Background: The relation between hepatitis C virus (HCV) infection and the development of type 2 diabetes mellitus (T2DM) remains unknown. The aim of this study was to investigate the presence of an association between T2DM and HCV. Methods: A case control study was conducted at the outpatients’ clinics of Kasr El-Aini Hospital (KAH), from October 2013 till March 2014. In this study, 389 HCV patients were selected as cases and 389 healthy controls were also included. Demographic and clinical data were collected using a structured questionnaire. Laboratory investigations including liver function tests (LFT), blood glucose level and radioimmunoblot assay (ELISA) were performed. Results: Out of 389 HCV cases, 219 (56.3%) were diabetic, whereas 145 (37.3%) were diabetic among the healthy controls. Occurrence of diabetes among cirrhotic patients was 1.7 times higher than non-cirrhotic. Logistic regression showed that residence (P < 0.001, OR = 2.7), occupation (P = 0.03, OR = 1.8), and smoking (P = 0.04, OR = 2) were the predictive factors for occurrence of T2DM in HCV patients. Conclusions: In this study, we found a positive association between HCV infection and T2DM. Residence, occupation and smoking were the predictive factors for the association of T2DM in HCV patients, whereas hypertension and BMI were only adjunctive factors.
KeywordsHCVPredictive FactorsT2DMCirrhosis
Bostan, N. and Mahmood, T. (2010) An Overview about Hepatitis C: A Devastating Virus. Critical Reviews in Microbiology, 36, 91-133. http://dx.doi.org/10.3109/10408410903357455
Esmat, G. (2013) Hepatitis C in the Eastern Mediterranean Region. Eastern Mediterranean Health Journal, 19, 587-588.
El-Zanaty, F. and Way, A. (2009) Egypt Demographic and Health Survey 2008. Ministry of Health, El-Zanaty and Associates, and Macro International, Cairo.
(2004) Global Burden of Disease (GBD) for Hepatitis C. Journal of Clinical Pharmacology, 44, 20-29. http://dx.doi.org/10.1177/0091270003258669
Alter, M.J. (2007) Epidemiology of Hepatitis C Virus Infection. World Journal of Gastroenterology, 13, 2436. http://dx.doi.org/10.3748/wjg.v13.i17.2436
Lecube, A., Hernandez, C., Genesca, J. and Esteban, J. (2004) Diabetes Is the Main Factor Accounting for the High Ferritin Levels Detected in Chronic HCV Infection. Diabetes Care, 27, 2669-2675. http://dx.doi.org/10.2337/diacare.27.11.2669
Negro, F. and Alaei, M. (2009) Hepatitis C Virus and Type 2 Diabetes. World Journal of Gastroenterology, 15, 1537-1547. http://dx.doi.org/10.3748/wjg.15.1537
Waheed, Y., Safi, S.Z. and Qadri, I. (2011) Role of Potash Alum in Hepatitis C Virus Transmission at Barber’s Shop. Virology Journal, 8, 211. http://dx.doi.org/10.1186/1743-422X-8-211
Safi, S.Z., Qvist, R., Kumar, S., Batumalaie, K. and Ismail, I.S. (2014) Molecular Mechanisms of Diabetic Retinopathy, General Preventive Strategies, and Novel Therapeutic Targets. BioMed Research International, 2014, Article ID: 801269. http://dx.doi.org/10.1155/2014/801269
