Hepatitis C in Tunisia from 1991 to 2019: A systematic review

##plugins.themes.academic_pro.article.main##

Marwa Khedhiri
Hatem Triki
Henda Triki

Abstract

Background: Hepatitis C virus (HCV) is one of the leading causes of chronic liver disease and liver cancer related deaths in Tunisia.
Aim: Perform a systematic review on viral hepatitis C in Tunisia between 1991 and 2019.
Methods: A global search of HCV-specific documentation in Tunisia (1991-2019) in bibliographic data search sites.
Results: Tunisia is a low endemic country for hepatitis C with a prevalence that not exceed 1% in the general population. Several studies have focused on populations at risk of HCV contamination such as hemodialysis and polytransfused patients. The prevalence of hepatitis C is higher in these groups. In relatively small series, a clear predominance of genotype 1 and subtype 1b has been reported in Tunisia with a lower co-circulation of the other genotypes.
Several polymorphisms of cytokine and chemokine genes can influence the clearance or persistence of HCV infection. Tunisian studies have focused on the efficacy of conventional dual therapy (pegylated IFN + ribavirin) by analyzing the predictive factors linked to SVR and mutations associated with resistance to viral inhibitors. No publication has discussed the effectiveness of new direct-acting antivirals in Tunisia.
Conclusion: This review of the literature provides an update on the status of hepatitis C in Tunisia and reveals a lack of investigations on new direct-acting antivirals.

Keywords:

