Relationship between hemoglobin levels and risk for suspected non-alcoholic fatty liver in taiwanese adults

Chinese Journal of Physiology

Volumn 57, Issue 5, 2014, Pages 286-294

  Bai, Chyi Huey ^a   Wu, Ming Shun ^b   Owaga, Eddy ^c   Cheng, Shu Yu ^c   Pan, Wen Harn ^d   Chang, Jung Su ^c  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

Alanine transaminase; Body iron levels; Metabolic syndrome; Non alcoholic fatty liver Disease

Indexed keywords

ALANINE AMINOTRANSFERASE; FERRITIN; HEMOGLOBIN; IRON;

ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANTHROPOMETRY; ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FERRITIN BLOOD LEVEL; HEALTH SURVEY; HEMOGLOBIN DETERMINATION; HUMAN; HYPERLIPIDEMIA; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; NONALCOHOLIC FATTY LIVER; PHLEBOTOMY; PREVALENCE; RISK FACTOR; TAIWANESE; AGE DISTRIBUTION; AGED; BLOOD; HYPERLIPIDEMIAS; IRON OVERLOAD; METABOLISM; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; ODDS RATIO; SENSITIVITY AND SPECIFICITY; SEX RATIO; TAIWAN;

ADULT; AGE DISTRIBUTION; AGED; ALANINE TRANSAMINASE; FEMALE; FERRITINS; HEMOGLOBINS; HUMANS; HYPERLIPIDEMIAS; IRON OVERLOAD; MALE; METABOLIC SYNDROME X; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; ODDS RATIO; PREVALENCE; RISK FACTORS; SENSITIVITY AND SPECIFICITY; SEX DISTRIBUTION; TAIWAN;

EID: 84911867975     PISSN: 03044920     EISSN: 26660059     Source Type: Journal    
DOI: 10.4077/CJP.2014.BAD280     Document Type: Article

References (51)

