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Published in: Hepatology International 3/2016

01-05-2016 | Original Article

Males seropositive for hepatitis B surface antigen are at risk of lower bone mineral density: the 2008–2010 Korea National Health and Nutrition Examination Surveys

Authors: Myong Ki Baeg, Seung Kew Yoon, Sun-Hye Ko, Kyung-Do Han, Hye Jin Choi, Si Hyun Bae, Jong Young Choi, Myung-Gyu Choi

Published in: Hepatology International | Issue 3/2016

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Abstract

Background

Hepatic osteodystrophy has been reported in patients with various chronic liver diseases, including liver cirrhosis. However, it has not been well investigated in patients with hepatitis B virus infection. The aim of this study was to investigate the association between hepatitis B surface antigen (HBsAg) seropositivity and bone mineral density (BMD) in a population representative of normal Koreans.

Methods

Subjects with both HBsAg and BMD levels examined during the 2008–2010 Korea National Health and Nutrition Examination Surveys were included. HBsAg-seropositive (+) subjects were compared with those who were HBsAg-seronegative (−). BMD was measured at the lumbar spine and femur by dual-energy X-ray absorptiometry. Multivariable logistic regression was performed for BMD .

Results

In total, 11,306 participants were included in this study, among which 423 (3.7 %) were HBsAg(+): 153 premenopausal female (3.4 %), 83 postmenopausal female (3.5 %), and 187 male (4.2 %). Multivariable logistic regression analysis adjusted for age and body mass index showed that HBsAg(+) male had significantly lower BMD of the femoral neck than HBsAg(−) male (0.810 ± 0.009 vs. 0.827 ± 0.002 g/cm2, p = 0.035). Further adjustment for waist circumference, smoking, drinking, exercise, income, occupation, and vitamin D levels showed that HBsAg(+) male had significantly lower BMD of the femur neck (0.810 ± 0.010 vs. 0.831 ± 0.002 g/cm2, p = 0.032) and lumbar spine (0.953 ± 0.011 vs. 0.974 ± 0.003 g/cm2, p = 0.049) than HBsAg(−) male.

