Towards hepatitis C virus elimination: Egyptian experience, achievements and limitations

Dalia Omran, Mohamed Alboraie, Rania A Zayed, Mohamed-Naguib Wifi, Mervat Naguib, Mohamed Eltabbakh, Mohamed Abdellah, Ahmed Fouad Sherief, Sahar Maklad, Heba Hamdy Eldemellawy, Omar Khalid Saad, Doaa Mohamed Khamiss, Mohamed El Kassas, Dalia Omran, Mohamed Alboraie, Rania A Zayed, Mohamed-Naguib Wifi, Mervat Naguib, Mohamed Eltabbakh, Mohamed Abdellah, Ahmed Fouad Sherief, Sahar Maklad, Heba Hamdy Eldemellawy, Omar Khalid Saad, Doaa Mohamed Khamiss, Mohamed El Kassas

Abstract

Worldwide, more than one million people die each year from hepatitis C virus (HCV) related diseases, and over 300 million people are chronically infected with hepatitis B or C. Egypt used to be on the top of the countries with heavy HCV burden. Some countries are making advances in elimination of HCV, yet multiple factors preventing progress; remain for the majority. These factors include lack of global funding sources for treatment, late diagnosis, poor data, and inadequate screening. Treatment of HCV in Egypt has become one of the top national priorities since 2007. Egypt started a national treatment program intending to provide cure for Egyptian HCV-infected patients. Mass HCV treatment program had started using Pegylated interferon and ribavirin between 2007 and 2014. Yet, with the development of highly-effective direct acting antivirals (DAAs) for HCV, elimination of viral hepatitis has become a real possibility. The Egyptian National Committee for the Control of Viral Hepatitis did its best to provide Egyptian HCV patients with DAAs. Egypt adopted a strategy that represents a model of care that could help other countries with high HCV prevalence rate in their battle against HCV. This review covers the effects of HCV management in Egyptian real life settings and the outcome of different treatment protocols. Also, it deals with the current and future strategies for HCV prevention and screening as well as the challenges facing HCV elimination and the prospect of future eradication of HCV.

Keywords: Direct acting antivirals; Egypt; Elimination; Hepatitis C virus; Limitations; Screening.

Conflict of interest statement

Conflict-of-interest statement: No potential conflicts of interest. No financial support.

Figures

Figure 1
Figure 1
Frequency distribution of different hepatitis C virus genotypes in Egypt.
Figure 2
Figure 2
Timeline of hepatitis C virus prevalence in Egypt among adults.
Figure 3
Figure 3
Management of hepatitis C virus patients in Egyptian viral hepatitis treatment centers. DAAs: Direct acting antivirals.

