Original Article

Frequency and genotype distribution of hepatitis C virus infection in patients with diabetes type 2 in Ahvaz, Iran


Background and Objectives: Diabetes is recognized as a great concern and a public health problem worldwide. Several factors including environmental and genetic factors have been involved. Recently, infectious agents such as hepatitis C virus (HCV) have been reported to be associated with diabetes. Thus, this study was conducted to determine the frequency of HCV infection among patients with diabetes type 2 in Ahvaz city, Iran.
Materials and Methods: A case-control study design was conducted at Ahvaz Jundishapur University of Medical Sciences. A total of 600 study subjects were included in this research. All the patient sera were tested for Anti- HCV antibody, HBsAg, and HIV antibody. The sera of positive Anti-HCV antibody, were assayed for 5'- UTR and core regions of the HCV genome by Nested RT-PCR. Finally, the HCV genotyping was determined by sequencing.
Results: The prevalence of HCV in type 2 diabetes and nondiabetic controls was 2% and 0.33%, respectively. The distribution of HCV genotypes among the HCV-positive patients were 3a (1.66%) and 1a (0.33%).
Conclusion: To control and improve the treatment, the screening of HCV infection with anti-HCV antibody was followed by molecular techniques such as PCR and HCV genotyping which should be implemented for all patients with diabetes type 2.

1. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes care 2013;36 Suppl 1(Suppl 1):S67-S74.
2. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 2014;103:137-149.
3. Ardeshir Larijani MB, BANDARIAN F. On diabetes mellitus and hepatitis C infection: should the patients be screened? Hepat Mon 2009;9:92-94.
4. Petruzziello A, Marigliano S, Loquercio G, Cozzolino A, Cacciapuoti C. Global epidemiology of hepatitis C virus infection: an up-date of the distribution and circulation of hepatitis C virus genotypes. World J Gastroenterol 2016;22:7824-7840.
5. Drazilova S, Gazda J, Janicko M, Jarcuska P. Chronic hepatitis C association with diabetes mellitus and cardiovascular risk in the era of DAA therapy. Can J Gastroenterol Hepatol 2018;2018:6150861.
6. Jalilian S, Latifi SM, Makvandi M, Teimoori A, Azaran A, Parsanahad M, et al. The evaluation of interferon lambda 4 rs368234815 as a predictor factor in treated patients with chronic hepatitis C genotype 1a infection. Indian J Med Microbiol 2017;35:262-268.
7. El-Shamy A, Hotta H. Impact of hepatitis C virus heterogeneity on interferon sensitivity: an overview. World J Gastroenterol 2014;20:7555-7569.
8. Zhang X, Dou J, Germann MW. Characterization of the cellular immune response in hepatitis C virus infection. Med Res Rev 2009;29:843-866.
9. Pachiadakis I, Pollara G, Chain BM, Naoumov NV. Is hepatitis C virus infection of dendritic cells a mechanism facilitating viral persistence? Lancet Infect Dis 2005;5:296-304.
10. Umar M, Bilal M. Hepatitis C, a mega menace: a Pakistani perspective. J Pioneer Med Sci 2012;2:68-72.
11. Ali SS, Ali IS, Aamir AH, Jadoon Z, Inayatullah S. Frequency of hepatitis C infection in diabetic patients. J Ayub Med Coll Abbottabad 2007;19:46-49.
12. Khodabandehloo M, Roshani D, Sayehmiri K. Prevalence and trend of hepatitis C virus infection among blood donors in Iran: a systematic review and meta-analysis. J Res Med Sci 2013;18:674-682.
13. Alavian SM, Adibi P, ZALI MR. Hepatitis C virus in Iran: epidemiology of an emerging infection. Arch Iran Med 2005;8:84-90.
14. Andalibalshohada A, Rezaii SA, Abedi F. HCV prevalence and predominant genotype in IV drug users. Rev Clin Med 2014;1:200-206.
15. Merat S, Poustchi H. Hepatitis C in Iran. How extensive of a problem is it? Arch Iran Med 2012;15:268.
16. Marzouk D, Sass J, Bakr I, El Hosseiny M, Abdel-Hamid M, Rekacewicz C, et al. Metabolic and cardiovascular risk profiles and hepatitis C virus infection in rural Egypt. Gut 2007;56:1105–1110.
