Should adults with diabetes mellitus be vaccinated against hepatitis B virus? A systematic review of diabetes mellitus and the progression of hepatitis B disease

References

• World Health Organization. Global Status Report on non-communicable diseases. 2014. http://www.who.int/nmh/publications/ncd-status-report-2014/en/ (accessed December 2016)
   Google Scholar
• World Health Organization. Hepatitis B factsheet. 2015. www.who.int/mediacentre/factsheets/fs204/en/ (accessed December 2016)
   Google Scholar
• World Health Organization. Hepatitis B vaccines: WHO position paper–recommendations. Vaccine 2010; 28(3):589-90; PMID:19896455; https://doi.org/10.1016/j.vaccine.2009.10.110
   PubMedGoogle Scholar
• Schillie SF, Xing J, Murphy TV, Hu DJ. Prevalence of hepatitis B virus infection among persons with diagnosed diabetes mellitus in the United States, 1999-2010. J Viral Hepat 2012; 19(9):674-6; PMID:22863272; https://doi.org/10.1111/j.1365-2893.2012.01616.x
   PubMed Web of Science ®Google Scholar
• Reilly ML, Schillie SF, Smith E, Poissant T, Vonderwahl CW, Gerard K, Baumgartner J, Mercedes L, Sweet K, Muleta D, et al. Increased risk of acute hepatitis B among adults with diagnosed diabetes mellitus. J Diabetes Sci Technol 2012; 6(4):858-66; PMID:22920812; https://doi.org/10.1177/193229681200600417
   PubMedGoogle Scholar
• Collier B, Dossett LA, May AK, Diaz JJ. Glucose control and the inflammatory response. Nutr Clin Pract 2008; 23(1):3-15; PMID:18203960; https://doi.org/10.1177/011542650802300103
   PubMed Web of Science ®Google Scholar
• Leclercq IA, Da Silva Morais A, Schroyen B, Van Hul N, Geerts A. Insulin resistance in hepatocytes and sinusoidal liver cells: Mechanisms and consequences. J Hepatol 2007; 47(1):142-56; PMID:17512085; https://doi.org/10.1016/j.jhep.2007.04.002
   PubMed Web of Science ®Google Scholar
• Postic C, Dentin R, Girard J. Role of the liver in the control of carbohydrate and lipid homeostasis. Diabetes Metab 2004; 30(5):398-408; PMID:15671906; https://doi.org/10.1016/S1262-3636(07)70133-7
   PubMed Web of Science ®Google Scholar
• Raddatz D, Ramadori G. Carbohydrate metabolism and the liver: Actual aspects from physiology and disease. Z Gastroenterol 2007; 45(1):51-62; PMID:17236121; https://doi.org/10.1055/s-2006-927394
   PubMed Web of Science ®Google Scholar
• Tappy L, Minehira K. New data and new concepts on the role of the liver in glucose homeostasis. Curr Opin Clin Nutr Metab Care 2001; 4(4):273-7; PMID:11458020; https://doi.org/10.1097/00075197-200107000-00005
   PubMed Web of Science ®Google Scholar
• Teli T, Xanthaki D, Karalis KP. Regulation of appetite and insulin signaling in inflammatory states. Ann N Y Acad Sci 2006; 1083:319-28; PMID:17148747; https://doi.org/10.1196/annals.1367.022
   PubMed Web of Science ®Google Scholar
• Chen CL, Yang HI, Yang WS, Liu CJ, Chen PJ, You SL, Wang LY, Sun CA, Lu SN, Chen DS, et al. Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: A follow-up study in Taiwan. Gastroenterology 2008; 135(1):111-21; PMID:18505690; https://doi.org/10.1053/j.gastro.2008.03.073
   PubMed Web of Science ®Google Scholar
• Hsiang JC, Wong GL, Chan HL, Chan AW, Chim AM, Wong VW. Metabolic syndrome delays HBeAg seroclearance in Chinese patients with hepatitis B. Aliment Pharmacol Ther 2014; 40(6):716-26; PMID:25039861; https://doi.org/10.1111/apt.12874
   PubMed Web of Science ®Google Scholar
• Huang YW, Wang TC, Lin SC, Chang HY, Chen DS, Hu JT, Yang SS, Kao JH. Increased risk of cirrhosis and its decompensation in chronic hepatitis B patients with newly diagnosed diabetes: A nationwide cohort study. Clin Infect Dis 2013; 57(12):1695-702; PMID:24051864; https://doi.org/10.1093/cid/cit603
   PubMed Web of Science ®Google Scholar
• Li Q, Li WW, Yang X, Fan WB, Yu JH, Xie SS, Liu L, Ma LX, Chen SJ, Kato N. Type 2 diabetes and hepatocellular carcinoma: A case-control study in patients with chronic hepatitis B. Int J Cancer 2012; 131(5):1197-202; PMID:22052244; https://doi.org/10.1002/ijc.27337
   PubMed Web of Science ®Google Scholar
• Bi Y, Min M, Shen W, Deng P, Du Q, Dong M, Liu Y. Prognostic value of high sensitivity C-reaction protein in non-insulin dependent diabetes mellitus patients with non-alcoholic fatty liver disease. Int J Clin Exp Pathol 2015; 8(7):8494-9; PMID:26339423.