References

    1. World Health Organization (WHO) 2016. Hepatitis C Fact sheet. July.
    1. Simmonds P, Alberti A, Alter HJ, Bonino F, Bradley DW, Brechot C, Brouwer JT, Chan SW, Chayama K, Chen DS. A proposed system for the nomenclature of hepatitis C viral genotypes. Hepatology. 1994;19:1321–1324.
    1. Smith DB, Bukh J, Kuiken C, Muerhoff AS, Rice CM, Stapleton JT, Simmonds P. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource. Hepatology. 2014;59:318–327.
    1. Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS, Pybus OG, Barnes E. Global distribution and prevalence of hepatitis C virus genotypes. Hepatology. 2015;61:77–87.
    1. Polaris Observatory HCV Collaborators. Global prevalence and genotype distribution of hepatitis C virus infection in 2015: a modelling study. Lancet Gastroenterol Hepatol. 2017;2:161–176.
    1. Kouyoumjian SP, Chemaitelly H, Abu-Raddad LJ. Characterizing hepatitis C virus epidemiology in Egypt: systematic reviews, meta-analyses, and meta-regressions. Sci Rep. 2018;8:1661.
    1. Rao MR, Naficy AB, Darwish MA, Darwish NM, Schisterman E, Clemens JD, Edelman R. Further evidence for association of hepatitis C infection with parenteral schistosomiasis treatment in Egypt. BMC Infect Dis. 2002;2:29.
    1. Abdel-Aziz F, Habib M, Mohamed MK, Abdel-Hamid M, Gamil F, Madkour S, Mikhail NN, Thomas D, Fix AD, Strickland GT, et al. Hepatitis C virus (HCV) infection in a community in the Nile Delta: population description and HCV prevalence. Hepatology. 2000;32:111–115.
    1. El-Zanaty F, Way A. Egypt Demographic and Health Survey 2008. Egyptian: Ministry of Health. Cairo: El-Zanaty and Associates and Macro International;; 2009. p. 31. Available from: .
    1. Ministry of Health and Population/Egypt, El-Zanaty and Associates/Egypt, and ICF International. 2015. Egypt Health Issues Survey 2015. Cairo, Egypt: Ministry of Health and Population/EgyptandICFInternational. Available from: .
    1. Kandeel A, Genedy M, El-Refai S, Funk AL, Fontanet A, Talaat M. The prevalence of hepatitis C virus infection in Egypt 2015: implications for future policy on prevention and treatment. Liver Int. 2017;37:45–53.
    1. Esmat G. Hepatitis C in the Eastern Mediterranean Region. East Mediterr Health J. 2013;19:587–588.
    1. Alazawi W, Cunningham M, Dearden J, Foster GR. Systematic review: outcome of compensated cirrhosis due to chronic hepatitis C infection. Aliment Pharmacol Ther. 2010;32:344–355.
    1. World Bank Health Expenditure, Total (% of GDP) Available from: .
    1. Wedemeyer H, Duberg AS, Buti M, Rosenberg WM, Frankova S, Esmat G, Örmeci N, Van Vlierberghe H, Gschwantler M, Akarca U, et al. Strategies to manage hepatitis C virus (HCV) disease burden. J Viral Hepat. 2014;21 Suppl 1:60–89.
    1. Estes C, Abdel-Kareem M, Abdel-Razek W, Abdel-Sameea E, Abuzeid M, Gomaa A, Osman W, Razavi H, Zaghla H, Waked I. Economic burden of hepatitis C in Egypt: the future impact of highly effective therapies. Aliment Pharmacol Ther. 2015;42:696–706.
    1. El-Akel W, El-Sayed MH, El Kassas M, El-Serafy M, Khairy M, Elsaeed K, Kabil K, Hassany M, Shawky A, Yosry A, et al. National treatment programme of hepatitis C in Egypt: Hepatitis C virus model of care. J Viral Hepat. 2017;24:262–267.
    1. Doss W, Mohamed MK, Esmat G, El Sayed M, Fontanet A, Cooper S, El Sayed N. 2008. Egyptian National Control Strategy for Viral Hepatitis 2008-2012. Arab Republic of Egypt, Ministry of Health and Population, National Committee for the Control of Viral Hepatitis. Available from: .