Conclusions

HBsAg seropositivity was significantly associated with lower BMD in male. Future long-term prospective studies investigating bone turnover markers and hormones are needed to better understand the pathophysiology and clinical significance of chronic hepatitis B virus-related hepatic osteodystrophy.
Literature
1.
go back to reference Leslie WD, Bernstein CN, Leboff MS. AGA technical review on osteoporosis in hepatic disorders. Gastroenterology 2003;125:941–966CrossRefPubMed Leslie WD, Bernstein CN, Leboff MS. AGA technical review on osteoporosis in hepatic disorders. Gastroenterology 2003;125:941–966CrossRefPubMed
4.
go back to reference Nakchbandi IA, van der Merwe SW. Current understanding of osteoporosis associated with liver disease. Nat Rev Gastroenterol Hepatol 2009;6:660–670CrossRefPubMed Nakchbandi IA, van der Merwe SW. Current understanding of osteoporosis associated with liver disease. Nat Rev Gastroenterol Hepatol 2009;6:660–670CrossRefPubMed
5.
go back to reference Lopez-Larramona G, Lucendo AJ, Gonzalez-Castillo S, Tenias JM. Hepatic osteodystrophy: an important matter for consideration in chronic liver disease. World J Hepatol 2011;3:300–307CrossRefPubMedPubMedCentral Lopez-Larramona G, Lucendo AJ, Gonzalez-Castillo S, Tenias JM. Hepatic osteodystrophy: an important matter for consideration in chronic liver disease. World J Hepatol 2011;3:300–307CrossRefPubMedPubMedCentral
6.
go back to reference Gonzalez-Calvin JL, Gallego-Rojo F, Fernandez-Perez R, Casado-Caballero F, Ruiz-Escolano E, Olivares EG. Osteoporosis, mineral metabolism, and serum soluble tumor necrosis factor receptor p55 in viral cirrhosis. J Clin Endocrinol Metab 2004;89:4325–4330CrossRefPubMed Gonzalez-Calvin JL, Gallego-Rojo F, Fernandez-Perez R, Casado-Caballero F, Ruiz-Escolano E, Olivares EG. Osteoporosis, mineral metabolism, and serum soluble tumor necrosis factor receptor p55 in viral cirrhosis. J Clin Endocrinol Metab 2004;89:4325–4330CrossRefPubMed
7.
go back to reference Gonzalez-Calvin JL, Mundi JL, Casado-Caballero FJ, Abadia AC, Martin-Ibanez JJ. Bone mineral density and serum levels of soluble tumor necrosis factors, estradiol, and osteoprotegerin in postmenopausal women with cirrhosis after viral hepatitis. J Clin Endocrinol Metab 2009;94:4844–4850CrossRefPubMed Gonzalez-Calvin JL, Mundi JL, Casado-Caballero FJ, Abadia AC, Martin-Ibanez JJ. Bone mineral density and serum levels of soluble tumor necrosis factors, estradiol, and osteoprotegerin in postmenopausal women with cirrhosis after viral hepatitis. J Clin Endocrinol Metab 2009;94:4844–4850CrossRefPubMed
8.
go back to reference Corazza GR, Trevisani F, Di Stefano M, De Notariis S, Veneto G, Cecchetti L, et al. Early increase of bone resorption in patients with liver cirrhosis secondary to viral hepatitis. Dig Dis Sci 2000;45:1392–1399CrossRefPubMed Corazza GR, Trevisani F, Di Stefano M, De Notariis S, Veneto G, Cecchetti L, et al. Early increase of bone resorption in patients with liver cirrhosis secondary to viral hepatitis. Dig Dis Sci 2000;45:1392–1399CrossRefPubMed
9.
go back to reference Chen CC, Wang SS, Jeng FS, Lee SD. Metabolic bone disease of liver cirrhosis: is it parallel to the clinical severity of cirrhosis? J Gastroenterol Hepatol 1996;11:417–421CrossRefPubMed Chen CC, Wang SS, Jeng FS, Lee SD. Metabolic bone disease of liver cirrhosis: is it parallel to the clinical severity of cirrhosis? J Gastroenterol Hepatol 1996;11:417–421CrossRefPubMed
10.
go back to reference Gallego-Rojo FJ, Gonzalez-Calvin JL, Munoz-Torres M, Mundi JL, Fernandez-Perez R, Rodrigo-Moreno D. Bone mineral density, serum insulin-like growth factor I, and bone turnover markers in viral cirrhosis. Hepatology 1998;28:695–699CrossRefPubMed Gallego-Rojo FJ, Gonzalez-Calvin JL, Munoz-Torres M, Mundi JL, Fernandez-Perez R, Rodrigo-Moreno D. Bone mineral density, serum insulin-like growth factor I, and bone turnover markers in viral cirrhosis. Hepatology 1998;28:695–699CrossRefPubMed
11.
go back to reference Bell H, Raknerud N, Falch JA, Haug E. Inappropriately low levels of gonadotrophins in amenorrhoeic women with alcoholic and non-alcoholic cirrhosis. Eur J Endocrinol 1995;132:444–449CrossRefPubMed Bell H, Raknerud N, Falch JA, Haug E. Inappropriately low levels of gonadotrophins in amenorrhoeic women with alcoholic and non-alcoholic cirrhosis. Eur J Endocrinol 1995;132:444–449CrossRefPubMed
12.
