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The association between hepatitis and osteoporosis: a nested case-control study using a national sample cohort

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Abstract

Summary

The prevalence of hepatitis B was higher in osteoporosis patients than the control group, especially in females. However, the prevalence of hepatitis C was not different. The matching for various factors improved to have same conditions between osteoporosis patients and the control group.

Purpose

Although chronic liver disease, including hepatitis B and hepatitis C, has been associated with osteoporosis in previous studies, the evidence was insufficient, and some findings were inconsistent. The aim of this study was to evaluate the relationship between hepatitis B or hepatitis C and osteoporosis.

Methods

We used the Korean National Health Insurance Service-National Sample Cohort with ≥ 50-year-old participants from 2002 to 2013. Age was determined at osteoporosis diagnosis. We extracted 68,492 osteoporosis patients (ICD-10 codes E7001–E7004, HC341–HC345) with a 68,492-member control group at a ratio of 1:1 by age, sex, income, region of residence, hypertension, diabetes, and dyslipidemia. We analyzed previous histories of hepatitis B (ICD-10 codes B18.0–B18.1) and hepatitis C (ICD-10 code B18.2) in the osteoporosis patients and control groups. The logistic regression with the crude and adjusted model was analyzed. Additionally, subgroup analyses divided by age and sex were performed.

Results

The adjusted odds ratios for hepatitis B and hepatitis C were 1.19 (95% confidence interval (CI) = 1.11–1.28, P < 0.001) and 1.04 (95% CI = 0.90–1.19, P > 0.05), respectively, in osteoporosis patients. Subgroup analyses showed that the risk of hepatitis B was higher in osteoporosis patients in female groups but not in male groups.

Conclusion

Hepatitis B virus infection might be a risk factor for osteoporosis.

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References

  1. World Health Organization (2018) Hepatitis C https://www.who.int/news-room/fact-sheets/detail/hepatitis-c

  2. World Health Organization (2018) Hepatitis B https://www.who.int/en/news-room/fact-sheets/detail/hepatitis-b

  3. Cho EJ, Kim SE, Suk KT, An J, Jeong SW, Chung WJ, Kim YJ (2017) Current status and strategies for hepatitis B control in Korea. Clin Mol Hepatol 23(3):205–211. https://doi.org/10.3350/cmh.2017.0104

    Article  PubMed  PubMed Central  Google Scholar 

  4. Jeong S-H, Jang ES, Choi HY, Kim K-A, Chung W, Ki M (2017) Current status of hepatitis C virus infection and countermeasures in South Korea. Epidemiol Health 39

  5. Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis (1993). Am J Med 94 (6):646–650

  6. Cosman F, de Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R, National Osteoporosis F (2014) Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int 25(10):2359–2381. https://doi.org/10.1007/s00198-014-2794-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Wright NC, Saag KG, Dawson-Hughes B, Khosla S, Siris ES (2017) The impact of the new National Bone Health Alliance (NBHA) diagnostic criteria on the prevalence of osteoporosis in the USA. Osteoporos Int 28(4):1225–1232. https://doi.org/10.1007/s00198-016-3865-3

    Article  CAS  PubMed  Google Scholar 

  8. Choi YJ, Oh HJ, Kim DJ, Lee Y, Chung YS (2012) The prevalence of osteoporosis in Korean adults aged 50 years or older and the higher diagnosis rates in women who were beneficiaries of a national screening program: the Korea National Health and Nutrition Examination Survey 2008-2009. J Bone Miner Res 27(9):1879–1886. https://doi.org/10.1002/jbmr.1635

    Article  PubMed  Google Scholar 

  9. Guarino M, Loperto I, Camera S, Cossiga V, Di Somma C, Colao A, Caporaso N, Morisco F (2016) Osteoporosis across chronic liver disease. Osteoporos Int 27(6):1967–1977. https://doi.org/10.1007/s00198-016-3512-z

    Article  CAS  PubMed  Google Scholar 

  10. Lindor KD, Janes CH, Crippin JS, Jorgensen RA, Dickson ER (1995) Bone disease in primary biliary cirrhosis: does ursodeoxycholic acid make a difference? Hepatology 21(2):389–392

    CAS  PubMed  Google Scholar 

  11. van Leeuwen JP, van Driel M, van den Bemd GJ, Pols HA (2001) Vitamin D control of osteoblast function and bone extracellular matrix mineralization. Crit Rev Eukaryot Gene Expr 11(1–3):199–226

