Risk of Hepatitis C Virus Infection in Tuberculosis Patients: A Systematic Review and Meta-Analysis
Abstract
Background: Tuberculosis (TB) and infection of Hepatitis C virus (HCV) have appeared as major public health problems. The present systematic review and meta-analysis aimed at determining the relationship between TB and the risk of HCV infection.
Methods: Google Scholar, Embase, Medline, Pubmed, web of sciences (ISI), and Scopus were searched until March 2022. The pooled ORs of HCV in patients with TB were calculated utilizing the random-effect model with a 95% confidence interval (CI). test was utilized for evaluating the heterogeneity. To check publication bias Egger and Beggs' tests were used.
Results: From among 1500 articles from 2006 to 2020, 13 studies were examined and analyzed based on the inclusion/exclusion criteria. The overall risk of HCV infection in patients with TB was (OR: 1.34, 95% CI: 1.10-1.63, P=0.001). According to the type of the countries subgroup analysis, the risk of HCV infection in patients with TB in developing countries was (OR: 1.95, 95% CI: 1.00-3.80), which was higher than the risk in developed countries (OR: 1.47, 95% CI: 1.42-1.52). In addition, the risk of hepatitis C infection in men compared to women (OR: 1.84, 95% CI: 1.75-1.94, P=0.001) and in age groups over 65 yr compared to other age groups (OR: 1.46, 95% CI: 0.98-2.16) was significantly higher.
Conclusion: The results of this study emphasized the importance of screening HCV in patients with TB. Being aware of the presence or absence of HCV in these patients can contribute to their effective treatment.
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2. Rokni M, Massoud J, Hanilo A (2003). Comparison of adult somatic and cysteine proteinase antigens of Fasciola gigantica in enzyme linked immunosorbent assay for serodiagnosis of human fasciolosis. Acta Trop, 88 (1):69-75.
3. World Health Organization(2020). Global tuberculosis report. Available from: https://www.who.int/publications/i/item/9789240037021
4. Agha MA, El-Mahalawy II, Seleem HM, Helwa MA (2015). Prevalence of hepatitis C virus in patients with tuberculosis and its impact in the incidence of anti-tuberculosis drugs induced hepatotoxicity. Egypt J Chest DisTuberc, 64(1):91-96.
5. Feleke BE, Feleke TE, Adane WG, Girma A (2020). Impacts of hepatitis B and hepatitis C co-infection with tuberculosis, a prospective cohort study. Virol J, 17:113.
6. Nooredinvand HA, Connell DW, Asgheddi M, et al (2015). Viral hepatitis prevalence in patients with active and latent tuberculosis. World J Gastroenterol, 21 (29):8920-26.
7. Woldegiorgis AE, Erku W, Medhin G, Berhe N, Legesse M (2019). Community-based sero-prevalence of hepatitis B and C infections in South Omo Zone, Southern Ethiopia. PloS One, 14 (12):e0226890.
8. Araújo‐Mariz C, Lopes EP, Ximenes RA, et al (2016). Serological markers of hepatitis B and C in patients with HIV/AIDS and active tuberculosis .J Med Virol, 88 (6):996-1002.
9. Bushnell G, Stennis N, Drobnik A, et al(2015) . Characteristics and TB treatment outcomes in TB patients with viral hepatitis, New York City, 2000–2010. Epidemiol Infect, 143 (9):1972-1981.
10. El Hamdouni M, Ahid S, Bourkadi JE, Benamor J, Hassar M, Cherrah Y (2020). Incidence of adverse reactions caused by first-line anti-tuberculosis drugs and treatment outcome of pulmonary tuberculosis patients in Morocco. Infection, 48 (1):43-50.
11. de Oliveira Uehara SN, Emori CT, Perez RM, et al (2016). High incidence of tuberculosis in patients treated for hepatitis C chronic infection. Braz J Infect Dis, 20 (2):205-209.
12. Torres J, Aguado JM, San Juan R, et al (2008). Hepatitis C virus, an important risk factor for tuberculosis in immunocompromised: experience with kidney transplantation. Transpl Int, 21 (9):873-878.
13. Awofeso N (2010). Prisons as social determinants of hepatitis C virus and tuberculosis infections. Public Health Reports, 125 (4_suppl):25-33.