go back to reference Gonzalez-Calvin JL, Mundi JL, Casado FJ, Olivares EG. Bone mineral density and serum levels of estradiol and osteoprotegerin in postmenopausal women with viral cirrhosis. Gastroenterology 2004;126:1225–1226; author reply 1226 Gonzalez-Calvin JL, Mundi JL, Casado FJ, Olivares EG. Bone mineral density and serum levels of estradiol and osteoprotegerin in postmenopausal women with viral cirrhosis. Gastroenterology 2004;126:1225–1226; author reply 1226
13.
go back to reference Orsini LG, Pinheiro MM, Castro CH, Silva AE, Szejnfeld VL. Bone mineral density measurements, bone markers and serum vitamin D concentrations in men with chronic non-cirrhotic untreated hepatitis C. PLoS ONE 2013;8:e81652CrossRefPubMedPubMedCentral Orsini LG, Pinheiro MM, Castro CH, Silva AE, Szejnfeld VL. Bone mineral density measurements, bone markers and serum vitamin D concentrations in men with chronic non-cirrhotic untreated hepatitis C. PLoS ONE 2013;8:e81652CrossRefPubMedPubMedCentral
14.
go back to reference Duarte MP, Farias ML, Coelho HS, Mendonça LM, Stabnov LM, do Carmo d Oliveira M, Lamy RA, Oliveira DS. Calcium-parathyroid hormone-vitamin D axis and metabolic bone disease in chronic viral liver disease. J Gastroenterol Hepatol 2001;16:1022–1027CrossRefPubMed Duarte MP, Farias ML, Coelho HS, Mendonça LM, Stabnov LM, do Carmo d Oliveira M, Lamy RA, Oliveira DS. Calcium-parathyroid hormone-vitamin D axis and metabolic bone disease in chronic viral liver disease. J Gastroenterol Hepatol 2001;16:1022–1027CrossRefPubMed
15.
go back to reference Gaudio A, Pennisi P, Muratore F, Bertino G, Ardiri A, Pulvirenti I, et al. Reduction of volumetric bone mineral density in postmenopausal women with hepatitis C virus-correlated chronic liver disease: a peripheral quantitative computed tomography (pQCT) study. Eur J Intern Med 2012;23:656–660CrossRefPubMed Gaudio A, Pennisi P, Muratore F, Bertino G, Ardiri A, Pulvirenti I, et al. Reduction of volumetric bone mineral density in postmenopausal women with hepatitis C virus-correlated chronic liver disease: a peripheral quantitative computed tomography (pQCT) study. Eur J Intern Med 2012;23:656–660CrossRefPubMed
16.
go back to reference Arase Y, Suzuki F, Suzuki Y, Akuta N, Kobayashi M, Sezaki H, et al. Virus clearance reduces bone fracture in postmenopausal women with osteoporosis and chronic liver disease caused by hepatitis C virus. J Med Virol 2010;82:390–395CrossRefPubMed Arase Y, Suzuki F, Suzuki Y, Akuta N, Kobayashi M, Sezaki H, et al. Virus clearance reduces bone fracture in postmenopausal women with osteoporosis and chronic liver disease caused by hepatitis C virus. J Med Virol 2010;82:390–395CrossRefPubMed
19.
go back to reference Yim HJ, Lok AS. Natural history of chronic hepatitis B virus infection: what we knew in 1981 and what we know in 2005. Hepatology 2006;43:S173–S181CrossRefPubMed Yim HJ, Lok AS. Natural history of chronic hepatitis B virus infection: what we knew in 1981 and what we know in 2005. Hepatology 2006;43:S173–S181CrossRefPubMed
20.
go back to reference Schiefke I, Fach A, Wiedmann M, Aretin AV, Schenker E, Borte G, et al. Reduced bone mineral density and altered bone turnover markers in patients with non-cirrhotic chronic hepatitis B or C infection. World J Gastroenterol 2005;11:1843–1847CrossRefPubMedPubMedCentral Schiefke I, Fach A, Wiedmann M, Aretin AV, Schenker E, Borte G, et al. Reduced bone mineral density and altered bone turnover markers in patients with non-cirrhotic chronic hepatitis B or C infection. World J Gastroenterol 2005;11:1843–1847CrossRefPubMedPubMedCentral
21.
go back to reference Wariaghli G, Mounach A, Achemlal L, Benbaghdadi I, Aouragh A, Bezza A, et al. Osteoporosis in chronic liver disease: a case-control study. Rheumatol Int 2010;30:893–899CrossRefPubMed Wariaghli G, Mounach A, Achemlal L, Benbaghdadi I, Aouragh A, Bezza A, et al. Osteoporosis in chronic liver disease: a case-control study. Rheumatol Int 2010;30:893–899CrossRefPubMed
22.
go back to reference Yenice N, Gumrah M, Mehtap O, Kozan A, Turkmen S. Assessment of bone metabolism and mineral density in chronic viral hepatitis. Turk J Gastroenterol 2006;17:260–266PubMed Yenice N, Gumrah M, Mehtap O, Kozan A, Turkmen S. Assessment of bone metabolism and mineral density in chronic viral hepatitis. Turk J Gastroenterol 2006;17:260–266PubMed
23.
go back to reference Lim H, Nguyen T, Choue R, Wang Y. Sociodemographic disparities in the composition of metabolic syndrome components among adults in South Korea. Diabetes Care 2012;35:2028–2035CrossRefPubMedPubMedCentral Lim H, Nguyen T, Choue R, Wang Y. Sociodemographic disparities in the composition of metabolic syndrome components among adults in South Korea. Diabetes Care 2012;35:2028–2035CrossRefPubMedPubMedCentral