    1. Esmat G, El Kassas M. 2017. The control of HCV in Egypt. Hepatitis B and C Public Policy Association Newsletter; pp. 4–5. Available from: .
    1. Gomaa A, Allam N, Elsharkawy A, El Kassas M, Waked I. Hepatitis C infection in Egypt: prevalence, impact and management strategies. Hepat Med. 2017;9:17–25.
    1. El Raziky M, Fathalah WF, El-Akel WA, Salama A, Esmat G, Mabrouk M, Salama RM, Khatab HM. The Effect of Peginterferon Alpha-2a vs. Peginterferon Alpha-2b in Treatment of Naive Chronic HCV Genotype-4 Patients: A Single Centre Egyptian Study. Hepat Mon. 2013;13:e10069.
    1. Ruane PJ, Ain D, Stryker R, Meshrekey R, Soliman M, Wolfe PR, Riad J, Mikhail S, Kersey K, Jiang D, et al. Sofosbuvir plus ribavirin for the treatment of chronic genotype 4 hepatitis C virus infection in patients of Egyptian ancestry. J Hepatol. 2015;62:1040–1046.
    1. Doss W, Shiha G, Hassany M, Soliman R, Fouad R, Khairy M, Samir W, Hammad R, Kersey K, Jiang D, et al. Sofosbuvir plus ribavirin for treating Egyptian patients with hepatitis C genotype 4. J Hepatol. 2015;63:581–585.
    1. Elsharkawy A, Fouad R, El Akel W, El Raziky M, Hassany M, Shiha G, Said M, Motawea I, El Demerdash T, Seif S, et al. Sofosbuvir-based treatment regimens: real life results of 14 409 chronic HCV genotype 4 patients in Egypt. Aliment Pharmacol Ther. 2017;45:681–687.
    1. El Kassas M, Alboraie M, Omran D, Salaheldin M, Wifi MN, ElBadry M, El Tahan A, Ezzat S, Moaz E, Farid AM, et al. An account of the real-life hepatitis C management in a single specialized viral hepatitis treatment centre in Egypt: results of treating 7042 patients with 7 different direct acting antiviral regimens. Expert Rev Gastroenterol Hepatol. 2018 Epub ahead of print.
    1. Ahmed OA, Elsebaey MA, Fouad MHA, Elashry H, Elshafie AI, Elhadidy AA, Esheba NE, Elnaggar MH, Soliman S, Abd-Elsalam S. Outcomes and predictors of treatment response with sofosbuvir plus daclatasvir with or without ribavirin in Egyptian patients with genotype 4 hepatitis C virus infection. Infect Drug Resist. 2018;11:441–445.
    1. Abd-Elsalam S, Sharaf-Eldin M, Soliman S, Elfert A, Badawi R, Ahmad YK. Efficacy and safety of sofosbuvir plus ribavirin for treatment of cirrhotic patients with genotype 4 hepatitis C virus in real-life clinical practice. Arch Virol. 2018;163:51–56.
    1. El Kassas M, Omran D, Elsaeed K, Alboraie M, Elakel W, El Tahan A, Abd El Latif Y, Nabeel MM, Korany M, Ezzat S, et al. Spur-of-the-Moment Modification in National Treatment Policies Leads to a Surprising HCV Viral Suppression in All Treated Patients: Real-Life Egyptian Experience. J Interferon Cytokine Res. 2018;38:81–85.
    1. El-Khayat HR, Fouad YM, Maher M, El-Amin H, Muhammed H. Efficacy and safety of sofosbuvir plus simeprevir therapy in Egyptian patients with chronic hepatitis C: a real-world experience. Gut. 2017;66:2008–2012.
    1. Eletreby R, Elakel W, Said M, El Kassas M, Seif S, Elbaz T, El Raziky M, Abdel Rehim S, Zaky S, Fouad R, et al. Real life Egyptian experience of efficacy and safety of Simeprevir/Sofosbuvir therapy in 6211 chronic HCV genotype IV infected patients. Liver Int. 2017;37:534–541.
    1. Abdel-Moneim A, Aboud A, Abdel-Gabaar M, Zanaty MI, Ramadan M. Efficacy and safety of sofosbuvir plus daclatasvir with or without ribavirin: large real-life results of patients with chronic hepatitis C genotype 4. Hepatol Int. 2018 Epub ahead of print.
    1. El-Khayat H, Fouad Y, Mohamed HI, El-Amin H, Kamal EM, Maher M, Risk A. Sofosbuvir plus daclatasvir with or without ribavirin in 551 patients with hepatitis C-related cirrhosis, genotype 4. Aliment Pharmacol Ther. 2018;47:674–679.