Hepatitis C, Tunisia, prevalence, genotypes, population at risk, therapy

##plugins.themes.academic_pro.article.details##

References

  1. Références 1. Mahmud S, Al-Kanaani Z, Chemaitelly H, Chaabna K, Kouyoumjian SP, Abu-Raddad LJ. Hepatitis C virus genotypes in the Middle East and North Africa: Distribution, diversity, and patterns. J Med Virol 2018; 90(1):131‑41. 2. Gorgi Y, Yalaoui S, Ben Nejma HL, Azzouz MM, Hsairi M, Ben Khelifa H, et al. [Detection of hepatitis C virus in the general population of Tunisia]. Bull Soc Pathol Exot 1990. 1998;91(2):177. 3. Mejri S, Salah AB, Triki H, Alaya NB, Djebbi A, Dellagi K. Contrasting patterns of hepatitis C virus infection in two regions from Tunisia. J Med Virol 2005;76(2):185‑93. 4. Bettaieb J, Chouikha A, Khedhiri M, Kharroubi G, Badreddine M, Bel Hadj Hmida N, et al. Hepatitis C virus epidemiology in Central-West Tunisia: a population-based cross-sectional study. Arch Virol 2019; 164(9):2243‑53. 5. Triki H, Said N, Ben Salah A, Arrouji A, Ben Ahmed F, Bouguerra A, et al. Seroepidemiology of hepatitis B, C and delta viruses in Tunisia. Trans R Soc Trop Med Hyg 1997; 91(1):11‑4. 6. Bizid S, Ben Sassi S, Ben Abdallah H, Doghri A, Tounsi C, Bouali R, et al. Screening for viral hepatitis C in a young Tunisian population (more than 175,000 recruits). Tunis Med 2015;93(12):742‑5. 7. Jemni S, Ikbel K, Kortas M, Mahjoub J, Ghachem L, Bidet JM, et al. Seropositivity to hepatitis C virus in Tunisian haemodialysis patients. Nouv Rev Fr Hematol 1994;36(5):349‑51. 8. Hachicha J, Hammami A, Masmoudi H, Ben Hmida M, Karray H, Kharrat M, et al. [Viral hepatitis C in chronic hemodialyzed patients in southern Tunisia. Prevalence and risk factors]. Ann Med Interne (Paris) 1995; 146(5):295‑8. 9. Sassi F, Gorgi Y, Ayed K, Abdallah TB, Lamouchi A, Maiz HB. Hepatitis C virus antibodies in dialysis patients in Tunisia: a single center study. Saudi J Kidney Dis Transplant Off Publ Saudi Cent Organ Transplant Saudi Arab 2000; 11(2):218‑22. 10. Ayed K, Gorgi Y, Ben Abdallah T, Aouadi H, Jendoubi-Ayed S, Sfar I, et al. Hepatitis C virus infection in hemodialysis patients from Tunisia: national survey by serologic and molecular methods. Transplant Proc 2003; 35(7):2573‑5. 11. Ben Othman S, Bouzgarrou N, Achour A, Bourlet T, Pozzetto B, Trabelsi A. [High prevalence and incidence of hepatitis C virus infections among dialysis patients in the East-Centre of Tunisia]. Pathol Biol (Paris) 2004; 52(6):323‑7. 12. Mhalla S, Hammoud R, Frih A, Kadri Y, El Argoubi A, Elmay M, et al. Prevalence and risk factors of hepatitis B and C among hemodialysis patients in Tunisia. Med Mal Infect 2018; 48(3):175‑9. 13. Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS, Pybus OG, et al. Global distribution and prevalence of hepatitis C virus genotypes. Hepatol Baltim Md 2015; 61(1):77‑87. 14. Fissell RB, Bragg-Gresham JL, Woods JD, Jadoul M, Gillespie B, Hedderwick SA, et al. Patterns of hepatitis C prevalence and seroconversion in hemodialysis units from three continents: the DOPPS. Kidney Int 2004; 65(6):2335‑42. 15. Kilani B, Ammari L, Marrakchi C, Letaief A, Chakroun M, Ben Jemaa M, et al. Seroepidemiology of HCV-HIV coinfection in Tunisia. Tunis Med 2007; 85(2):121‑3. 16. Maaref F, Kilani B, Ammari L, Ben Othman A, Zribi M, Fendri C, et al. [Prevalence of hepatitis G, B and C virus infections among positive HIV population in a Tunisian Hospital, La Rabta, Tunis]. Pathol Biol (Paris) 2011; 59(4):213‑6. 17. Kaabia N, Ben Jazia E, Hannachi N, Khalifa M, Dhouibi S, Dabbabi F, et al. [Prevalence of hepatitis C virus among health care workers in central Tunisia]. Med Mal Infect 2009; 39(1):66‑7. 18. Slama H, Mojaat N, Dahri R, Boukef K. [Epidemiologic study of anti-HCV antibodies in Tunisian blood donors]. Rev Francaise Transfus Hemobiologie Bull Soc Natl Transfus Sang 1991; 34(6):459‑64. 19. Abid S, Fkih S, Khlass B, Cherif W, Toumi NH, Jenhani F, et al. Dépistage et confirmation des anticorps anti-VHC chez les donneurs de sang tunisiens. Transfus Clin Biol 1997; 4(2):221‑6. 20. Hatira SA, Yacoub-Jemni S, Houissa B, Kaabi H, Zaeir M, Kortas M, et al. [Hepatitis C virus antibodies in 34130 blood donors in Tunisian Sahel]. Tunis Med 2000; 78(2):101‑5. 