Does vitamin D improve liver enzymes, oxidative stress, and inflammatory biomarkers in adults with non-alcoholic fatty liver disease? A randomized clinical trial

Endocrine

Volumn 47, Issue 1, 2014, Pages 70-80

  Sharifi, Nasrin ^a   Amani, Reza ^a   Hajiani, Eskandar ^a   Cheraghian, Bahman ^a  

^a AHVAZ JUNDISHAPUR UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Inflammation; Non alcoholic fatty liver disease; Oxidative stress; Vitamin D

Indexed keywords

ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; BIOLOGICAL MARKER; C REACTIVE PROTEIN; CALCIFEDIOL; COLECALCIFEROL; D VITIN; INFLAMMATORY BIOMARKER; LIVER ENZYME; MALONALDEHYDE; PLACEBO; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VITAMIN D;

ADJUVANT THERAPY; ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALKALINE PHOSPHATASE BLOOD LEVEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; FATTY LIVER; FEMALE; HUMAN; INSULIN RESISTANCE; LIPID PEROXIDATION; MAJOR CLINICAL STUDY; MALE; METABOLIC PARAMETERS; NONALCOHOLIC FATTY LIVER; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PARALLEL DESIGN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL; TOTAL ANTIOXIDANT CAPACITY; TREATMENT DURATION; VITAMIN BLOOD LEVEL; VITAMIN SUPPLEMENTATION; DRUG EFFECTS; ENZYMOLOGY; INFLAMMATION; LIVER; METABOLISM; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE;

ADULT; BIOLOGICAL MARKERS; C-REACTIVE PROTEIN; FEMALE; HUMANS; INFLAMMATION; INSULIN RESISTANCE; LIVER; MALE; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATIVE STRESS; VITAMIN D;

EID: 84906940023     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-014-0336-5     Document Type: Article

References (59)