1. Adams, L.A., Angulo, P. and Lindor, K.D. Nonalcoholic fatty liver disease. Can. Med. Assoc. J. 172: 899-905, 2005.
2. Aigner, E., Theurl, I., Theurl, M., Lederer, D., Haufe, H., Dietze, O., Strasser, M., Datz, C. and Weiss, G. Pathways underlying iron accumulation in human nonalcoholic fatty liver disease. Am. J. Clin. Nutr. 87: 1374-1383, 2008.
3. Amarapurkar, D., Kamani, P., Patel, N., Gupte, P., Kumar, P., Agal, S., Baijal, R., Lala, S., Chaudhary, D. and Deshpande, A. Prevalence of non-alcoholic fatty liver disease: population based study. Ann. Hepatol. 6: 161-163, 2007.
4. Aragon, G. and Younossi, Z.M. When and how to evaluate mildly elevated liver enzymes in apparently healthy patients. Cleve. Clin. J. Med. 77: 195-204, 2010.
5. Chang, C.C., Chang, C.Y., Huang, J.P. and Hung, L.M. Effect of resveratrol on oxidative and inflammatory stress in liver and spleen of streptozotocin-induced type 1 diabetic rats. Chinese J. Physiol. 55: 192-201, 2012.
6. Chang, J.S., Lin, S.M., Chao, J.C., Chen, Y.C., Wang, C.M., Chou, N.H., Pan, W.H. and Bai, C.H. Serum ferritin contributes to racial or geographic disparities in metabolic syndrome in Taiwan. Public Health Nutr. 17: 1498-1506, 2014.
7. Chang, J.S., Lin, S.M., Huang, T.C., Chao, J.C., Chen, Y.C., Pan, W.H. and Bai, C.H. Serum ferritin and risk of the metabolic syndrome: a population-based study. Asia Pac. J. Clin. Nutr. 22: 400-407, 2013.
8. Chang, Y., Ryu, S., Sung, E. and Jang, Y. Higher concentrations of alanine aminotransferase within the reference interval predict nonalcoholic fatty liver disease. Clin. Chem. 53: 686-692, 2007.
9. Chen, C.H., Huang, M.H., Yang, J.C., Nien, C.K., Yang, C.C., Yeh, Y.H. and Yueh, S.K. Prevalence and etiology of elevated serum alanine aminotransferase level in an adult population in Taiwan. J. Gastroenterol. Hepatol. 22: 1482-1489, 2007.
10. Chen, C.H., Huang, M.H., Yang, J.C., Nien, C.K., Yang, C.C., Yeh, Y.H. and Yueh, S.K. Prevalence and risk factors of nonalcoholic fatty liver disease in an adult population of Taiwan: metabolic significance of nonalcoholic fatty liver disease in nonobese adults. J. Clin. Gastroenterol. 40: 745-752, 2006.
11. Chen, C.J., Wang, L.Y. and Yu, M.W. Epidemiology of hepatitis B virus infection in the Asia-Pacific region. J. Gastroenterol. Hepatol. 15 (Suppl 2): E3-E6, 2000.
12. Chen, S.M., Lin, H.Y. and Kuo, C.H. Altitude training improves glycemic control. Chinese J. Physiol. 56: 193-198, 2013.
13. Cheng, C.C., Lin, N.N., Lee, Y.F., Wu, L.Y., Hsu, H.P., Lee, W.J., Tung, K.C. and Chiu, Y.T. Effects of Shugan-Huayu powder, a traditional Chinese medicine, on hepatic fibrosis in rat model. Chinese J. Physiol. 53: 223-233, 2010.
14. Choi, J.W., Kim, S.K. and Pai, S.H. Changes in serum lipid concentrations during iron depletion and after iron supplementation. Ann. Clin. Lab. Sci. 31: 151-156, 2001.
15. Demirci, C., Gargili, A., Kandil, A., Cetinkaya, H., Uyaner, I., Boynuegri, B. and Gumustas, M.K. Inhibition of inducible nitric oxide synthase in murine visceral larva migrans: effects on lung and liver damage. Chinese J. Physiol. 49: 326-334, 2006.
16. Dongiovanni, P., Fracanzani, A.L., Fargion, S. and Valenti, L. Iron in fatty liver and in the metabolic syndrome: a promising therapeutic target. J. Hepatol. 55: 920-932, 2011.
17. Fu, C.C., Chen, M.C., Li, Y.M., Liu, T.T. and Wang, L.Y. The risk factors for ultrasound-diagnosed non-alcoholic fatty liver disease among adolescents. Ann. Acad. Med. Singapore 38: 15-21, 2009.
18. Fujita, N., Sugimoto, R., Motonishi, S., Tomosugi, N., Tanaka, H., Takeo, M., Iwasa, M., Kobayashi, Y., Hayashi, H., Kaito, M. and Takei, Y. Patients with chronic hepatitis C achieving a sustained virological response to peginterferon and ribavirin therapy recover from impaired hepcidin secretion. J. Hepatol. 49: 702-710, 2008.
