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Review

A review of the experience of childhood hepatitis A vaccination in Saudi Arabia and Turkey: implications for hepatitis A control and prevention in the Middle East and North African region

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Pages 3710-3728 | Received 15 Dec 2020, Accepted 18 Apr 2021, Published online: 02 Jul 2021

References

  • Centers for Disease Control and Prevention. Epidemiology and prevention of vaccine-preventable diseases. Washington (D.C.): Centers for Disease Control and Prevention; 2015.
  • World Health Organization. Hepatitis A. Geneva (Switzerland): World Health Organization; 2019 [accessed 2020 Apr 15]. https://www.who.int/en/news-room/fact-sheets/detail/hepatitis-a.
  • Kurkela S, Pebody R, Kafatos G, Andrews N, Barbara C, Bruzzone B, Butur D, Caplinskas S, Davidkin I, Hatzakis A, et al. Comparative hepatitis A seroepidemiology in 10 European countries. Epidemiol Infect. 2012;140(12):2172–81. doi:10.1017/s0950268812000015.
  • Franco E, Meleleo C, Serino L, Sorbara D, Zaratti L. Hepatitis A: epidemiology and prevention in developing countries. World J Hepatol. 2012;4(3):68–73. doi:10.4254/wjh.v4.i3.68.
  • Agrawal A, Singh S, Kolhapure S, Hoet B, Arankalle V, Mitra M. Increasing Burden of Hepatitis A in Adolescents and Adults and the Need for Long-Term Protection: a Review from the Indian Subcontinent. Infect Dis Ther. 2019;8(4):483–97. doi:10.1007/s40121-019-00270-9.
  • John Hopkins Medicine. Viral hepatitis A and E. Internet. 2020 [accessed 2020 May 31]. https://www.hopkinsmedicine.org/health/conditions-and-diseases/hepatitis/viral-hepatitis-a-and-e.
  • Jacobsen KH. Globalization and the changing epidemiology of hepatitis A virus. Cold Spring Harb Perspect Med. 2018;8(10):a031716. doi:10.1101/cshperspect.a031716.
  • Jacobsen KH, Koopman JS. Declining hepatitis A seroprevalence: a global review and analysis. Epidemiol Infect. 2004;132(6):1005–22. doi:10.1017/s0950268804002857.
  • Jacobsen KH, Koopman JS. The effects of socioeconomic development on worldwide hepatitis A virus seroprevalence patterns. Int J Epidemiol. 2005;34(3):600–09. doi:10.1093/ije/dyi062.
  • World Health Organization. WHO position paper on hepatitis A vaccines – June 2012. Wkly Epidemiol Rec. 2012;87(28–29):261–276.
  • Jacobsen KH, Wiersma ST. Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine. 2010;28(41):6653–57. doi:10.1016/j.vaccine.2010.08.037.
  • Aggarwal R, Goel A. Hepatitis A: epidemiology in resource-poor countries. Curr Opin Infect Dis. 2015;28(5):488–96. doi:10.1097/qco.0000000000000188.
  • Jacobsen K. The global prevalence of hepatitis A virus infection and susceptibility: a systematic review. https://apps.who.int/iris/handle/10665/70180,2009.WHO/IVB/10.01
  • Lolekha S, Pratuangtham S, Punpanich W, Bowonkiratikachorn P, Chimabutra K, Weber F. Immunogenicity and safety of two doses of a paediatric hepatitis A vaccine in Thai children: comparison of three vaccination schedules. J Trop Pediatr. 2003;49(6):333–39. doi:10.1093/tropej/49.6.333.
  • Raczniak GA, Bulkow LR, Bruce MG, Zanis CL, Baum RL, Snowball MM, Byrd KK, Sharapov UM, Hennessy TW, McMahon BJ. Long-term immunogenicity of hepatitis A virus vaccine in Alaska 17 years after initial childhood series. J Infect Dis. 2013;207(3):493–96. doi:10.1093/infdis/jis710.
  • Sharapov UM, Bulkow LR, Negus SE, Spradling PR, Homan C, Drobeniuc J, Bruce M, Kamili S, Hu DJ, McMahon BJ. Persistence of hepatitis A vaccine induced seropositivity in infants and young children by maternal antibody status: 10-year follow-up. Hepatology. 2012;56(2):516–22. doi:10.1002/hep.25687.
  • Mohd Hanafiah K, Jacobsen KH, Wiersma ST. Challenges to mapping the health risk of hepatitis A virus infection. Int J Health Geogr. 2011;10:57. doi:10.1186/1476-072x-10-57.
  • Koroglu M, Jacobsen KH, Demiray T, Ozbek A, Erkorkmaz U, Altindis M. Socioeconomic indicators are strong predictors of hepatitis A seroprevalence rates in the Middle East and North Africa. J Infect Public Health. 2017;10(5):513–17. doi:10.1016/j.jiph.2016.09.020.
  • Safiabadi M, Rezaee-Zavareh MS, Moayed Alavian S. Estimation of hepatitis A virus infection prevalence among Eastern Mediterranean and Middle Eastern Countries: a systematic review and pooled analysis. Hepat Mon. 2017;17(2):e44695. doi:10.5812/hepatmon.44695.