1. E.A. Yetley, Assessing the vitamin D status of the US population. Am. J. Clin. Nutr. 88(2), 558S-564S (2008)
2. M.F. Holick, Vitamin D deficiency. N. Engl. J. Med. 357(3), 266-281 (2007)
3. J.S. Adams, M. Hewison, Update in vitamin D. J. Clin. Endocrinol. Metab. 95(2), 471-478 (2010)
4. G. Musso, Non-alcoholic fatty liver, adipose tissue, and the bone: a new triumvirate on the block. Endocrine 42, 237-239 (2012)
5. E. Hyppönen, B.J. Boucher, D.J. Berry, C. Power, 25-hydroxyvitamin D, IGF-1, and metabolic syndrome at 45 years of age. Diabetes 57(2), 298-305 (2008)
6. J.P. Reis, D. von Mühlen, D. Kritz-Silverstein, D.L. Wingard, E. Barrett-Connor, Vitamin D, parathyroid hormone levels, and the prevalence of metabolic syndrome in community-dwelling older adults. Diabetes Care 30(6), 1549-1555 (2007)
7. L.-H. Li, X.-Y. Yin, C.-Y. Yao, X.-C. Zhu, X.-H. Wu, Serum 25-hydroxyvitamin D, parathyroid hormone, and their association with metabolic syndrome in Chinese. Endocrine 44(2), 465-472 (2013)
8. N.C. Bozkurt, E. Cakal, M. Sahin, E.C. Ozkaya, H. Firat, T. Delibasi, The relation of serum 25-hydroxyvitamin-D levels with severity of obstructive sleep apnea and glucose metabolism abnormalities. Endocrine 41(3), 518-525 (2012)
9. G. Targher, L. Bertolini, L. Scala, M. Cigolini, L. Zenari, G. Falezza, G. Arcaro, Associations between serum 25-hydroxyvitamin D3 concentrations and liver histology in patients with non-alcoholic fatty liver disease. Nutr. Metab. Cardiovasc. Dis 17(7), 517-524 (2007)
10. J.M. Clark, F.L. Brancati, A.M. Diehl, Nonalcoholic fatty liver disease. Gastroenterology 122(6), 1649-1657 (2002)
11. I. Barchetta, F. Angelico, M.D. Ben, M.G. Baroni, P. Pozzilli, S. Morini, M.G. Cavallo, Strong association between non alcoholic fatty liver disease (NAFLD) and low 25 (OH) vitamin D levels in an adult population with normal serum liver enzymes. BMC Med. 9(1), 85 (2011)
12. T. Nakano, Y.F. Cheng, C.Y. Lai, L.W. Hsu, Y.C. Chang, J.Y. Deng, Y.Z. Huang, H. Honda, K.D. Chen, C.C. Wang, Impact of artificial sunlight therapy on the progress of non-alcoholic fatty liver disease in rats. J. Hepatol. 55(2), 415-425 (2011)
13. E. Rhee, M. Kim, S. Park, C. Park, K. Baek, W. Lee, M. Kang, S. Park, S. Kim, K. Oh, High serum vitamin D levels reduce the risk for nonalcoholic fatty liver disease in healthy men independent of metabolic syndrome. Endocr. J. 60(6), 743-752 (2013)
14. G. Targher, C. Byrne, Lower 25-hydroxyvitamin D3 levels and increased risk of liver diseases: is there a causal link? Endocrine (2014). doi:10.1007/s12020-014-0220-3
15. C.L. Roth, C.T. Elfers, D.P. Figlewicz, S.J. Melhorn, G.J. Morton, A. Hoofnagle, M.M. Yeh, J.E. Nelson, K.V. Kowdley, Vitamin D deficiency in obese rats exacerbates nonalcoholic fatty liver disease and increases hepatic resistin and toll-like receptor activation. Hepatology 55(4), 1103-1111 (2012)
16. D. Prati, E. Taioli, A. Zanella, E. Della Torre, S. Butelli, E. Del Vecchio, L. Vianello, F. Zanuso, F. Mozzi, S. Milani, Updated definitions of healthy ranges for serum alanine aminotransferase levels. Ann. Intern. Med. 137(1), 1-10 (2002)
17. S. Abu-Mouch, Z. Fireman, J. Jarchovsky, A.R. Zeina, N. Assy, Vitamin D supplementation improves sustained virologic response in chronic hepatitis C (genotype 1)-naïve patients. World J. Gastroenterol. 17(47), 5184-5190 (2011)
18. C.L. Craig, A.L. Marshall, M. Sjöström, A.E. Bauman, M.L. Booth, B.E. Ainsworth, M. Pratt, U. Ekelund, A. Yngve, J.F. Sallis, International physical activity questionnaire: 12-country reliability and validity. Med. Sci. Sports Exerc. 85(3), 1381-1395 (2003)
19. N.A. Botsoglou, D.J. Fletouris, G.E. Papageorgiou, V.N. Vassilopoulos, A.J. Mantis, A.G. Trakatellis, Rapid, sensitive, and specific thiobarbituric acid method for measuring lipid peroxidation in animal tissue, food, and feedstuff samples. J. Agric. Food Chem. 42(9), 1931-1937 (1994)
20. A. Khosrowbeygi, N. Zarghami, Y. Deldar, Correlation between sperm quality parameters and seminal plasma antioxidants status. Iran. J. Reprod. Med. 2(2), 58-64 (2012)