19. Green, R.M. NASH-hepatic metabolism and not simply the metabolic syndrome. Hepatology 38: 14-17, 2003.
20. Hsiao, T.J., Chen, J.C. and Wang, J.D. Insulin resistance and ferritin as major determinants of nonalcoholic fatty liver disease in apparently healthy obese patients. Int. J. Obes. 28: 167-172, 2004.
21. Hsu, C.S. and Kao, J.H. Non-alcoholic fatty liver disease: an emerging liver disease in Taiwan. J. Formos. Med. Assoc. 111: 527-535, 2012.
22. James, P.E., Lang, D., Tufnell-Barret, T., Milsom, A.B. and Frenneaux, M.P. Vasorelaxation by red blood cells and impairment in diabetes: reduced nitric oxide and oxygen delivery by glycated hemoglobin. Circ. Res. 94: 976-983, 2004.
23. Kariv, R., Leshno, M., Beth-Or, A., Strul, H., Blendis, L., Kokia, E., Noff, D., Zelber-Sagie, S., Sheinberg, B., Oren, R. and Halpern, Z. Re-evaluation of serum alanine aminotransferase upper normal limit and its modulating factors in a large-scale population study. Liver Int. 26: 445-450, 2006.
24. Kowdley, K.V., Belt, P., Wilson, L.A., Yeh, M.M., Neuschwander-Tetri, B.A., Chalasani, N., Sanyal, A.J., Nelson, J.E. and Network, N.C.R. Serum ferritin is an independent predictor of histologic severity and advanced fibrosis in patients with nonalcoholic fatty liver disease. Hepatology 55: 77-85, 2012.
25. Lecube, A., Hernandez, C. and Simo, R. Glucose abnormalities in non-alcoholic fatty liver disease and chronic hepatitis C virus infection: the role of iron overload. Diabetes-Metab. Res. Rev. 25: 403-410, 2009.
26. Lee, C.J., Subeq, Y.M., Lee, R.P., Ke, C.Y., Lin, N.T. and Hsu, B.G. Beneficial effects of enalapril on chlorhexidine digluconateinduced liver peritoneal fibrosis in rats. Chinese J. Physiol. 54: 225-234, 2011.
27. Lee, J.K., Shim, J.H., Lee, H.C., Lee, S.H., Kim, K.M., Lim, Y.S., Chung, Y.H., Lee, Y.S. and Suh, D.J. Estimation of the healthy upper limits for serum alanine aminotransferase in Asian populations with normal liver histology. Hepatology 51: 1577-1583, 2010.
28. Lin, C.H., Ho, C.Y., Liu, C.S., Lin, W.Y., Li, C.I., Yang, C.W., Bau, D.T., Li, T.C. and Lin, C.C. Influence of adiponectin gene polymorphisms on adiponectin serum level and insulin resistance index in Taiwanese metabolic syndrome patients. Chinese J. Physiol. 55: 405-411, 2012.
29. Lin, H.I., Wang, D., Leu, F.J., Chen, C.F. and Chen, H.I. Ischemia and reperfusion of liver induces eNOS and iNOS expression: effects of a NO donor and NOS inhibitor. Chinese J. Physiol. 47: 121-127, 2004.
30. Lin, Y.C., Chou, S.C., Huang, P.T. and Chiou, H.Y. Risk factors and predictors of non-alcoholic fatty liver disease in Taiwan. Ann. Hepatol. 10: 125-132, 2011.
31. Liu, C.J. Prevalence and risk factors for non-alcoholic fatty liver disease in Asian people who are not obese. J. Gastroenterol. Hepatol. 27: 1555-1560, 2012.
32. Ludwig, J., Hashimoto, E., Porayko, M.K., Moyer, T.P. and Baldus, W.P. Hemosiderosis in cirrhosis: a study of 447 native livers. Gastroenterology 112: 882-888, 1997.
33. Manousou, P., Kalambokis, G., Grillo, F., Watkins, J., Xirouchakis, E., Pleguezuelo, M., Leandro, G., Arvaniti, V., Germani, G., Patch, D., Calvaruso, D., Mikhailidis, D.P., Dhillon, A.P. and Burroughs, A.K. Serum ferritin is a discriminant marker for both fibrosis and inflammation in histologically proven non-alcoholic fatty liver disease patients. Liver Int. 31: 730-739, 2011.
34. Marchesini, G., Brizi, M., Bianchi, G., Tomassetti, S., Bugianesi, E., Lenzi, M., McCullough, A.J., Natale, S., Forlani, G. and Melchionda, N. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes 50: 1844-1850, 2001.