Mehta, S.H., Brancati, F.L., Sulkowski, M.S., Strathdee, S.A., Szklo, M. and Thomas, D.L. (2000) Prevalence of Type 2 Diabetes Mellitus among Persons with Hepatitis C Virus Infection in the United States. Annals of Internal Medicine, 133, 592-599. http://dx.doi.org/10.7326/0003-4819-133-8-200010170-00009
Antonelli, A., Ferri, C., Fallahi, P., Ferrari, S.M., Ghinoi, A., Rotondi, M., et al. (2006) Thyroid Disorders in Chronic Hepatitis C Virus Infection. Thyroid, 16, 563-572. http://dx.doi.org/10.1089/thy.2006.16.563
Sanzone, A.M. and Begue, R.E. (2006) Hepatitis C and Arthritis: An Update. Infectious Disease Clinics of North America, 20, 877-889. http://dx.doi.org/10.1016/j.idc.2006.09.010
Chen, L.K., Hwang, S.J., Tsai, S.T., Luo, J.C., Lee, S.D. and Chang, F.Y. (2003) Glucose Intolerance in Chinese Patients with Chronic Hepatitis C. World Journal of Gastroenterology, 9, 505-508. http://dx.doi.org/10.3748/wjg.v9.i3.505
Wilson, C. (2004) Hepatitis C Infection and Type 2 Diabetes in American-Indian Women. Diabetes Care, 27, 2116-2719. http://dx.doi.org/10.2337/diacare.27.9.2116
Mohamoud, Y., Mumtaz, G., Riome, S., Miller, D. and Abu-Raddad, L. (2013) The Epidemiology of Hepatitis C Virus in Egypt: A Systematic Review and Data Synthesis. BMC Infectious Diseases, 13, 288. http://dx.doi.org/10.1186/1471-2334-13-288
Chehadeh, W., Abdella, N., Ben-Nakhi, A., Al-Arouj, M. and Al-Nakib, W. (2009) Risk Factors for the Development of Diabetes Mellitus in Chronic Hepatitis C Virus Genotype 4 Infection. Journal of Gastroenterology, 24, 42-48. http://dx.doi.org/10.1111/j.1440-1746.2008.05503.x
Elhawary, E.I., Mahmoud, G.F., El-Daly, M.A., Mekky, F.A., Esmat, G.G. and Abdel-Hamid, M. (2011) Association of HCV with Diabetes Mellitus: An Egyptian Case-Control Study. Virology Journal, 8, 367-377.
Corsini, A. (2009) Free Statistics. Free Statistical Software Comparisons. http://en.freestatistics.info/comp.php
American Diabetes Association (ADA) (2008) Diagnosis and Classification of Diabetes Mellitus. Diabetes Care, 31, S55-S60.
World Health Organization (WHO) (2000) Obesity: Preventing and Managing the Global Epidemic. Report of a WHO Consultation. Technical Report Series No. 894, World Health Organization, Geneva. http://www. who.int/nutrition/publications/obesity/WHO_TRS_894/en/
Levesque, R. (2007) SPSS Programming and Data Management. A Guide for SPSS and SAS Users. 4th Edition, SPSS Inc., Chicago.
Medical Association Declaration of Helsinki-Ethical Principles for Medical Research Involving Human Subjects. http://www.wma.net/en/30publications/10policies/b3/index.html
Gulcan, A., Gulcan, E., Toker, A., Bulut, I. and Akcan, Y. (2008) Evaluation of Risk Factors and Seroprevalence of Hepatitis B and C in Diabetic Patients in Kutahya, Turkey. Journal of Investigative Medicine, 56, 858-863.