21. J. Jou, S.S. Choi, A.M. Diehl, Mechanisms of disease progression in nonalcoholic fatty liver disease. Semin. Liver Dis. 28(04), 370-379 (2008)
22. J.W. Haukeland, J.K. Damås, Z. Konopski, E.M. Løberg, T. Haaland, I. Goverud, P.A. Torjesen, K. Birkeland, K. Bjøro, P. Aukrust, Systemic inflammation in nonalcoholic fatty liver disease is characterized by elevated levels of CCL2. J. Hepatol. 44(6), 1167-1174 (2006)
23. G. Targher, Relationship between high-sensitivity C-reactive protein levels and liver histology in subjects with non-alcoholic fatty liver disease. J. Hepatol. 45(6), 879-881 (2006)
24. G. Targher, G. Arcaro, Non-alcoholic fatty liver disease and increased risk of cardiovascular disease. Atherosclerosis 191(2), 235-240 (2007)
25. M.T. Cantorna, Y. Zhu, M. Froicu, A. Wittke, Vitamin D status, 1, 25-dihydroxyvitamin D3, and the immune system. Am. J. Clin. Nutr. 80(6), 1717S-1720S (2004)
26. S. Zúñiga, D. Firrincieli, C. Housset, N. Chignard, Vitamin D and the vitamin D receptor in liver pathophysiology. Clin. Res. Hepatol. Gastroenterol. 35, 295-302 (2011)
27. A. Zittermann, S. Frisch, H.K. Berthold, C. Götting, J. Kuhn, K. Kleesiek, P. Stehle, H. Koertke, R. Koerfer, Vitamin D supplementation enhances the beneficial effects of weight loss on cardiovascular disease risk markers. Am. J. Clin. Nutr. 89(5), 1321-1327 (2009)
28. S.S. Schleithoff, A. Zittermann, G. Tenderich, H.K. Berthold, P. Stehle, R. Koerfer, Vitamin D supplementation improves cytokine profiles in patients with congestive heart failure: a double-blind, randomized, placebo-controlled trial. Am. J. Clin. Nutr. 83(4), 754-759 (2006)
29. J. Beilfuss, V. Berg, M. Sneve, R. Jorde, E. Kamycheva, Effects of a 1-year supplementation with cholecalciferol on interleukin-6, tumor necrosis factor-alpha and insulin resistance in overweight and obese subjects. Cytokine 60(3), 870-874 (2012)
30. Y. Karim, C. Turner, N. Dalton, R. Roplekar, A. Sankaralingam, M. Ewang, I. Fogelman, G. Hampson, The relationship between pro-resorptive inflammatory cytokines and the effect of high dose vitamin D supplementation on their circulating concentrations. Int. Immunopharmacol. 17(3), 693-697 (2013)
31. S. Shab-Bidar, T.R. Neyestani, A. Djazayery, M.R. Eshraghian, A. Houshiarrad, A. Kalayi, N. Shariatzadeh, N. Khalaji, Improvement of vitamin D status resulted in amelioration of biomarkers of systemic inflammation in the subjects with type 2 diabetes. Diabetes Metab. Res. Rev. 28(5), 424-430 (2012)
32. M.J. Czaja, F.R. Weiner, K.C. Flanders, M.-A. Giambrone, R. Wind, L. Biempica, M.A. Zern, In vitro and in vivo association of transforming growth factor-beta 1 with hepatic fibrosis. J. Cell Biol. 108(6), 2477-2482 (1989)
33. F.H. Epstein, G.C. Blobe, W.P. Schiemann, H.F. Lodish, Role of transforming growth factor b in human disease. N. Engl. J. Med. 342(18), 1350-1358 (2000)
34. T. Hasegawa, M. Yoneda, K. Nakamura, I. Makino, A. Terano, Plasma transforming growth factor-β1 level and efficacy of α-tocopherol in patients with non-alcoholic steatohepatitis: a pilot study. Aliment Pharmacol. Ther. 15(10), 1667-1672 (2001)
35. S. Isik, U. Ozuguz, Y. Ates Tutuncu, G. Erden, D. Berker, K. Acar, Y. Aydin, G. Akbaba, N. Helvaci, S. Guler, Serum transforming growth factor-beta levels in patients with vitamin D deficiency. Eur. J. Intern. Med. 23(1), 93-97 (2012)
36. A.A. Mahmoud, A.S. Bakir, S.S. Shabana, Serum TGF-β, Serum MMP-1, and HOMA-IR as non-invasive predictors of fibrosis in Egyptian patients with NAFLD. Saudi J. Gastroenterol. 18(5), 327 (2012)
37. L. Malaguarnera, R. Madeddu, E. Palio, N. Arena, M. Malaguarnera, Heme oxygenase-1 levels and oxidative stress-related parameters in non-alcoholic fatty liver disease patients. J. Hepatol. 42(4), 585-591 (2005)
38. H. Wiseman, Vitamin D is a membrane antioxidant Ability to inhibit iron-dependent lipid peroxidation in liposomes compared to cholesterol, ergosterol and tamoxifen and relevance to anticancer action. FEBS Lett. 326(1), 285-288 (1993)
39. O. Tarcin, D.G. Yavuz, B. Ozben, A. Telli, A.V. Ogunc, M. Yuksel, A. Toprak, D. Yazici, S. Sancak, O. Deyneli, Effect of vitamin D deficiency and replacement on endothelial function in asymptomatic subjects. J. Clin. Endocrinol. Metab. 94(10), 4023-4030 (2009)