14. Reis N, Lopes C, Teles SA, et al (2011). Hepatitis C virus infection in patients with tuberculosis in Central Brazil. Int J Tuberc Lung Dis, 15 (10):1397-1402.
15. Wu PH, Lin YT, Hsieh KP, Chuang HY, Sheu CC (2015). Hepatitis C virus infection is associated with an increased risk of active tuberculosis disease: a nationwide population-based study. Medicine, 94(33):e1328.
16. Page MJ, McKenzie JE, Bossuyt PM, et al (2021). Updating guidance for reporting systematic reviews: development of the PRISMA 2020 statement. J Clin Epidemiol, 134:103-112.
17. Stang A (2010). Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol,. 25(9):603-5
18. Bae J-M (2016). A suggestion for quality assessment in systematic reviews of observational studies in nutritional epidemiology. Epidemiol Health, 38. e2016014.
19. Kim WS, Lee SS, Lee CM, et al (2016). Hepatitis C and not Hepatitis B virus is a risk factor for anti-tuberculosis drug induced liver injury. BMC Infect.Dis, 16:50.
20. Chien J, Huang R, Wang J, et al (2010). Hepatitis C virus infection increases hepatitis risk during anti-tuberculosis treatment. Int J Tuberc Lung Dis, 14 (5):616-621.
21. Campo M, Shrestha A, Oren E, et al (2014). Characterization of hepatitis C infection in tuberculosis patients in an urban city in the USA. Epidemiol Infect, 142 (7):1459-1466.
22. Richards D, Mikiashvili T, Parris J, et al (2006). High prevalence of hepatitis C virus but not HIV co-infection among patients with tuberculosis in Georgia. Int J Tuberc Lung Dis, 10 (4):396-401.
23. Khalili H, Dashti Ks, Rasoulinezhad M, Rezaei L, Etminani M (2009). Anti-tuberculosis drugs related hepatotoxicity; incidence, risk factors, pattern of changes in liver enzymes and outcome. https://www.sid.ir/paper/275509/en
24. Aung A (2018). Hepatitis C and Risk of Adverse Treatment Outcomes among Patients with HIV and Multidrug-resistant Tuberculosis Georgia State University. https://scholarworks.gsu.edu/cgi/viewcontent.cgi?article=1660&context=iph_theses
25. Lin SY, Chen TC, Lu PL, et al (2014). Incidence rates of tuberculosis in chronic hepatitis C infected patients with or without interferon based therapy: a population-based cohort study in Taiwan. BMC Infect Dis, 14 (1):1-8.
26. El-Serag HB, Anand B, Richardson P, Rabeneck L (2003). Association between hepatitis C infection and other infectious diseases: a case for targeted screening? Am J Gastroenterol, 98 (1):167-174.
27. Baliashvili D, Blumberg HM, Benkeser D, et al (2023). Association of treated and untreated chronic hepatitis C with the incidence of active tuberculosis disease: a population-based cohort study.
Clin Infect Dis, 76(2): 245-251.
28. Sirinak C, Kittikraisak W, Pinjeesekikul D, et al (2008). Viral hepatitis and HIV-associated tuberculosis: risk factors and TB treatment outcomes in Thailand. BMC Public Health, 8 (1):1-10.
29. Akhtar JAJ, Qamar MU, Sarwar AHAWF, Anwar J (2013). Sero-prevalence of HBV and HCV in tuberculous patients at Sheikh Zayed hospital Rahim Yar khan, Pakistan. Acta Biomed, 29 (2):69-72.
30. Badawy M, Taha M, Mohamed L, Fathy A (2011). Hepatitis C virus infection among tuberculosis patients in Sohag Governorate: Seroprevalence and associated risk factors. Eur Respiratory Soc. https://channel.ersnet.org/media-58388-hepatitis-c-virus-infection-among-tuberculosis-patients-in-sohag-governorate-seroprevalence-and-associated-risk-factors
31. Ungo JR, Jones D, Ashkin D, et al (1998). Antituberculosis drug–induced hepatotoxicity: the role of hepatitis C virus and the human immunodeficiency virus. Am J Respir Crit Care Med, 157 (6):1871-1876.
