condition,” Acta Medica Scandinavica, vol. 220, no. 1, pp. 83–88, 1986. View at Google Scholar
  149. T. Andersen, C. Gluud, M. B. Franzmann, and P. Christoffersen, “Hepatic effects of dietary weight loss in morbidly obese subjects,” Journal of Hepatology, vol. 12, no. 2, pp. 224–229, 1991. View at Google Scholar
  150. F. H. Luyckx, A. J. Scheen, C. Desaive, W. Dewe, J. E. Gielen, and P. J. Lefebvre, “Effects of gastroplasty on body weight and related biological abnormalities in morbid obesity,” Diabetes and Metabolism, vol. 24, no. 4, pp. 355–361, 1998. View at Google Scholar
  151. E. J. Drenick, F. Simmons, and J. F. Murphy, “Effect on hepatic morphology of treatment of obesity by fasting, reducing diets and small-bowel bypass,” New England Journal of Medicine, vol. 282, no. 15, pp. 829–834, 1970. View at Google Scholar
  152. H. Tilg and A. M. Diehl, “Cytokines in alcoholic and nonalcoholic steatohepatitis,” New England Journal of Medicine, vol. 343, no. 20, pp. 1467–1476, 2000. View at Publisher · View at Google Scholar · View at PubMed
  153. J. M. Hui, A. Hodge, G. C. Farrell, J. G. Kench, A. Kriketos, and J. George, “Beyond insulin resistance in NASH: TNF-α or adiponectin?” Hepatology, vol. 40, no. 1, pp. 46–54, 2004. View at Publisher · View at Google Scholar · View at PubMed
  154. S. Choi and A. M. Diehl, “Role of inflammation in nonalcoholic steatohepatitis,” Current Opinion in Gastroenterology, vol. 21, no. 6, pp. 702–707, 2005. View at Publisher · View at Google Scholar
  155. G. Atzmon, X. M. Yang, R. Muzumdar, X. H. Ma, I. Gabriely, and N. Barzilai, “Differential gene expression between visceral and subcutaneous fat depots,” Hormone and Metabolic Research, vol. 34, no. 11-12, pp. 622–628, 2002. View at Publisher · View at Google Scholar · View at PubMed
  156. C. J. Lyon, R. E. Law, and W. A. Hsueh, “Minireview: adiposity, inflammation, and atherogenesis,” Endocrinology, vol. 144, no. 6, pp. 2195–2200, 2003. View at Publisher · View at Google Scholar
  157. P. Ziccardi, F. Nappo, G. Giugliano et al., “Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year,” Circulation, vol. 105, no. 7, pp. 804–809, 2002. View at Publisher · View at Google Scholar
  158. M. Lehrke, M. P. Reilly, S. C. Millington, N. Iqbal, D. J. Rader, and M. A. Lazar, “An inflammatory cascade leading to hyperresistinemia in humans,” PLoS Medicine, vol. 1, pp. 161–168, 2004. View at Publisher · View at Google Scholar · View at PubMed
  159. S. Chitturi, G. Farrell, L. Frost et al., “Serum leptin in NASH correlates with hepatic steatosis but not fibrosis: a manifestation of lipotoxicity?” Hepatology, vol. 36, no. 2, pp. 403–409, 2002. View at Publisher · View at Google Scholar · View at PubMed
  160. N. Chalasani, D. W. Crabb, O. W. Cummings et al., “Does leptin play a role in the pathogenesis of human nonalcoholic steatohepatitis?” American Journal of Gastroenterology, vol. 98, no. 12, pp. 2771–2776, 2003. View at Publisher · View at Google Scholar · View at PubMed
  161. P. Angulo, L. M. Alba, L. M. Petrovic, L. A. Adams, K. D. Lindor, and M. D. Jensen, “Leptin, insulin resistance, and liver fibrosis in human nonalcoholic fatty liver disease,” Journal of Hepatology, vol. 41, no. 6, pp. 943–949, 2004. View at Publisher · View at Google Scholar · View at PubMed
  162. G. Musso, R. Gambino, M. Durazzo et al., “Adipokines in NASH: postprandial lipid metabolism as a link between adiponectin and liver disease,” Hepatology, vol. 42, no. 5, pp. 1175–1183, 2005. View at Publisher · View at Google Scholar · View at PubMed
  163. M. J. Czaja, “Liver injury in the setting of steatosis: crosstalk between adipokine and cytokine,” Hepatology, vol. 40, no. 1, pp. 19–22, 2004. View at Publisher · View at Google Scholar · View at PubMed
  164. J. Janke, S. Angeli, K. Gorzelniak, F. C. Luft, and A. M. Sharma, “Resistin gene expression in human adipocytes is not related to insulin resistance,” Obesity Research, vol. 10, no. 1, pp. 1–5, 2002. View at Google Scholar
  165. C. Pagano, G. Soardo, C. Pilon et al., “Increased serum resistin in nonalcoholic fatty liver disease is related to liver disease severity and not to insulin resistance,” Journal of Clinical Endocrinology and Metabolism, vol. 91, no. 3, pp. 1081–1086, 2006. View at Publisher · View at Google Scholar · View at PubMed
  166. D. G. Tiniakos, M. B. Vos, and E. M. Brunt, “Nonalcoholic fatty liver disease,” Annual Review of Pathology, vol. 5, pp. 145–171, 2010. View at Google Scholar
  167. D. Van Der Poorten, K. L. Milner, J. Hui et al., “Visceral fat: a key mediator of steatohepatitis in metabolic liver disease,” Hepatology, vol. 48, no. 2, pp. 449–457, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  168. R. Guerrero, G. L. Vega, S. M. Grundy, and J. D. Browning, “Ethnic differences in hepatic steatosis: an insulin resistance paradox?” Hepatology, vol. 49, no. 3, pp. 791–801, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  169. S. R. Weston, W. Leyden, R. Murphy, N. M. Bass, and B. P. Bell, “Racial and ethnic distribution ofnonalcoholic fatty liver in persons with newly diagnosed chronic liver disease,” Hepatology, vol. 41, pp. 372–379, 2005. View at Google Scholar