    PubMed  Google Scholar 

  12. Baeg MK, Yoon SK, Ko SH, Han KD, Choi HJ, Bae SH, Choi JY, Choi MG (2016) 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. Hepatol Int 10(3):470–477. https://doi.org/10.1007/s12072-015-9672-7

    Article  PubMed  Google Scholar 

  13. Byrne DD, Newcomb CW, Carbonari DM, Nezamzadeh MS, Leidl KB, Herlim M, Yang YX, Hennessy S, Kostman JR, Leonard MB, Localio AR, Lo Re V 3rd (2014) Risk of hip fracture associated with untreated and treated chronic hepatitis B virus infection. J Hepatol 61(2):210–218. https://doi.org/10.1016/j.jhep.2014.04.001

    Article  PubMed  PubMed Central  Google Scholar 

  14. Chen CH, Lin CL, Kao CH (2015) Association between chronic hepatitis B virus infection and risk of osteoporosis: a Nationwide population-based study. Medicine (Baltimore) 94(50):e2276. https://doi.org/10.1097/MD.0000000000002276

    Article  CAS  Google Scholar 

  15. Huang Z, Wei H, Cheng C, Yang S, Wang J, Liu X (2017) Low bone mineral density in chronic hepatitis B virus infection: a case-control study. Pak J Med Sci 33(2):457–461. https://doi.org/10.12669/pjms.332.12099

    Article  PubMed  PubMed Central  Google Scholar 

  16. Chen CH, Lin CL, Kao CH (2015) Relation between hepatitis C virus exposure and risk of osteoporosis: a Nationwide population-based study. Medicine (Baltimore) 94(47):e2086. https://doi.org/10.1097/MD.0000000000002086

    Article  CAS  Google Scholar 

  17. Gaudio A, Pennisi P, Muratore F, Bertino G, Ardiri A, Pulvirenti I, Tringali G, Fiore CE (2012) 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 23(7):656–660. https://doi.org/10.1016/j.ejim.2012.05.011

    Article  PubMed  Google Scholar 

  18. Lin JC, Hsieh TY, Wu CC, Chen PJ, Chueh TH, Chang WK, Chu HC (2012) Association between chronic hepatitis C virus infection and bone mineral density. Calcif Tissue Int 91(6):423–429. https://doi.org/10.1007/s00223-012-9653-y

    Article  CAS  PubMed  Google Scholar 

  19. Orsini LG, Pinheiro MM, Castro CH, Silva AE, Szejnfeld VL (2013) Bone mineral density measurements, bone markers and serum vitamin D concentrations in men with chronic non-cirrhotic untreated hepatitis C. PLoS One 8(11):e81652. https://doi.org/10.1371/journal.pone.0081652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gilbert L, He X, Farmer P, Rubin J, Drissi H, van Wijnen AJ, Lian JB, Stein GS, Nanes MS (2002) Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem 277(4):2695–2701. https://doi.org/10.1074/jbc.M106339200

  21. Gonzalez-Calvin JL, Gallego-Rojo F, Fernandez-Perez R, Casado-Caballero F, Ruiz-Escolano E, Olivares EG (2004) Osteoporosis, mineral metabolism, and serum soluble tumor necrosis factor receptor p55 in viral cirrhosis. J Clin Endocrinol Metab 89(9):4325–4330. https://doi.org/10.1210/jc.2004-0077

    Article  CAS  PubMed  Google Scholar 

  22. Lee J, Lee JS, Park SH, Shin SA, Kim K (2016) Cohort profile: The National Health Insurance Service-National Sample Cohort (NHIS-NSC), South Korea. Int J Epidemiol:dyv319. https://doi.org/10.1093/ije/dyv319

  23. National Health Insurance Sharing Service. National sample cohort. https://nhiss.nhis.or.kr/. Accessed October 24 2017

  24. Pelazas-Gonzalez R, Gonzalez-Reimers E, Aleman-Valls MR, Santolaria-Fernandez F, Lopez-Prieto J, Gonzalez-Diaz A, Gomez-Sirvent JL, de la Vega-Prieto MJ (2013) Bone alterations in hepatitis C virus infected patients. Eur J Intern Med 24 (1):92–96. doi:https://doi.org/10.1016/j.ejim.2012.09.007

  25. Gaudio A, Lasco A, Morabito N, Atteritano M, Vergara C, Catalano A, Fries W, Trifiletti A, Frisina N (2005) Hepatic osteodystrophy: does the osteoprotegerin/receptor activator of nuclear factor-kB ligand system play a role? J Endocrinol Investig 28(8):677–682