32. Kwon YS, Koh WJ, Suh GY, et al (2007). Hepatitis C virus infection and hepatotoxicity during antituberculosis chemotherapy. Chest, 131 (3):803-808.
33. Sharma SK, Balamurugan A, Saha PK, Pandey RM, Mehra NK (2002). Evaluation of clinical and immunogenetic risk factors for the development of hepatotoxicity during antituberculosis treatment. Am J Respir Crit Care Med, 166 (7):916-919.
34. Saukkonen JJ, Cohn DL, Jasmer RM, et al (2006). An official ATS statement: hepatotoxicity of antituberculosis therapy. Am J Respir Crit Care Med, 174 (8):935-952.
35. Lee BH, Koh W-J, Choi MS, et al (2005). Inactive hepatitis B surface antigen carrier state and hepatotoxicity during antituberculosis chemotherapy. Chest, 127 (4):1304-1311.
36. Wong WM, Wu PC, Yuen MF, et al (2000). Antituberculosis drug‐related liver dysfunction in chronic hepatitis B infection. Hepatology, 31 (1):201-206.
37. Hwang SJ, Wu JC, Lee CN, et al (1997). A prospective clinical study of isoniazid‐rifampicin‐pyrazinamide‐induced liver injury in an area endemic for hepatitis B. J Gastroenterol Hepatol, 12 (1):87-91.
38. Yew WW, Leung CC (2006). Antituberculosis drugs and hepatotoxicity. Respirology, 11 (6):699-707.
39. Ramappa V, Aithal GP (2013). Hepatotoxicity related to anti-tuberculosis drugs: mechanisms and management. J Clin Exp Hepatol, 3 (1):37-49.
40. Mohamed AA, Elbedewy TA, El-Serafy M, El-Toukhy N, Ahmed W, El Din ZA (2015). Hepatitis C virus: A global view. World J Hepatol, 7 (26):2676.-80
41. McGowan CE, Monis A, Bacon BR, et al (2013). A global view of hepatitis C: physician knowledge, opinions, and perceived barriers to care. Hepatology, 57 (4):1325-1332.
42. Hagan LM, Schinazi RF (2013). Best strategies for global HCV eradication. Liver International, 33:68-79.
43. Lawal MA, Adeniyi OF, Akintan PE, Salako AO, Omotosho OS, Temiye EO (2020). Prevalence of and risk factors for hepatitis B and C viral co-infections in HIV infected children in Lagos, Nigeria. PloS One, 15 (12):e0243656.
44. Jadoul M, Bieber BA, Martin P, et al (2019). Prevalence, incidence, and risk factors for hepatitis C virus infection in hemodialysis patients. Kidney Int, 95 (4):939-947.
2. Rokni M, Massoud J, Hanilo A (2003). Comparison of adult somatic and cysteine proteinase antigens of Fasciola gigantica in enzyme linked immunosorbent assay for serodiagnosis of human fasciolosis. Acta Trop, 88 (1):69-75.
3. World Health Organization(2020). Global tuberculosis report. Available from: https://www.who.int/publications/i/item/9789240037021
4. Agha MA, El-Mahalawy II, Seleem HM, Helwa MA (2015). Prevalence of hepatitis C virus in patients with tuberculosis and its impact in the incidence of anti-tuberculosis drugs induced hepatotoxicity. Egypt J Chest DisTuberc, 64(1):91-96.
5. Feleke BE, Feleke TE, Adane WG, Girma A (2020). Impacts of hepatitis B and hepatitis C co-infection with tuberculosis, a prospective cohort study. Virol J, 17:113.
6. Nooredinvand HA, Connell DW, Asgheddi M, et al (2015). Viral hepatitis prevalence in patients with active and latent tuberculosis. World J Gastroenterol, 21 (29):8920-26.
7. Woldegiorgis AE, Erku W, Medhin G, Berhe N, Legesse M (2019). Community-based sero-prevalence of hepatitis B and C infections in South Omo Zone, Southern Ethiopia. PloS One, 14 (12):e0226890.
8. Araújo‐Mariz C, Lopes EP, Ximenes RA, et al (2016). Serological markers of hepatitis B and C in patients with HIV/AIDS and active tuberculosis .J Med Virol, 88 (6):996-1002.