35. Mitsuyoshi, H., Yasui, K., Harano, Y., Endo, M., Tsujim, K., Minami, M., Itoh, Y., Okanoue, T. and Yoshikawa, T. Analysis of hepatic genes involved in the metabolism of fatty acids and iron in nonalcoholic fatty liver disease. Hepatol. Res. 39: 366-373, 2009.
36. Miyake, T., Kumagi, T., Hirooka, M., Koizumi, M., Furukawa, S., Ueda, T., Tokumoto, Y., Ikeda, Y., Abe, M., Kitai, K., Hiasa, Y., Matsuura, B. and Onji, M. Metabolic markers and ALT cutoff level for diagnosing nonalcoholic fatty liver disease: a communitybased cross-sectional study. J. Gastroenterol. 47: 696-703, 2012.
37. Pan, W.H., Le, M.S., Chuang, S.Y., Lin, Y.C. and Fu, M.L. Obesity pandemic, correlated factors and guidelines to define, screen and manage obesity in Taiwan. Obes. Rev. 9 (Suppl 1): 22-31, 2008.
38. Peng, Y.M. and Elson, C.E. Effect of iron on lipid metabolism of Tetrahymena pyriformis. J. Nutr. 101: 1177-1184, 1971.
39. Ruhl, C.E. and Everhart, J.E. Determinants of the association of overweight with elevated serum alanine aminotransferase activity in the United States. Gastroenterology 124: 71-79, 2003.
40. Satchell, L. and Leake, D.S. Oxidation of low-density lipoprotein by iron at lysosomal pH: implications for atherosclerosis. Biochemistry 51: 3767-3775, 2012.
41. Schwimmer, J.B., Dunn, W., Norman, G.J., Pardee, P.E., Middleton, M.S., Kerkar, N. and Sirlin, C.B. SAFETY study: alanine aminotransferase cutoff values are set too high for reliable detection of pediatric chronic liver disease. Gastroenterology 138: 1357-1364, 2010.
42. Senates, E., Yilmaz, Y., Colak, Y., Ozturk, O., Altunoz, M.E., Kurt, R., Ozkara, S., Aksaray, S., Tuncer, I. and Ovunc, A.O. Serum levels of hepcidin in patients with biopsy-proven nonalcoholic fatty liver disease. Metab. Syndr. Relat. Disord. 9: 287-290, 2011.
43. Trak-Smayra, V., Dargere, D., Noun, R., Albuquerque, M., Yaghi, C., Gannage-Yared, M.H., Bedossa, P. and Paradis, V. Serum proteomic profiling of obese patients: correlation with liver pathology and evolution after bariatric surgery. Gut 58: 825-832, 2009.
44. Tung, T., Chiu, W., Lin, T., Shih, H. and Hsu, C. An exploration of prevalence and associated factors of nonalcoholic fatty liver disease in the taiwanese police service. Iran. J. Public Health 40: 54-62, 2011.
45. Valenti, L., Dongiovanni, P. and Fargion, S. Diagnostic and therapeutic implications of the association between ferritin level and severity of nonalcoholic fatty liver disease. World J. Gastroenterol. 18: 3782-3786, 2012.
46. Westerbacka, J., Corner, A., Tiikkainen, M., Tamminen, M., Vehkavaara, S., Hakkinen, A.M., Fredriksson, J. and Yki-Jarvinen, H. Women and men have similar amounts of liver and intra-abdominal fat, despite more subcutaneous fat in women: implications for sex differences in markers of cardiovascular risk. Diabetologia 47: 1360-1369, 2004.
47. Xu, C., Yu, C., Ma, H., Xu, L., Miao, M. and Li, Y. Prevalence and risk factors for the development of nonalcoholic fatty liver disease in a nonobese Chinese population: the Zhejiang Zhenhai Study. Am. J. Gastroenterol. 108: 1299-1304, 2013.
48. Yan, C.G., Ren, G.Y., Wang, F., Zhu, D.F. and Zhuang, Y. CD14-159 and-260 gene polymorphisms are associated with HBV-related cirrhotic injury in Chinese Han patients. Chinese J. Physiol. 51: 94-99, 2008.
49. Yilmaz, Y., Senates, E., Ayyildiz, T., Colak, Y., Tuncer, I., Ovunc, A.O., Dolar, E. and Kalayci, C. Characterization of nonalcoholic fatty liver disease unrelated to the metabolic syndrome. Eur. J. Clin. Invest. 42: 411-418, 2012.
50. Younossi, Z.M., Diehl, A.M. and Ong, J.P. Nonalcoholic fatty liver disease: an agenda for clinical research. Hepatology 35: 746-752, 2002.
51. Yu, C., Xu, C., Xu, L., Yu, J., Miao, M. and Li, Y. Serum proteomic analysis revealed diagnostic value of hemoglobin for nonalcoholic fatty liver disease. J. Hepatol. 56: 241-247, 2012.