    Article  CAS  Google Scholar 

  26. Lopez-Larramona G, Lucendo AJ, Gonzalez-Castillo S, Tenias JM (2011) Hepatic osteodystrophy: an important matter for consideration in chronic liver disease. World J Hepatol 3(12):300–307. https://doi.org/10.4254/wjh.v3.i12.300

    Article  PubMed  PubMed Central  Google Scholar 

  27. Diez Ruiz A, Santos Perez JL, Lopez Martinez G, Gonzalez Calvin J, Gil Extremera B, Gutierrez Gea F (1993) Tumour necrosis factor, interleukin-1 and interleukin-6 in alcoholic cirrhosis. Alcohol Alcohol 28(3):319–323

    CAS  PubMed  Google Scholar 

  28. Khoruts A, Stahnke L, McClain CJ, Logan G, Allen JI (1991) Circulating tumor necrosis factor, interleukin-1 and interleukin-6 concentrations in chronic alcoholic patients. Hepatology 13(2):267–276

    Article  CAS  PubMed  Google Scholar 

  29. Luo XH, Guo LJ, Xie H, Yuan LQ, Wu XP, Zhou HD, Liao EY (2006) Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res 21(10):1648–1656. https://doi.org/10.1359/jbmr.060707

    Article  CAS  PubMed  Google Scholar 

  30. Gatta A, Verardo A, Di Pascoli M, Giannini S, Bolognesi M (2014) Hepatic osteodystrophy. Clin Cases Miner Bone Metab 11(3):185–191

    PubMed  PubMed Central  Google Scholar 

  31. Pignata S, Daniele B, Galati MG, Esposito G, Vallone P, Fiore F, Ricchi P, Pergola M (1997) Oestradiol and testosterone blood levels in patients with viral cirrhosis and hepatocellular carcinoma. Eur J Gastroenterol Hepatol 9(3):283–286

    Article  CAS  PubMed  Google Scholar 

  32. Bolland MJ, Grey A, Reid IR (2015) Skeletal health in adults with HIV infection. Lancet Diabetes Endocrinol 3(1):63–74. https://doi.org/10.1016/s2213-8587(13)70181-5

    Article  PubMed  Google Scholar 

  33. Farhat GN, Cauley JA (2008) The link between osteoporosis and cardiovascular disease. Clin Cases Miner Bone Metab 5(1):19–34

    PubMed  PubMed Central  Google Scholar 

  34. Gillis J, Smieja M, Cescon A, Rourke SB, Burchell AN, Cooper C, Raboud JM (2014) Risk of cardiovascular disease associated with HCV and HBV coinfection among antiretroviral-treated HIV-infected individuals. Antivir Ther 19(3):309–317. https://doi.org/10.3851/imp2724

    Article  CAS  PubMed  Google Scholar 

  35. Raison CL, Miller AH (2011) Is depression an inflammatory disorder? Curr Psychiatry Rep 13(6):467–475. https://doi.org/10.1007/s11920-011-0232-0

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The manuscript was edited for proper English language, grammar, punctuation, spelling, and overall style by the highly qualified native English-speaking editors at American Journal Experts (EF6A-C642-3739-A20A-499P).

Funding

This work was supported by the Hallym University Research Fund and in part by a research grant (NRF-2018-R1D1A1A02085328) from the National Research Foundation (NRF) of Korea.

Author information

Authors and Affiliations

  1. Hallym Data Science Laboratory, Hallym University College of Medicine, Anyang, South Korea

    Chanyang Min & Hyo Geun Choi

  2. Department of Otorhinolaryngology-Head & Neck Surgery, Hallym University College of Medicine, Anyang, South Korea

    Chanyang Min & Hyo Geun Choi

  3. Graduate School of Public Health, Seoul National University, Seoul, South Korea

    Chanyang Min

  4. Department of Urology, Hallym University College of Medicine, Anyang, South Korea

    Woo Jin Bang

  5. Department of Laboratory Medicine, Hallym University College of Medicine, Anyang, South Korea

    Miyoung Kim

  6. Department of Internal Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, South Korea

    Dong Jun Oh

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  1. Chanyang Min
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Corresponding author

Correspondence to Hyo Geun Choi.

Ethics declarations

The Ethics Committee of Hallym University (2014-I148) approved the use of the data from the Korean National Health Insurance Service-National Sample Cohort (NHIS-NSC). The Institutional Review Board waived the requirement for written informed consent.

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Min, C., Bang, W.J., Kim, M. et al. The association between hepatitis and osteoporosis: a nested case-control study using a national sample cohort. Arch Osteoporos 14, 34 (2019). https://doi.org/10.1007/s11657-019-0590-5

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