17. El‐Serag HB, Hampel H, Yeh C, Rabeneck L. Extrahepatic manifestations of hepatitis C among United States male veterans. Hepatology 2002;36:1439-1445.
18. Taherkhani R, Farshadpour F. Epidemiology of hepatitis C virus in Iran. World J Gastroenterol 2015;21:10790-10810.
19. Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. Global epidemiology of hepatitis C virus infection: new estimates of age‐specific antibody to HCV seroprevalence. Hepatology 2013;57:1333-1342.
20. Abenavoli L, Masarone M, Peta V, Milic N, Kobyliak N, Rouabhia S, et al. Insulin resistance and liver steatosis in chronic hepatitis C infection genotype 3. World J gastroenterol 2014;20:15233-15240.
21. Makvandi M, Khalafkhany D, Rasti M, Neisi N, Omidvarinia A, Mirghaed AT, et al. Detection of hepatitis C virus RNA in peripheral blood mononuclear cells of patients with abnormal alanine transaminase in Ahvaz. Indian J Med Microbiol 2014;32:251-255.
22. Ohno O, Mizokami M, Wu RR, Saleh MG, Ohba K, Orito E, et al. New hepatitis C virus (HCV) genotyping system that allows for identification of HCV genotypes 1a, 1b, 2a, 2b, 3a, 3b, 4, 5a, and 6a. J Clin Microbiol 1997;35:201-207.
23. Greca LF, Pinto L, Rados DR, Canani LH, Gross JL. Clinical features of patients with type 2 diabetes mellitus and hepatitis C infection. Braz J Med Biol Res 2012;45:284-290.
24. Nwokediuko SC, Oli JM. Hepatitis C virus infection in Nigerians with diabetes mellitus. Niger J Clin Pract 2008;11:94-99.
25. Naing C, Mak JW, Ahmed SI, Maung M. Relationship between hepatitis C virus infection and type 2 diabetes mellitus: meta-analysis. World J Gastroenterol 2012;18:1642-1651.
26. Memon MS, Arain ZI, Naz F, Zaki M, Kumar S, Burney AA. Prevalence of type 2 diabetes mellitus in hepatitis C virus infected population: a Southeast Asian study. J Diabetes Res 2013;2013:539361.
27. Mirminachi B, Mohammadi Z, Merat S, Neishabouri A, Sharifi AH, Alavian SH, et al. Update on the prevalence of hepatitis C virus infection among Iranian general population: a systematic review and meta-analysis. Hepat Mon 2017;17(2):e42291.
28. Ali S, Abera S, Mihret A, Abebe T. Association of hepatitis C virus infection with type II diabetes in Ethiopia: a hospital-based case-control study. Interdiscip Perspect Infect Dis 2012;2012:354656.
29. Mehta SH, Brancati FL, Sulkowski MS, Strathdee SA, Szklo M, Thomas DL. Prevalence of type 2 diabetes mellitus among persons with hepatitis C virus infection in the United States. Ann Intern Med 2000;133:592-599.
30. Ndako JA, Echeonwu GO, Shidali NN, Bichi IA, Paul GA, Onovoh E, et al. Occurrence of hepatitis C virus infection in type 2 diabetic patients attending plateau state specialist hospital Jos Nigeria. Virol J 2009;6:98.
31. Wang CS, Wang ST, Yao WJ, Chang TT, Chou P. Community-based study of hepatitis C virus infection and type 2 diabetes: an association affected by age and hepatitis severity status. Am J Epidemiol 2003;158:1154-1160.
32. Fukui M, Kitagawa Y, Nakamura N, Yoshikawa T. Hepatitis C virus and atherosclerosis in patients with type 2 diabetes. JAMA 2003;289:1245-1246.
33. Qureshi H, Ahsan T, Mujeeb SA, Jawad F, Mehdi I, Ahmed W, et al. Diabetes mellitus is equally frequent in chronic HCV and HBV infection. J Pak Med Assoc 2002;52:280-283.