   PubMed Web of Science ®Google Scholar
• Shimada M, Hashimoto E, Kaneda H, Noguchi S, Hayashi N. Nonalcoholic steatohepatitis: Risk factors for liver fibrosis. Hepatol Res 2002; 24(4):429-38; PMID:12479942; https://doi.org/10.1016/S1386-6346(02)00246-2
   PubMed Web of Science ®Google Scholar
• Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 2016; 64(1):73-84; PMID:26707365; https://doi.org/10.1002/hep.28431
   PubMed Web of Science ®Google Scholar
• Adinolfi LE, Gambardella M, Andreana A, Tripodi MF, Utili R, Ruggiero G. Steatosis accelerates the progression of liver damage of chronic hepatitis C patients and correlates with specific HCV genotype and visceral obesity. Hepatology 2001; 33(6):1358-64; PMID:11391523; https://doi.org/10.1053/jhep.2001.24432
   PubMed Web of Science ®Google Scholar
• Lonardo A, Adinolfi LE, Loria P, Carulli N, Ruggiero G, Day CP. Steatosis and hepatitis C virus: Mechanisms and significance for hepatic and extrahepatic disease. Gastroenterology 2004; 126(2):586-97; PMID:14762795; https://doi.org/10.1053/j.gastro.2003.11.020
   PubMed Web of Science ®Google Scholar
• Ong JP, Younossi ZM, Speer C, Olano A, Gramlich T, Boparai N. Chronic hepatitis C and superimposed nonalcoholic fatty liver disease. Liver 2001; 21(4):266-71; PMID:11454190; https://doi.org/10.1034/j.1600-0676.2001.021004266.x
   PubMedGoogle Scholar
• Altlparmak E, Koklu S, Yalinkilic M, Yuksel O, Cicek B, Kayacetin E, Sahin T. Viral and host causes of fatty liver in chronic hepatitis B. World J Gastroenterol 2005; 11(20):3056-9; PMID:15918189; https://doi.org/10.3748/wjg.v11.i20.3056
   PubMed Web of Science ®Google Scholar
• Cheng YL, Wang YJ, Kao WY, Chen PH, Huo TI, Huang YH, Lan KH, Su CW, Chan WL, Lin HC, et al. Inverse association between hepatitis B virus infection and fatty liver disease: a large-scale study in populations seeking for check-up. PloS One 2013; 8(8):e72049; PMID:23991037; https://doi.org/10.1371/journal.pone.0072049
   PubMed Web of Science ®Google Scholar
• Thomopoulos KC, Arvaniti V, Tsamantas AC, Dimitropoulou D, Gogos CA, Siagris D, Theocharis GJ, Labropoulou-Karatza C. Prevalence of liver steatosis in patients with chronic hepatitis B: A study of associated factors and of relationship with fibrosis. Eur J Gastroenterol Hepatol 2006; 18(3):233-7; PMID:16462535; https://doi.org/10.1097/00042737-200603000-00002
   PubMed Web of Science ®Google Scholar
• Centers for Disease Control and Prevention (CDC). Use of hepatitis B vaccination for adults with diabetes mellitus: Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 2011; 60(50):1709-11; PMID:22189894
   PubMedGoogle Scholar
• FOD Volksgezondheid en Sociale Zekerheid /SPF Santé Publique et Securité Sociale. Vaccination contre l'hépatite B. 2013.