    1. Mohamed MS, Hanafy AS, Bassiony MAA, Hussein S. Sofosbuvir and daclatasvir plus ribavirin treatment improve liver function parameters and clinical outcomes in Egyptian chronic hepatitis C patients. Eur J Gastroenterol Hepatol. 2017;29:1368–1372.
    1. Omar H, El Akel W, Elbaz T, El Kassas M, Elsaeed K, El Shazly H, Said M, Yousif M, Gomaa AA, Nasr A, et al. Generic daclatasvir plus sofosbuvir, with or without ribavirin, in treatment of chronic hepatitis C: real-world results from 18 378 patients in Egypt. Aliment Pharmacol Ther. 2018;47:421–431.
    1. El-Khayat HR, Kamal EM, El-Sayed MH, El-Shabrawi M, Ayoub H, RizK A, Maher M, El Sheemy RY, Fouad YM, Attia D. The effectiveness and safety of ledipasvir plus sofosbuvir in adolescents with chronic hepatitis C virus genotype 4 infection: a real-world experience. Aliment Pharmacol Ther. 2018;47:838–844.
    1. Elsharkawy A, El-Raziky M, El-Akel W, El-Saeed K, Eletreby R, Hassany M, El-Sayed MH, Kabil K, Ismail SA, El-Serafy M, et al. Planning and prioritizing direct-acting antivirals treatment for HCV patients in countries with limited resources: Lessons from the Egyptian experience. J Hepatol. 2017
    1. Attia D, El Saeed K, Elakel W, El Baz T, Omar A, Yosry A, Elsayed MH, Said M, El Raziky M, Anees M, et al. The adverse effects of interferon-free regimens in 149 816 chronic hepatitis C treated Egyptian patients. Aliment Pharmacol Ther. 2018;47:1296–1305.
    1. Wanis H, Hussein A, El Shibiny A, et al. 2014. HCV treatment in Egypt - why cost remains a challenge Egyptian initiative for personal rights; pp. 6–18. Available from: .
    1. Medhat A, Shehata M, Magder LS, Mikhail N, Abdel-Baki L, Nafeh M, Abdel-Hamid M, Strickland GT, Fix AD. Hepatitis c in a community in Upper Egypt: risk factors for infection. Am J Trop Med Hyg. 2002;66:633–638.
    1. Mostafa A, Taylor SM, el-Daly M, el-Hoseiny M, Bakr I, Arafa N, Thiers V, Rimlinger F, Abdel-Hamid M, Fontanet A, et al. Is the hepatitis C virus epidemic over in Egypt? Incidence and risk factors of new hepatitis C virus infections. Liver Int. 2010;30:560–566.
    1. Talaat M, Radwan E, El-Sayed N, Ismael T, Hajjeh R, Mahoney FJ. Case-control study to evaluate risk factors for acute hepatitis B virus infection in Egypt. East Mediterr Health J. 2010;16:4–9.
    1. Talaat M, el-Oun S, Kandeel A, Abu-Rabei W, Bodenschatz C, Lohiniva AL, Hallaj Z, Mahoney FJ. Overview of injection practices in two governorates in Egypt. Trop Med Int Health. 2003;8:234–241.
    1. Hagan H, Jarlais DC, Friedman SR, Purchase D, Alter MJ. Reduced risk of hepatitis B and hepatitis C among injection drug users in the Tacoma syringe exchange program. Am J Public Health. 1995;85:1531–1537.
    1. Abdel-Ghaffar TY, Sira MM, El Naghi S. Hepatitis C genotype 4: The past, present, and future. World J Hepatol. 2015;7:2792–2810.
    1. Gamal E. 2014. Situation of HCV in Egypt Towards an End to HCV Epidemic. Available from: .
    1. Ayoub HH, Abu-Raddad LJ. Impact of treatment on hepatitis C virus transmission and incidence in Egypt: A case for treatment as prevention. J Viral Hepat. 2017;24:486–495.
    1. Paez Jimenez A, El-Din NS, El-Hoseiny M, El-Daly M, Abdel-Hamid M, El Aidi S, Sultan Y, El-Sayed N, Mohamed MK, Fontanet A. Community transmission of hepatitis B virus in Egypt: results from a case-control study in Greater Cairo. Int J Epidemiol. 2009;38:757–765.