40. M.C. Banakar, S.K. Paramasivan, M.B. Chattopadhyay, S. Datta, P. Chakraborty, M. Chatterjee, K. Kannan, E. Thyagarajan, 1,25-Dihydroxyvitamin D3 prevents DNA damage and restores antioxidant enzymes in rat hepatocarcinogenesis induced by diethylnitrosamine and promoted by phenobarbital. World J. Gasteroenterol. 10, 1268-1275 (2004)
41. A.G. Pittas, S.S. Harris, P.C. Stark, B. Dawson-Hughes, The effects of calcium and vitamin D supplementation on blood glucose and markers of inflammation in nondiabetic adults. Diabetes Care 30(4), 980-986 (2007)
42. P.R. von Hurst, W. Stonehouse, J. Coad, Vitamin D supplementation reduces insulin resistance in South Asian women living in New Zealand who are insulin resistant and vitamin D deficient: a randomised, placebo-controlled trial. Br. J. Nutr. 103(4), 549 (2010)
43. E. Kamycheva, V. Berg, R. Jorde, Insulin-like growth factor I, growth hormone, and insulin sensitivity: the effects of a one-year cholecalciferol supplementation in middle-aged overweight and obese subjects. Endocrine 43(2), 412-418 (2013)
44. H.R. Ardabili, B.P. Gargari, L. Farzadi, Vitamin D supplementation has no effect on insulin resistance assessment in women with polycystic ovary syndrome and vitamin D deficiency. Nutr. Res. 32(3), 195-201 (2012)
45. I.H. de Boer, L.F. Tinker, S. Connelly, J.D. Curb, B.V. Howard, B. Kestenbaum, J.C. Larson, J.E. Manson, K.L. Margolis, D.S. Siscovick, Calcium plus vitamin D supplementation and the risk of incident diabetes in the Women's Health Initiative. Diabetes Care 31(4), 701-707 (2008)
46. R. Jorde, Y. Figenschau, Supplementation with cholecalciferol does not improve glycaemic control in diabetic subjects with normal serum 25-hydroxyvitamin D levels. Eur. J. Nutr. 48(6), 349-354 (2009)
47. A.G. Pittas, B. Dawson-Hughes, Vitamin D and diabetes. J. Steroid Biochem. Mol. Biol. 121(1), 425-429 (2010)
48. A.G. Pittas, J. Lau, F.B. Hu, B. Dawson-Hughes, The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 92(6), 2017-2029 (2007)
49. R.A. DeFronzo, J.D. Tobin, R. Andres, Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am. J. Physiol. Endocrinol. Metab. 237(3), E214 (1979)
50. S.H. Ipekci, M. Basaranoglu, A. Sonsuz, The fluctuation of serum levels of aminotransferase in patients with nonalcoholic steatohepatitis. J. Clin. Gastroenterol. 36(4), 371 (2003)
51. S. Liangpunsakul, N. Chalasani, Serum vitamin D concentrations and unexplained elevation in ALT among US adults. Dig. Dis. Sci. 56(7), 2124-2129 (2011)
52. T. Skaaby, L. Husemoen, A. Borglykke, T. Jørgensen, B. Thuesen, C. Pisinger, L. Schmidt, A. Linneberg, Vitamin D status, liver enzymes, and incident liver disease and mortality: a general population study. Endocrine (2013). doi:10.1007/s12020-013-0107-8
53. H.A. Saleh, A.H. Abu-Rashed, Liver biopsy remains the gold standard for evaluation of chronic hepatitis and fibrosis. J. Gastrointest. Liver. Dis. 16(4), 425 (2007)
54. J.F. Cobbold, D. Patel, S.D. Taylor-Robinson, Assessment of inflammation and fibrosis in non-alcoholic fatty liver disease by imaging-based techniques. J. Gastroenterol. Hepatol. 27(8), 1281-1292 (2012)
55. G. Ligabue, G. Besutti, R. Scaglioni, C. Stentarelli, G. Guaraldi, MR quantitative biomarkers of non-alcoholic fatty liver disease: technical evolutions and future trends. Quant. Imaging Med. Surg. 3(4), 192 (2013)
56. M. Manco, P. Ciampalini, V. Nobili, Low levels of 25-hydroxyvitamin D3 in children with biopsy-proven nonalcoholic fatty liver disease. Hepatology 51(6), 2229 (2010)
57. M. Eliades, E. Spyrou, N. Agrawal, M. Lazo, F. Brancati, J. Potter, A. Koteish, J. Clark, E. Guallar, R. Hernaez, Meta-analysis: vitamin D and non-alcoholic fatty liver disease. Aliment Pharmacol. Ther. 38(3), 246-254 (2013)
58. A. Geier, Shedding new light on vitamin D and fatty liver disease. J. Hepatol. 55(2), 273-275 (2011)
59. G. Targher, E. Scorletti, A. Mantovani, C.D. Byrne, Nonalcoholic fatty liver disease and reduced serum vitamin D3 levels. Metab. Syndr. Relat. Disord. 11 (4), 217-228 (2013)