34. Sangiorgio L, Attardo T, Gangemi R, Rubino C, Barone M, Lunetta M. Increased frequency of HCV and HBV infection in type 2 diabetic patients. Diabetes Res Clin Pract 2000;48:147-151.
35. Ndako JA, Owolabi AO, Olisa JA, Akinwumi JA, Dojumo VT, Olatinsu O, et al. Studies on the prevalence of hepatitis C virus infection in diabetic patients attending a tertiary health-care facility South-West Nigeria. BMC Infect Dis 2020;20:664.
36. Chen HF, Li CY, Chen P, See TT, Lee HY. Seroprevalence of hepatitis B and C in type 2 diabetic patients. J Chin Med Assoc 2006;69:146-152.
37. Howard AA, Klein RS, Schoenbaum EE. Association of hepatitis C infection and antiretroviral use with diabetes mellitus in drug users. Clin Infect Dis 2003;36:1318-1323.
38. Balogun WO, Adeleye JO, Akinlade KS, Kuti M, Otegbayo JA. Low prevalence of hepatitis-C viral seropositivity among patients with type-2 diabetes mellitus in a tertiary hospital. J Natl Med Assoc 2006;98:1805-1808.
39. Costa LM, Mussi AD, Brianeze MR, Souto FJ. Hepatitis C as a risk factor for diabetes type 2: lack of evidence in a hospital in central-west Brazil. Braz J Infect Dis 2008;12:24-26.
40. Gulcan A, Gulcan E, Toker A, Bulut I, Akcan Y. Evaluation of risk factors and seroprevalence of hepatitis B and C in diabetic patients in Kutahya, Turkey. J Investig Med 2008;56:858-863.
41. Triantos C, Konstantakis C, Tselekouni P, Kalafateli M, Aggeletopoulou I, Manolakopoulos S. Epidemiology of hepatitis C in Greece. World J Gastroenterol 2016;22:8094-8102.
42. Chiquete E, Ochoa-Guzmán A, García-Lamas L, Anaya-Gómez F, Gutiérrez-Manjarrez JI, Sánchez-Orozco LV, et al. Hepatitis C virus infection and type 2 diabetes mellitus in Mexican patients. Rev Med Inst Mex Seguro Soc 2012;50:481-486.
43. Shaheen M, Echeverry D, Oblad MG, Montoya MI, Teklehaimanot S, Akhtar AJ. Hepatitis C, metabolic syndrome, and inflammatory markers: results from the Third National Health and Nutrition Examination Survey [NHANES III]. Diabetes Res Clin Pract 2007;75:320-326.
44. Saxena AK, Suresh RB. An intriguing relationship between type 2 diabetes mellitus and hepatitis C virus infection: the renal perspective. Hepat Mon 2009;9:89-91.
45. Miyamoto H, Moriishi K, Moriya K, Murata S, Tanaka K, Suzuki T, et al. Involvement of the PA28gamma-dependent pathway in insulin resistance induced by hepatitis C virus core protein. J Virol 2007;81:1727-1735.
46. Aytug S, Reich D, Sapiro LE, Bernstein D, Begum N. Impaired IRS‐1/PI3‐kinase signaling in patients with HCV: a mechanism for increased prevalence of type 2 diabetes. Hepatology 2003;38:1384-1392.
47. Heppner DS, Harrison SA. Obesity, insulin resistance, and HCV: implications for pathogenesis. Curr Hepat Rep 2005;4:153-157.
48. Negro F, Alaei M. Hepatitis C virus and type 2 diabetes. World J Gastroenterol 2009;15:1537-1547.
49. Serfaty L, Capeau J. Hepatitis C, insulin resistance and diabetes: clinical and pathogenic data. Liver Int 2009;29 Suppl 2:13-25.
IssueVol 13 No 5 (2021) QRcode
SectionOriginal Article(s)
DOI https://doi.org/10.18502/ijm.v13i5.7437
Diabetes mellitus type 2; HCV; Prevalence;

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
Makvandi M, Azaran A, Jalilian S, Parsa Nahad M, Azizolahi B, Neisi N. Frequency and genotype distribution of hepatitis C virus infection in patients with diabetes type 2 in Ahvaz, Iran. Iran J Microbiol. 2021;13(5):703-711.