    1. Metwally A, Mohsen A, Saleh R, Foaud W, Ibrahim N, Rabaah T, El-Sayed M. Prioritizing High-Risk Practices and Exploring New Emerging Ones Associated With Hepatitis C Virus Infection in Egypt. Iran J Public Health. 2014;43:1385–1394.
    1. Guerra J, Garenne M, Mohamed MK, Fontanet A. HCV burden of infection in Egypt: results from a nationwide survey. J Viral Hepat. 2012;19:560–567.
    1. Dolan K, MacDonald M, Silins E, Topp L. Needle and syringe programs: A review of the evidence. Canberra: Australian Government Department of Health and Ageing; 2005. Available from: .
    1. Islam MM, Topp L, Conigrave KM, Haber PS, White A, Day CA. Sexually transmitted infections, sexual risk behaviours and perceived barriers to safe sex among drug users. Aust N Z J Public Health. 2013;37:311–315.
    1. Centers for Disease Control and Prevention (CDC) Progress toward prevention and control of hepatitis C virus infection--Egypt, 2001-2012. MMWR Morb Mortal Wkly Rep. 2012;61:545–549.
    1. Calès P, Boursier J, Bertrais S, Oberti F, Gallois Y, Fouchard-Hubert I, Dib N, Zarski JP, Rousselet MC; multicentric groups (SNIFF 14 & 17, ANRS HC EP 23 Fibrostar) Optimization and robustness of blood tests for liver fibrosis and cirrhosis. Clin Biochem. 2010;43:1315–1322.
    1. Nguyen LH, Nguyen MH. Systematic review: Asian patients with chronic hepatitis C infection. Aliment Pharmacol Ther. 2013;37:921–936.
    1. Kandeel AM, Talaat M, Afifi SA, El-Sayed NM, Abdel Fadeel MA, Hajjeh RA, Mahoney FJ. Case control study to identify risk factors for acute hepatitis C virus infection in Egypt. BMC Infect Dis. 2012;12:294.
    1. Breban R, Arafa N, Leroy S, Mostafa A, Bakr I, Tondeur L, Abdel-Hamid M, Doss W, Esmat G, Mohamed MK, et al. Effect of preventive and curative interventions on hepatitis C virus transmission in Egypt (ANRS 1211): a modelling study. Lancet Glob Health. 2014;2:e541–e549.
    1. U.S. Preventive Services Task Force. Final recommendation statement: Hepatitis C screening. USPSTF. 2013. Available from: .
    1. Artenie AA, Bruneau J, Lévesque A, Wansuanganyi JM. Role of primary care providers in hepatitis C prevention and care: one step away from evidence-based practice. Can Fam Physician. 2014;60:881–882, e468-e470.
    1. Alter HJ, Purcell RH, Shih JW, Melpolder JC, Houghton M, Choo QL, Kuo G. Detection of antibody to hepatitis C virus in prospectively followed transfusion recipients with acute and chronic non-A, non-B hepatitis. N Engl J Med. 1989;321:1494–1500.
    1. Elkareh S. HCV screening of donors in Governmental Blood Transfusion Centers at Menoufia Governorate (from Jan. 2008 to Oct. 2008) Vox Sang. 2009;96:89–90.
    1. Eita N. Prevalence of HCV and HBV infections among blood donors in Dakahilia, Egypt. Vox Sang. 2009;96:106–107.
    1. Rushdy O, Moftah F, Zakareya S. Trasmitted transfused viral infections among blood donors during years 2006 and 2007 in suez canal area, Egypt. Vox Sang. 2009;96:86–87.
    1. Arthur RR, Hassan NF, Abdallah MY, el-Sharkawy MS, Saad MD, Hackbart BG, Imam IZ. Hepatitis C antibody prevalence in blood donors in different governorates in Egypt. Trans R Soc Trop Med Hyg. 1997;91:271–274.
    1. El-Sherbini A, Hassan W, Abdel-Hamid M, Naeim A. Natural history of hepatitis C virus among apparently normal schoolchildren: follow-up after 7 years. J Trop Pediatr. 2003;49:384–385.
    1. Mohamed MK, Magder LS, Abdel-Hamid M, El-Daly M, Mikhail NN, Abdel-Aziz F, Medhat A, Thiers V, Strickland GT. Transmission of hepatitis C virus between parents and children. Am J Trop Med Hyg. 2006;75:16–20.