   Google Scholar
• Huo T, Wu JC, Hwang SJ, Lai CR, Lee PC, Tsay SH, Chang FY, Lee SD. Factors predictive of liver cirrhosis in patients with chronic hepatitis B: A multivariate analysis in a longitudinal study. Eur J Gastroenterol Hepatol 2000; 12(6):687-93; PMID:10912490; https://doi.org/10.1097/00042737-200012060-00019
   PubMed Web of Science ®Google Scholar
• Papatheodoridis GV, Chrysanthos N, Savvas S, Sevastianos V, Kafiri G, Petraki K, Manesis EK. Diabetes mellitus in chronic hepatitis B and C: Prevalence and potential association with the extent of liver fibrosis. J Viral Hepat 2006; 13(5):303-10; PMID:16637860; https://doi.org/10.1111/j.1365-2893.2005.00677.x
   PubMed Web of Science ®Google Scholar
• Wong GL, Chan HL, Yu Z, Chan AW, Choi PC, Chim AM, Chan HY, Tse CH, Wong VW. Coincidental metabolic syndrome increases the risk of liver fibrosis progression in patients with chronic hepatitis B–a prospective cohort study with paired transient elastography examinations. Aliment Pharmacol Ther 2014; 39(8):883-93; PMID:24612251; https://doi.org/10.1111/apt.12658
   PubMed Web of Science ®Google Scholar
• Mallet V, Hamed K, Schwarzinger M. Prognosis of patients with chronic hepatitis B in France (2008-2013): A nationwide, observational and hospital-based study. J Hepatol 2017; 66(3):514-20; PMID:27826056; https://doi.org/10.1016/j.jhep.2016.10.031
   PubMed Web of Science ®Google Scholar
• Chen C, Chen J, Wang J, Chang K, Tseng P, Kee K, Chen PF, Tsai LS, Chen SC, Lin SC, et al. Diabetes mellitus, metabolic syndrome and obesity are not significant risk factors for hepatocellular carcinoma in an HBV- and HCV-endemic area of Southern Taiwan. Kaohsiung J Med Sci 2013; 29:451-9; PMID:23906236; https://doi.org/10.1016/j.kjms.2012.12.006
   PubMed Web of Science ®Google Scholar
• Fu SC, Huang YW, Wang TC, Hu JT, Chen DS, Yang SS. Increased risk of hepatocellular carcinoma in chronic hepatitis B patients with new onset diabetes: A nationwide cohort study. Aliment Pharmacol Ther 2015; 41(11):1200-9; PMID:25846548; https://doi.org/10.1111/apt.13191
   PubMed Web of Science ®Google Scholar
• Ko WH, Chiu SY, Yang KC, Chen HH. Diabetes, hepatitis virus infection and hepatocellular carcinoma: A case-control study in hepatitis endemic area. Hepatol Res 2012; 42(8):774-81; PMID:22469194; https://doi.org/10.1111/j.1872-034X.2012.00979.x
   PubMed Web of Science ®Google Scholar
• Wang CS, Yao WJ, Chang TT, Wang ST, Chou P. The impact of type 2 diabetes on the development of hepatocellular carcinoma in different viral hepatitis statuses. Cancer Epidemiol Biomarkers Prev 2009; 18(7):2054-60; PMID:19549812; https://doi.org/10.1158/1055-9965.EPI-08-1131
   PubMed Web of Science ®Google Scholar
• Xiong J, Wang J, Huang J, Sun W, Wang J, Chen D. Non-alcoholic steatohepatitis-related liver cirrhosis is increasing in China: A ten-year retrospective study. Clinics (Sao Paulo, Brazil) 2015; 70(8):563-8; PMID:26247669; https://doi.org/10.6061/clinics/2015(08)06
   PubMed Web of Science ®Google Scholar
• Seo YS, Kim MN, Kim SU, Kim SG, Um SH, Han KH, Kim YS. Risk assessment of hepatocellular carcinoma using transient elastography Vs. liver biopsy in chronic hepatitis B patients receiving antiviral therapy. Medicine 2016; 95(12):e2985; PMID:27015173; https://doi.org/10.1097/MD.0000000000002985
