Frequency and genotype distribution of hepatitis C virus infection in patients with diabetes type 2 in Ahvaz, Iran
-
Manoochehr Makvandi
,
Azarakhsh Azaran
,
Shahram Jalilian
,
Mehdi Parsa Nahad
,
Behnam Azizolahi
,
Niloofar Neisi
Abstract
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.
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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.
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.
| Files | ||
| Issue | Vol 13 No 5 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v13i5.7437 | |
| Keywords | ||
| Diabetes mellitus type 2; HCV; Prevalence; | ||
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How to Cite
1.
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.