21. Ben Jemia R, Gouider E. Seroprevalency of transfusion-transmitted infections in first-time volunteer and replacement donors in Tunisia. Transfus Clin Biol J Soc Francaise Transfus Sang 2014; 21(6):303‑8. 22. Lakhoua Gorgi Y, Gorgi F, Madkouri G, Abderrahim E, Sfar I, Ramadani B, et al. [Hepatitis C in kidney transplantation: comparative study between two Maghrebin centers: Casablanca and Tunis]. Tunis Med 2010; 88(12):902‑9. 23. Kaabia N, Ben Jazia E, Slim I, Fodha I, Hachfi W, Gaha R, et al. Association of hepatitis C virus infection and diabetes in central Tunisia. World J Gastroenterol 2009; 15(22):2778‑81. 24. Souii A, Elargoubi A, Fallecker C, Mastouri M, Drouet E. Hepatitis C Genotype Prevalence in Monastir Region, Tunisia: Correlation between 5' Untranslated Region (5'UTR), Non-structural 5B (NS5B), and Core Sequences in HCV Subtyping. Curr Microbiol 2016; 73(3):324‑34. 25. Karray-Hakim H, Goudeau A, Fki-Berrajah L, Hammami A. [Epidemiology of hepatitis C virus infection and circulating genotypes in the Sfax region--Tunisia]. Tunis Med 1999; 77(3):139‑44. 26. Djebbi A, Mejri S, Thiers V, Triki H. Phylogenetic analysis of hepatitis C virus isolates from Tunisian patients. Eur J Epidemiol 2004; 19(6):555‑62. 27. Djebbi A, Triki H, Bahri O, Cheikh I, Sadraoui A, Ben Ammar A, et al. Genotypes of hepatitis C virus circulating in Tunisia. Epidemiol Infect 2003; 130(3):501‑5. 28. Hmaied F, Ben Mamou M, Saune-Sandres K, Rostaing L, Slim A, Arrouji Z, et al. Hepatitis C virus infection among dialysis patients in Tunisia: incidence and molecular evidence for nosocomial transmission. J Med Virol 2006; 78(2):185‑91. 29. Hmaïed F, Ben Mamou M, Dubois M, Pasquier C, Sandres-Saune K, Rostaing L, et al. Determining the source of nosocomial transmission in hemodialysis units in Tunisia by sequencing NS5B and E2 sequences of HCV. J Med Virol 2007; 79(8):1089‑94. 30. Ksiaa Cheikhrouhou L, Lakhoua-Gorgi Y, Sfar I, Jendoubi-Ayed S, Aouadi H, Makhlouf M, et al. Natural evolution of hepatitis C virus infection in hemodialysis Tunisian patients and CTLA-4 SNP's. World J Gastroenterol 2015; 21(35):10150‑8. 31. Othman SB, Trabelsi A, Monnet A, Bouzgarrou N, Grattard F, Beyou A, et al. Evaluation of a prototype HCV NS5b assay for typing strains of hepatitis C virus isolated from Tunisian haemodialysis patients. J Virol Methods 2004; 119(2):177‑81. 32. Kchouk FH, Gorgi Y, Bouslama L, Sfar I, Ayari R, Khiri H, et al. Phylogenetic analysis of isolated HCV strains from tunisian hemodialysis patients. Viral Immunol 2013; 26(1):40‑8. 33. Djebbi A, Bahri O, Langar H, Sadraoui A, Mejri S, Triki H. Genetic variability of genotype 1 hepatitis C virus isolates from Tunisian haemophiliacs. New Microbiol 2008; 31(4):473‑80. 34. Rajhi M, Mejri S, Djebbi A, Chouaieb S, Cheikh I, Ben Yahia A, et al. Subtyping genotype 2 hepatitis C viruses from Tunisia: identification of two putative new subtypes. Virus Genes 2014; 48(2):209‑17. 35. Rajhi M, Ghedira K, Chouikha A, Djebbi A, Cheikh I, Ben Yahia A, et al. Phylogenetic Analysis and Epidemic History of Hepatitis C Virus Genotype 2 in Tunisia, North Africa. PloS One 2016; 11(4):e0153761. 36. Mejri S, Mhalla S, Ben Yahia A, Triki H. [Molecular and phylogenetic analyses of Tunisian hepatitis C virus strains subtype 1b]. Ann Biol Clin (Paris) 2012; 70(6):707‑16. 37. Bouzgarrou N, Hassen E, Mahfoudh W, Gabbouj S, Schvoerer E, Ben Yahia A, et al. NS5A(ISDR-V3) region genetic variability of Tunisian HCV-1b strains: Correlation with the response to the combined interferon/ribavirin therapy. J Med Virol 2009; 81(12):2021‑8. 38. Aissa Larousse J, Trimoulet P, Recordon Pinson P, Tauzin B, Azzouz MM, Ben Mami N, et al. Prevalence of hepatitis C virus (HCV) variants resistant to NS5A inhibitors in naïve patients infected with HCV genotype 1 in Tunisia. Virol J 2015 ; 12:84. 39. Larousse JA, Trimoulet P, Recordonâ€Pinson P, Papuchon J, Azzouz MM, Mami NB, et al. Natural prevalence of hepatitis C virus (HCV) variants resistant to protease and polymerase inhibitors in patients infected with HCV genotype 1 in Tunisia. J Med Virol 2014; 86(8):1350‑9. 