Costa, L.M., Mussi, A.D., Brianeze, M.R. and Souto, F.J. (2008) Hepatitis C as a Risk Factor for Diabetes Type 2: Lack of Evidence in a Hospital in Central-West Brazil. Brazilian Journal of Infectious Diseases, 12, 24-26. http://dx.doi.org/10.1590/S1413-86702008000100007
Kaabia, N., Ben Jazia, E., Slim, I., Fodha, I., Hachfi, W., Gaha, R., et al. (2009) Association of Hepatitis C Virus Infection and Diabetes in Central Tunisia. World Journal of Gastroenterology, 15, 2778-2781. http://dx.doi.org/10.3748/wjg.15.2778
Ali, S., Abera, S., Mihret, A. and Abebe, T. (2012) Association of Hepatitis C Virus Infection with Type II Diabetes in Ethiopia: A Hospital-Based Case-Control Study. Interdisciplinary Perspectives on Infectious Diseases, 2012, Article ID: 354656. http://dx.doi.org/10.1155/2012/354656
Sadik, M.M., Islam, A.Z., Naz, F., Zaki, M., Kumar, S. and Ali, B.A. (2013) Prevalence of Type 2 Diabetes Mellitus in Hepatitis C Virus Infected Population: A Southeast Asian Study Hindawi. Journal of Diabetes Research, 2013, Article ID: 539361. http://dx.doi.org/10.1155/2013/539361
Wang, C.S., Wang, S.T., Yao, W.J., Chang, T.T. and Chou, P. (2007) Hepatitis C Virus Infection and the Development of Type 2 Diabetes in a Community-Based Longitudinal Study. American Journal of Epidemiology, 166, 196-203. http://dx.doi.org/10.1093/aje/kwm061
Veldt, B.J., Chen, W., Heathcote, E.J., Wedemeyer, H., Reichen, J., Hofmann, W.P., et al. (2008) Increased Risk of Hepatocellular Carcinoma among Patients with Hepatitis C Cirrhosis and Diabetes Mellitus. Hepatology, 47, 1856-1862. http://dx.doi.org/10.1002/hep.22251
Herman, W.H., Ali, M.A., Aubert, R.E., Engelgau, M.M., Kenny, S.J., Gunter, E.W., et al. (1995) Diabetes Mellitus in Egypt: Risk Factors and Prevalence. Diabetic Medicine, 12, 1126-1131. http://dx.doi.org/10.1111/j.1464-5491.1995.tb00432.x
Sadikot, S.M., Nigam, A., Das, S., Bajaj, S., Zargar, A.H. and Sosale, A. (2004) The Burden of Diabetes and Impaired Glucose Tolerance in India Using the WHO 1999 Criteria; Prevalence of Diabetes in India Study (PODIS). Diabetes Research and Clinical Practice, 66, 301-307. http://dx.doi.org/10.1016/j.diabres.2004.04.008
Zhao, P., Wang, J.B. and Jiao, J. (2006) Investigation on the Incidence of Diabetes in Chronic Hepatitis C Patients and Their HCV Genotypes. Chinese Journal of Hepatology, 14, 86-88.
Giordanino, C., Bugianesi, E., Smedile, A., Ciancio, A., Abate, M.L., Olivero, A., et al. (2008) Incidence of Type 2 Diabetes Mellitus and Glucose Abnormalities in Patients with Chronic Hepatitis C Infection by Response to Treatment: Results of a Cohort Study. American Journal of Gastroenterology, 103, 2481-2487. http://dx.doi.org/10.1111/j.1572-0241.2008.02002.x
Wlazlo, N., Beijers, B.H., Schoon, E.J., Sauerwein, H.P., Stehouwer, C.D. and Bravenboer, B. (2010) High Prevalence of Diabetes Mellitus in Patients with Liver Cirrhosis. Diabetic Medicine, 27, 1308-1311. http://dx.doi.org/10.1111/j.1464-5491.2010.03093.x
Singal, A. and Ayoola, A. (2008) Prevalence and Factors Affecting Occurrence of Type 2 Diabetes Mellitus in Saudi Patients with Chronic Liver Disease. Saudi Journal of Gastroenterology, 14, 118-121. http://dx.doi.org/10.4103/1319-3767.41729