    1. El Sherbini A, Mohsen SA, Hasan W, Mostafa S, El Gohary K, Moneib A, Abaza AH. The peak impact of an Egyptain outbreak of hepatitis C virus: has it passed or has not yet occurred? Liver Int. 2007;27:876–877.
    1. Morad WS. Transmission of hepatitis C between spouses an epidemiological study at National Liver Institute hospital. Int J Infect Dis. 2011;15:S81.
    1. El-Zayadi A, Khalifa AA, El-Misiery A, Naser AM, Dabbous H, Aboul-Ezz AA. Evaluation of risk factors for intrafamilial transmission of HCV infection in Egypt. J Egypt Public Health Assoc. 1997;72:33–51.
    1. Mohamoud YA, Mumtaz GR, Riome S, Miller D, Abu-Raddad LJ. The epidemiology of hepatitis C virus in Egypt: a systematic review and data synthesis. BMC Infect Dis. 2013;13:288.
    1. Shalaby S, Kabbash IA, El Saleet G, Mansour N, Omar A, El Nawawy A. Hepatitis B and C viral infection: prevalence, knowledge, attitude and practice among barbers and clients in Gharbia governorate, Egypt. East Mediterr Health J. 2010;16:10–17.
    1. Coppola N, De Pascalis S, Onorato L, Calò F, Sagnelli C, Sagnelli E. Hepatitis B virus and hepatitis C virus infection in healthcare workers. World J Hepatol. 2016;8:273–281.
    1. Arguillas MO, Domingo EO, Tsuda F, Mayumi M, Suzuki H. Seroepidemiology of hepatitis C virus infection in the Philippines: a preliminary study and comparison with hepatitis B virus infection among blood donors, medical personnel, and patient groups in Davao, Philippines. Gastroenterol Jpn. 1991;26 Suppl 3:170–175.
    1. Ozsoy MF, Oncul O, Cavuslu S, Erdemoglu A, Emekdas G, Pahsa A. Seroprevalences of hepatitis B and C among health care workers in Turkey. J Viral Hepat. 2003;10:150–156.
    1. Okasha O, Munier A, Delarocque-Astagneau E, El Houssinie M, Rafik M, Bassim H, Hamid MA, Mohamed MK, Fontanet A. Hepatitis C virus infection and risk factors in health-care workers at Ain Shams University Hospitals, Cairo, Egypt. East Mediterr Health J. 2015;21:199–212.
    1. Central Agency for Public Mobilisation and Statistics (CAPMAS) 2013. Poverty indicators according to income, expenditure and consump¬tion data 2012-2013. Available from: .
    1. Waked I, Doss W, El-Sayed MH, Estes C, Razavi H, Shiha G, Yosry A, Esmat G. The current and future disease burden of chronic hepatitis C virus infection in Egypt. Arab J Gastroenterol. 2014;15:45–52.
    1. Iskander D. The Right to Health: a case study on Hepatitis C in Egypt. MS.c. thesis, American University in Cairo. 2013. Available from: URL: .
    1. Amer KE, Marwan I. Living donor liver transplantation in Egypt. Hepatobiliary Surg Nutr. 2016;5:98–106.
    1. World Health Organization. Mortality database. WHO statistical information system. Available from: .
    1. Venook AP, Papandreou C, Furuse J, de Guevara LL. The incidence and epidemiology of hepatocellular carcinoma: a global and regional perspective. Oncologist. 2010;15 Suppl 4:5–13.
    1. Egyptian National Cancer Registry. Available from: .
    1. Khalili K, Menezes R, Yazdi LK, Jang HJ, Kim TK, Sharma S, Feld J, Sherman M. Hepatocellular carcinoma in a large Canadian urban centre: stage at treatment and its potential determinants. Can J Gastroenterol Hepatol. 2014;28:150–154.
    1. Abdelaziz AO, Nabil MM, Abdelmaksoud AH, Shousha HI, Cordie AA, Hassan EM, Omran DA, Leithy R, Elbaz TM. De-novo versus recurrent hepatocellular carcinoma following direct-acting antiviral therapy for hepatitis C virus. Eur J Gastroenterol Hepatol. 2018;30:39–43.

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