40. Khedhiri M, Ghedira K, Chouikha A, Touzi H, Sadraoui A, Hammemi W, et al. Tracing the epidemic history of hepatitis C virus genotype 1b in Tunisia and in the world, using a Bayesian coalescent approach. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis 2019; 75:103944. 41. Hmida S, Mojaat N, Chaouchi E, Mahjoub T, Khlass B, Abid S, et al. [HCV antibodies in hemodialyzed patients in Tunisia]. Pathol Biol (Paris) 1995; 43(7):581‑3. 42. Gorgi Y, Ayed K, Ben Abdallah T, Kammoun A, Ben Maïz H. HBV and HCV infection before and after kidney transplantation. Transplant Proc 2001; 33(5):2856‑7. 43. Ben Alaya Bouafif N, Triki H, Mejri S, Bahri O, Chlif S, Bettaib J, et al. A case control study to assess risk factors for hepatitis C among a general population in a highly endemic area of northwest Tunisia. Arch Inst Pasteur Tunis 2007; 84(1‑4):21‑7. 44. Belhadj N, Houissa F, Elloumi H, Ouakaa A, Gargouri D, Romani M, et al. Virological response of Tunisians patients treated by peginterferon plus ribavirin for chronic hepatitis C: a preliminary study. Tunis Med 2008; 86(4):341‑5. 45. Sghaier I, Mouelhi L, Gazouani E, Morel V, Besma YL, Brochot E. Roles of ITPA and IL28B genotypes in chronic Hepatitis C patients treated with peginterferon plus ribavirin in Tunisian population. J Clin Virol Off Publ Pan Am Soc Clin Virol 2015; 69:184‑9. 46. Bizid S, Bouali R, Ouedrani A, Mrabet A, Ben Abdallah H, Ghazouani E, et al. Genome-wide association of IL-28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C in a Tunisian population. Tunis Med 2016; 94(1):6‑11. 47. Sghaier I, Mouelhi L, Rabia NA, Ghazoueni E, Almawi WY, Loueslati BY. IL-10 and IL-28B gene variants as predictors of sustained response to peginterferon and ribavirin therapy in chronic HCV infection. Cytokine 2017; S1043-4666(17)30073-X. 48. Sghaier I, Mouelhi L, Ghazoueni E, Brochot E, Almawi WY, Yacoubi-Loueslati B. Role of TLRs and IL-6 in the outcome of chronic hepatitis C treatment in Tunisian population. Cytokine 2017; 99:297‑304. 49. Hamzaoui L, El Bouchtili S, Siai K, Mahmoudi M, Azzouz MM. Hepatitis B virus and hepatitis C virus co-infection: a therapeutic challenge. Clin Res Hepatol Gastroenterol 2013; 37(1):e16-20. 50. Elloumi H, Houissa F, Hadj NB, Gargouri D, Romani M, Kharrat J, et al. Sudden hearing loss associated with peginterferon and ribavirin combination therapy during hepatitis C treatment. World J Gastroenterol WJG 2007; 13(40):5411‑2. 51. World Health Organization (WHO) (2016) Combating hepatitis b and c to reach elimination by 2030.https://apps.who.int/iris/bitstream/handle/10665/206453/WHO_HIV_2016.04_eng.pdf/jsessionid=CADC5914BBC22D9F5FEBA9B2033892A3?sequence=1 52. Ksiaa Cheikhrouhou L, Sfar I, Aounallah-Skhiri H, Aouadi H, Jendoubi-Ayed S, Ben Abdallah T, et al. Cytokine and apoptosis gene polymorphisms influence the outcome of hepatitis C virus infection. Hepatobiliary Pancreat Dis Int HBPD INT 2011; 10(3):280‑8. 53. Ksiaa Cheikh Rouhou L, Gorgi YL, Skhiri HA, Aouadi H, Ayed SJ, Sfar I, et al. Chemokine and chemokine receptor gene polymorphism in Tunisian hemodialysis patients with HCV infection. Arab J Nephrol Transplant 2011; 4(3):117‑24. 54. Ksiaa L, Ayed-Jendoubi S, Sfar I, Gorgi Y, Najjar HAT, Abdallah TB, et al. Clearance and persistence of hepatitis C virus in a Tunisian population: association with HLA class I and class II. Viral Immunol 2007; 20(2):312‑9. 55. Bouzgarrou N, Hassen E, Schvoerer E, Stoll-Keller F, Bahri O, Gabbouj S, et al. Association of interleukin-18 polymorphisms and plasma level with the outcome of chronic HCV infection. J Med Virol 2008; 80(4):607‑14. 56. Bouzgarrou N, Hassen E, Gabbouj S, Schvoerer E, Ben Mami N, Triki H, et al. Lack of effect of tumor necrosis factor-alpha -308 G/A polymorphism on severity of liver fibrosis in Tunisian hepatitis C virus (HCV)-infected patients. Gastroenterol Clin Biol 2010; 34(4‑5):297‑304. 57. Bouzgarrou N, Hassen E, Bahri O, Gabbouj S, Mami NB, Triki H, et al. Combined effect of pro- and anti-inflammatory cytokine gene polymorphisms on susceptibility to liver cirrhosis in Tunisian HCV-infected patients. Hepatol Int 2011; 5(2):681‑7.