9. Bushnell G, Stennis N, Drobnik A, et al(2015) . Characteristics and TB treatment outcomes in TB patients with viral hepatitis, New York City, 2000–2010. Epidemiol Infect, 143 (9):1972-1981.
10. El Hamdouni M, Ahid S, Bourkadi JE, Benamor J, Hassar M, Cherrah Y (2020). Incidence of adverse reactions caused by first-line anti-tuberculosis drugs and treatment outcome of pulmonary tuberculosis patients in Morocco. Infection, 48 (1):43-50.
11. de Oliveira Uehara SN, Emori CT, Perez RM, et al (2016). High incidence of tuberculosis in patients treated for hepatitis C chronic infection. Braz J Infect Dis, 20 (2):205-209.
12. Torres J, Aguado JM, San Juan R, et al (2008). Hepatitis C virus, an important risk factor for tuberculosis in immunocompromised: experience with kidney transplantation. Transpl Int, 21 (9):873-878.
13. Awofeso N (2010). Prisons as social determinants of hepatitis C virus and tuberculosis infections. Public Health Reports, 125 (4_suppl):25-33.
14. Reis N, Lopes C, Teles SA, et al (2011). Hepatitis C virus infection in patients with tuberculosis in Central Brazil. Int J Tuberc Lung Dis, 15 (10):1397-1402.
15. Wu PH, Lin YT, Hsieh KP, Chuang HY, Sheu CC (2015). Hepatitis C virus infection is associated with an increased risk of active tuberculosis disease: a nationwide population-based study. Medicine, 94(33):e1328.
16. Page MJ, McKenzie JE, Bossuyt PM, et al (2021). Updating guidance for reporting systematic reviews: development of the PRISMA 2020 statement. J Clin Epidemiol, 134:103-112.
17. Stang A (2010). Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol,. 25(9):603-5
18. Bae J-M (2016). A suggestion for quality assessment in systematic reviews of observational studies in nutritional epidemiology. Epidemiol Health, 38. e2016014.
19. Kim WS, Lee SS, Lee CM, et al (2016). Hepatitis C and not Hepatitis B virus is a risk factor for anti-tuberculosis drug induced liver injury. BMC Infect.Dis, 16:50.
20. Chien J, Huang R, Wang J, et al (2010). Hepatitis C virus infection increases hepatitis risk during anti-tuberculosis treatment. Int J Tuberc Lung Dis, 14 (5):616-621.
21. Campo M, Shrestha A, Oren E, et al (2014). Characterization of hepatitis C infection in tuberculosis patients in an urban city in the USA. Epidemiol Infect, 142 (7):1459-1466.
22. Richards D, Mikiashvili T, Parris J, et al (2006). High prevalence of hepatitis C virus but not HIV co-infection among patients with tuberculosis in Georgia. Int J Tuberc Lung Dis, 10 (4):396-401.
23. Khalili H, Dashti Ks, Rasoulinezhad M, Rezaei L, Etminani M (2009). Anti-tuberculosis drugs related hepatotoxicity; incidence, risk factors, pattern of changes in liver enzymes and outcome. https://www.sid.ir/paper/275509/en
24. Aung A (2018). Hepatitis C and Risk of Adverse Treatment Outcomes among Patients with HIV and Multidrug-resistant Tuberculosis Georgia State University. https://scholarworks.gsu.edu/cgi/viewcontent.cgi?article=1660&context=iph_theses
25. Lin SY, Chen TC, Lu PL, et al (2014). Incidence rates of tuberculosis in chronic hepatitis C infected patients with or without interferon based therapy: a population-based cohort study in Taiwan. BMC Infect Dis, 14 (1):1-8.
26. El-Serag HB, Anand B, Richardson P, Rabeneck L (2003). Association between hepatitis C infection and other infectious diseases: a case for targeted screening? Am J Gastroenterol, 98 (1):167-174.
27. Baliashvili D, Blumberg HM, Benkeser D, et al (2023). Association of treated and untreated chronic hepatitis C with the incidence of active tuberculosis disease: a population-based cohort study.
Clin Infect Dis, 76(2): 245-251.