24.
go back to reference Yoon JY, Park HA, Kang JH, Kim KW, Hur YI, Park JJ, et al. Prevalence of dietary supplement use in Korean children and adolescents: insights from Korea National Health and Nutrition Examination Survey 2007-2009. J Korean Med Sci 2012;27:512–517CrossRefPubMedPubMedCentral Yoon JY, Park HA, Kang JH, Kim KW, Hur YI, Park JJ, et al. Prevalence of dietary supplement use in Korean children and adolescents: insights from Korea National Health and Nutrition Examination Survey 2007-2009. J Korean Med Sci 2012;27:512–517CrossRefPubMedPubMedCentral
25.
go back to reference Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009;120:1640–1645CrossRefPubMed Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009;120:1640–1645CrossRefPubMed
26.
go back to reference Lee J, Lee S, Jang S, Ryu OH. age-related changes in the prevalence of osteoporosis according to gender and skeletal site: the Korea national health and Nutrition Examination Survey 2008–2010. Endocrinol Metab (Seoul) 2013;28:180–191CrossRef Lee J, Lee S, Jang S, Ryu OH. age-related changes in the prevalence of osteoporosis according to gender and skeletal site: the Korea national health and Nutrition Examination Survey 2008–2010. Endocrinol Metab (Seoul) 2013;28:180–191CrossRef
28.
go back to reference Raslan HM, Elhosary Y, Ezzat WM, Rasheed EA, Rasheed MA. The potential role of insulin-like growth factor 1, insulin-like growth factor binding protein 3 and bone mineral density in patients with chronic hepatitis C virus in Cairo, Egypt. Trans R Soc Trop Med Hyg 2010;104:429–432CrossRefPubMed Raslan HM, Elhosary Y, Ezzat WM, Rasheed EA, Rasheed MA. The potential role of insulin-like growth factor 1, insulin-like growth factor binding protein 3 and bone mineral density in patients with chronic hepatitis C virus in Cairo, Egypt. Trans R Soc Trop Med Hyg 2010;104:429–432CrossRefPubMed
29.
go back to reference Anastassakos C, Alexander GJ, Wolstencroft RA, Avery JA, Portmann BC, Panayi GS, et al. Interleukin-1 and interleukin-2 activity in chronic hepatitis B virus infection. Gastroenterology 1988;94:999–1005PubMed Anastassakos C, Alexander GJ, Wolstencroft RA, Avery JA, Portmann BC, Panayi GS, et al. Interleukin-1 and interleukin-2 activity in chronic hepatitis B virus infection. Gastroenterology 1988;94:999–1005PubMed
30.
go back to reference Fang JW, Shen WW, Meager A, Lau JY. Activation of the tumor necrosis factor-alpha system in the liver in chronic hepatitis B virus infection. Am J Gastroenterol 1996;91:748–753PubMed Fang JW, Shen WW, Meager A, Lau JY. Activation of the tumor necrosis factor-alpha system in the liver in chronic hepatitis B virus infection. Am J Gastroenterol 1996;91:748–753PubMed
31.
go back to reference Eghbali-Fatourechi G, Khosla S, Sanyal A, Boyle WJ, Lacey DL, Riggs BL. Role of RANK ligand in mediating increased bone resorption in early postmenopausal women. J Clin Invest 2003;111:1221–1230CrossRefPubMedPubMedCentral Eghbali-Fatourechi G, Khosla S, Sanyal A, Boyle WJ, Lacey DL, Riggs BL. Role of RANK ligand in mediating increased bone resorption in early postmenopausal women. J Clin Invest 2003;111:1221–1230CrossRefPubMedPubMedCentral
32.
go back to reference Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Spelsberg TC, Riggs BL. Estrogen stimulates gene expression and protein production of osteoprotegerin in human osteoblastic cells. Endocrinology 1999;140:4367–4370PubMed Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Spelsberg TC, Riggs BL. Estrogen stimulates gene expression and protein production of osteoprotegerin in human osteoblastic cells. Endocrinology 1999;140:4367–4370PubMed
33.
go back to reference Schafer JJ, Manlangit K, Squires KE. Bone health and human immunodeficiency virus infection. Pharmacotherapy 2013;33:665–682CrossRefPubMed Schafer JJ, Manlangit K, Squires KE. Bone health and human immunodeficiency virus infection. Pharmacotherapy 2013;33:665–682CrossRefPubMed
Metadata
Title
Males seropositive for hepatitis B surface antigen are at risk of lower bone mineral density: the 2008–2010 Korea National Health and Nutrition Examination Surveys
Authors
Myong Ki Baeg
Seung Kew Yoon
Sun-Hye Ko
Kyung-Do Han
Hye Jin Choi
Si Hyun Bae
Jong Young Choi
Myung-Gyu Choi
Publication date
01-05-2016
Publisher
Springer India
Published in
Hepatology International / Issue 3/2016
Print ISSN: 1936-0533
Electronic ISSN: 1936-0541
DOI
https://doi.org/10.1007/s12072-015-9672-7

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