Costantini, S., Capone, F., Guerriero, E., Marfella, R., Sorice, A., Maio, P., et al. (2012) Cytokine Profile of Patients with Type 2 Diabetes and/or Chronic Hepatitis C Infection. PLoS ONE, 7, e39486. http://dx.doi.org/10.1371/journal.pone.0039486
Stepanova, M., Lam, B., Younossi, Y., Srishord, M.K. and Younossi, Z.M. (2012) Association of Hepatitis C with Insulin Resistance and Type 2 Diabetes in US General Population: The Impact of the Epidemic of Obesity. Journal of Viral Hepatitis, 19, 341-345. http://dx.doi.org/10.1111/j.1365-2893.2011.01554.x
Wild, S., Roglic, G., Green, A., Sicree, R. and King, H. (2004) Global Prevalence of Diabetes; Estimates for the Year 2000 and Projection for 2030. Diabetes Care, 27, 1047-1053. http://dx.doi.org/10.2337/diacare.27.5.1047
Huang, J.F., Dai, C.Y., Hwang, S.J., Ho, C.K., Hsiao, P.J., Hsieh, M.Y., et al. (2007) Hepatitis C Viremia Increases the Association with Type 2 Diabetes Mellitus in a Hepatitis B and C Endemic Area: An Epidemiological Link with Virological Implication. American Journal of Gastroenterology, 102, 1237-1243. http://dx.doi.org/10.1111/j.1572-0241.2007.01181.x
Rajesh, N.G. and Sadiq, K.A. (2012) Seroprevalence and Risk Factors for Hepatitis C Virus Infection among General Population in Central Region of Yemen. Hepatitis Research and Treatment, 2012, Article ID: 689726.
Wang, C.S., Wang, S.T. and Chang, T.T. (2002) Smoking and Alanine Transferase Levels in Hepatitis C: Implications for Prevention of HCV Progression. Archives of Internal Medicine, 162, 811-815. http://dx.doi.org/10.1001/archinte.162.7.811
Eissa, N.A., Ghonaim, M., ElBanna, H., Bakr, A., Mostafa, M.S., Shoeib, S. and AbdelMoteleb, T. (2003) HCV-Related Chronic Liver Disease Co-Factors That Determine the Severity and Prognosis. Egyptian Journal of Medical Microbiology, 12, 123-133.
Alavian, S.M., Hajarizadeh, B., Nematizadeh, F. and Larijini, B. (2004) Prevalence and Determinants of Diabetes Mellitus among Iranian Patients with Chronic Liver Disease. BMC Endocrine Disorders, 4, 4. http://dx.doi.org/10.1186/1472-6823-4-4
Marchesini, G., Ronchi, M., Forlani, G., Bugianesi, E., Bianchi, G., Fabbri, A., et al. (1999) Cardiovascular Disease in Cirrhosis. American Journal of Gastroenterology, 94, 655-662.
Ndako, J.A., Echeonwu, G.O., Shidali, N.N., Bichi, I.A., Paul, G.A., Onovoh, E., et al. (2009) Occurrence of Hepatitis C Virus Infection in Type 2 Diabetic Patients Attending Plateau State Specialist Hospital Jos Nigeria. Virology Journal, 6, 98. http://dx.doi.org/10.1186/1743-422X-6-98
Zimmet, P., Alberti, K.G. and Shaw, J. (2001) Global and Societal Implications of the Diabetes Epidemic. Nature, 414, 782-787. http://dx.doi.org/10.1038/414782a
Lonardo, A., Adinolfi, L.E., Loria, P., Carulli, N., Ruggiero, G. and Day, C.P. (2004) Steatosis and Hepatitis C Virus: Mechanisms and Significance for Hepatic and Extrahepatic Disease. Gastroenterology, 126, 586-597. http://dx.doi.org/10.1053/j.gastro.2003.11.020
Harris, M.I. (2005) Elevated Liver Function Tests in Type II DM. Clinical Diabetes, 23, 115-119. http://dx.doi.org/10.2337/diaclin.23.3.115
Jadoon, N.A., Shahzad, M.A., Yaqoob, R., Hussain, M. and Ali, N. (2010) Seroprevalence of Hepatitis C in Type 2 Diabetes: Evidence for a Positive Association. Virology Journal, 7, 304.