28. Sirinak C, Kittikraisak W, Pinjeesekikul D, et al (2008). Viral hepatitis and HIV-associated tuberculosis: risk factors and TB treatment outcomes in Thailand. BMC Public Health, 8 (1):1-10.
29. Akhtar JAJ, Qamar MU, Sarwar AHAWF, Anwar J (2013). Sero-prevalence of HBV and HCV in tuberculous patients at Sheikh Zayed hospital Rahim Yar khan, Pakistan. Acta Biomed, 29 (2):69-72.
30. Badawy M, Taha M, Mohamed L, Fathy A (2011). Hepatitis C virus infection among tuberculosis patients in Sohag Governorate: Seroprevalence and associated risk factors. Eur Respiratory Soc. https://channel.ersnet.org/media-58388-hepatitis-c-virus-infection-among-tuberculosis-patients-in-sohag-governorate-seroprevalence-and-associated-risk-factors
31. Ungo JR, Jones D, Ashkin D, et al (1998). Antituberculosis drug–induced hepatotoxicity: the role of hepatitis C virus and the human immunodeficiency virus. Am J Respir Crit Care Med, 157 (6):1871-1876.
32. Kwon YS, Koh WJ, Suh GY, et al (2007). Hepatitis C virus infection and hepatotoxicity during antituberculosis chemotherapy. Chest, 131 (3):803-808.
33. Sharma SK, Balamurugan A, Saha PK, Pandey RM, Mehra NK (2002). Evaluation of clinical and immunogenetic risk factors for the development of hepatotoxicity during antituberculosis treatment. Am J Respir Crit Care Med, 166 (7):916-919.
34. Saukkonen JJ, Cohn DL, Jasmer RM, et al (2006). An official ATS statement: hepatotoxicity of antituberculosis therapy. Am J Respir Crit Care Med, 174 (8):935-952.
35. Lee BH, Koh W-J, Choi MS, et al (2005). Inactive hepatitis B surface antigen carrier state and hepatotoxicity during antituberculosis chemotherapy. Chest, 127 (4):1304-1311.
36. Wong WM, Wu PC, Yuen MF, et al (2000). Antituberculosis drug‐related liver dysfunction in chronic hepatitis B infection. Hepatology, 31 (1):201-206.
37. Hwang SJ, Wu JC, Lee CN, et al (1997). A prospective clinical study of isoniazid‐rifampicin‐pyrazinamide‐induced liver injury in an area endemic for hepatitis B. J Gastroenterol Hepatol, 12 (1):87-91.
38. Yew WW, Leung CC (2006). Antituberculosis drugs and hepatotoxicity. Respirology, 11 (6):699-707.
39. Ramappa V, Aithal GP (2013). Hepatotoxicity related to anti-tuberculosis drugs: mechanisms and management. J Clin Exp Hepatol, 3 (1):37-49.
40. Mohamed AA, Elbedewy TA, El-Serafy M, El-Toukhy N, Ahmed W, El Din ZA (2015). Hepatitis C virus: A global view. World J Hepatol, 7 (26):2676.-80
41. McGowan CE, Monis A, Bacon BR, et al (2013). A global view of hepatitis C: physician knowledge, opinions, and perceived barriers to care. Hepatology, 57 (4):1325-1332.
42. Hagan LM, Schinazi RF (2013). Best strategies for global HCV eradication. Liver International, 33:68-79.
43. Lawal MA, Adeniyi OF, Akintan PE, Salako AO, Omotosho OS, Temiye EO (2020). Prevalence of and risk factors for hepatitis B and C viral co-infections in HIV infected children in Lagos, Nigeria. PloS One, 15 (12):e0243656.
44. Jadoul M, Bieber BA, Martin P, et al (2019). Prevalence, incidence, and risk factors for hepatitis C virus infection in hemodialysis patients. Kidney Int, 95 (4):939-947.
| Files | ||
| Issue | Vol 53 No 11 (2024) | |
| Section | Review Article(s) | |
| Keywords | ||
| Hepatitis C virus Systematic review Meta-analysis Tuberculosis | ||
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How to Cite
1.
Amoori N, Cheraghian B, Amini P, Alavi SM. Risk of Hepatitis C Virus Infection in Tuberculosis Patients: A Systematic Review and Meta-Analysis. Iran J Public Health. 2024;53(11):2451-2461.