   PubMed Web of Science ®Google Scholar
• Hsiang JC, Gane EJ, Bai WW, Gerred SJ. Type 2 diabetes: A risk factor for liver mortality and complications in hepatitis B cirrhosis patients. J Gastroenterol Hepatol 2015; 30(3):591-9; PMID:25250942; https://doi.org/10.1111/jgh.12790
   PubMed Web of Science ®Google Scholar
• Huo TI, Wu JC, Lui WY, Lee PC, Huang YH, Chau GY, Tsay SH, Chang FY, Lee SD. Diabetes mellitus is a recurrence-independent risk factor in patients with hepatitis B virus-related hepatocellular carcinoma undergoing resection. Eur J Gastroenterol Hepatol 2003; 15(11):1203-8; PMID:14560154; https://doi.org/10.1097/00042737-200311000-00009
   PubMed Web of Science ®Google Scholar
• Ribes J, Cleries R, Rubio A, Hernandez JM, Mazzara R, Madoz P, Casanovas T, Casanova A, Gallen M, Rodríguez C, et al. Cofactors associated with liver disease mortality in an HBsAg-positive Mediterranean cohort: 20 years of follow-up. Int J Cancer 2006; 119(3):687-94; PMID:16496403; https://doi.org/10.1002/ijc.21882
   PubMed Web of Science ®Google Scholar
• Stepanova M, Rafiq N, Younossi ZM. Components of metabolic syndrome are independent predictors of mortality in patients with chronic liver disease: A population-based study. Gut 2010; 59(10):1410-5; PMID:20660697; https://doi.org/10.1136/gut.2010.213553
   PubMed Web of Science ®Google Scholar
• Szpakowski JL, Tucker LY. Causes of death in patients with hepatitis B: A natural history cohort study in the United States. Hepatology (Baltimore, Md) 2013; 58(1):21-30; PMID:23080403; https://doi.org/10.1002/hep.26110
   PubMed Web of Science ®Google Scholar
• Ling Q, Xu X, Wei Q, Wei X, Wang Z, Zhou L, Zheng S. Impact of preexisting diabetes mellitus on outcome after liver transplantation in patients with hepatitis B virus-related liver disease. Dig Dis Sci 2011; 56(3):889-93; PMID:20703811; https://doi.org/10.1007/s10620-010-1358-3
   PubMed Web of Science ®Google Scholar
• Bondini S, Kallman J, Wheeler A, Prakash S, Gramlich T, Jondle DM, Younossi ZM. Impact of non-alcoholic fatty liver disease on chronic hepatitis B. Liver Int 2007; 27(5):607-11; PMID:17498244; https://doi.org/10.1111/j.1478-3231.2007.01482.x
   PubMed Web of Science ®Google Scholar
• Hsieh PS, Hsieh YJ. Impact of liver diseases on the development of type 2 diabetes mellitus. World J Gastroenterol 2011; 17(48):5240-5; PMID:22219592; https://doi.org/10.3748/wjg.v17.i48.5240
   PubMed Web of Science ®Google Scholar
• Kingston ME, Ali MA, Atiyeh M, Donnelly RJ. Diabetes mellitus in chronic active hepatitis and cirrhosis. Gastroenterology 1984; 87(3):688-94; PMID:6086443.
   PubMed Web of Science ®Google Scholar
• Megyesi C, Samols E, Marks V. Glucose tolerance and diabetes in chronic liver disease. Lancet (London, England) 1967; 2(7525):1051-6; PMID:4168535; https://doi.org/10.1016/S0140-6736(67)90334-0
   PubMed Web of Science ®Google Scholar
• Hoerger TJ, Schillie S, Wittenborn JS, Bradley CL, Zhou F, Byrd K, Murphy TV. Cost-effectiveness of hepatitis B vaccination in adults with diagnosed diabetes. Diabetes Care 2013; 36(1):63-9; PMID:22933435; https://doi.org/10.2337/dc12-0759
   PubMed Web of Science ®Google Scholar
• Coordination of Cancer Clinical Practice Guidelines in Europe. www.cocancpg.eu/ (accessed December 2016)
   Google Scholar