  • Melhem NM, Talhouk R, Rachidi H, Ramia S. Hepatitis A virus in the Middle East and North Africa region: a new challenge. J Viral Hepat. 2014;21(9):605–15. doi:10.1111/jvh.12282.
  • Itani T, Jacobsen KH, Nguyen T, Wiktor SZ. A new method for imputing country-level estimates of hepatitis A virus endemicity levels in the Eastern Mediterranean region. Vaccine. 2014;32(46):6067–74. doi:10.1016/j.vaccine.2014.09.006.
  • Mahboobi N, Alavian S. Hepatitis A in the Eastern Mediterranean Region: a review on the prevalence. Scimetr. 2013;2:e14613. doi:10.5812/scimetr.14613.
  • Ministry of Health Kingdom of Saudi Arabia. Statistical yearbook. 2018 [accessed 2020 July 10]. https://www.moh.gov.sa/en/Ministry/Statistics/book/Documents/book-Statistics.pdf.
  • Turkish viral hepatitis prevention and control program (2018-2023), Ministry of health Ed. 1. Ankara; 2018 [accessed 2021 Mar 17]. https://hsgm.saglik.gov.tr/depo/birimler/Bulasici-hastaliklar-db/duyurular/Turkiye_Viral_Hepatit_Onleme_ve_Kontrol_Programi/Turkiye_Viral_Hepatit_Onleme_ve_Kontrol_Programi_TR.pdf.
  • World Population Review. About Saudi Arabia. World Population Review; 2020 [accessed 2020 July 10]. https://worldpopulationreview.com/countries/saudi-arabia-population/.
  • World Population Review. About Turkey. World Population Review; 2020 [accessed 2020 July 10]. https://worldpopulationreview.com/countries/turkey-population/.
  • Alshabanat A, Albacker R, Basalamah A, Salamah A, Al-Frayh A. Profile of viral hepatitis in Saudi Arabia. Biomedical Res. 2013;24:396–99.
  • Hendrickx G, Van Herck K, Vorsters A, Wiersma S, Shapiro C, Andrus JK, Ropero AM, Shouval D, Ward W, Van Damme P. Has the time come to control hepatitis A globally? Matching prevention to the changing epidemiology. J Viral Hepat. 2008;15(Suppl 2):1–15. doi:10.1111/j.1365-2893.2008.01022.x.
  • Memish ZA, Knawy BA, El-Saed A. Incidence trends of viral hepatitis A, B, and C seropositivity over eight years of surveillance in Saudi Arabia. Int J Infect Dis. 2010;14(2):e115–120. doi:10.1016/j.ijid.2009.03.027.
  • Babaeer MHS, Awfi MSHA. Prevalence Study of Hepatitis A Virus (HAV) on Jeddah Population. Biosci Biotech Res Asia. 2011;8(2).
  • Ashraf SJ, Arya SC, Parande CM, Kristensen E. Hepatitis A virus among natives and expatriates in Saudi Arabia. J Med Virol. 1986;19(2):151–53. doi:10.1002/jmv.1890190207.
  • Fathalla SE, Al-Jama AA, Al-Sheikh IH, Islam SI. Seroprevalence of hepatitis A virus markers in Eastern Saudi Arabia. Saudi Med J. 2000;21:945–49.
  • Al-Faleh FZ, Al-Jeffri MH, Ramia ST, Al-Rashed RS, Arif MA, Mohammed OM, Bakhsh MH, Al-Freihi HM, Aljumah AA, Rezeig MA, et al. Hepatitis A in Saudi Arabia: a comparative sero-epidemiological study. Saudi Med J. 1999;20(9):678–81.
  • El-Gilany A-H, Hammad S, Refaat K, Al-Enazi R. Seroprevalence of hepatitis A antibodies among children in a Saudi community. Asian Pac J Trop Med. 2010;3(4):278–82. doi:10.1016/S1995-7645(10)60068-5.
  • Baki A, Aynaci M, Koksal I. Prevalence of antibody to hepatitis A virus among children in Trabzon, Turkey. Infection. 1993;21(2):132–33. doi:10.1007/bf01710752.
  • Almuneef MA, Memish ZA, Balkhy HH, Qahtani M, Alotaibi B, Hajeer A, Qasim L, Al Knawy B. Epidemiologic shift in the prevalence of Hepatitis A virus in Saudi Arabia: a case for routine Hepatitis A vaccination. Vaccine. 2006;24(27–28):5599–5603. doi:10.1016/j.vaccine.2006.04.038
  • Jaber SM, Prevalence of anti-hepatitis B and anti-hepatitis A antibodies among school aged children in Western Saudi Arabia. Saudi Med J. 2006;27(10):1515–1522.
  • Almuneef MA, Memish ZA, Balkhy HH, Otaibi B, Helmi M. Seroprevalence survey of varicella, measles, rubella, and hepatitis A and B viruses in a Xhealthcare workforce in Saudi Arabia. Infect Control Hosp Epidemiol. 2006;27(11):1178–1183. doi:10.1086/508826
  • Al-Tawfiq JA, Anani A. Profile of viral hepatitis A, B, and C in a Saudi Arabian hospital. Med Sci Monit. 2008;14(1):Cr52–56.
  • Memish Z, Qasim L, Abed E, AlBasheer A, Aldraihim A, Knawy B, Hajeer AH. Pattern of viral hepatitis infection in a selected population from Saudi Arabia. Mil Med. 2003;168(7):565–568.
  • Barrimah E, Salem KA, Gabal MS. An outbreak of hepatitis A associated with treated waste water used for irrigation. J Egypt Public Health Assoc. 1999;74(3–4):227–239.
  • Ersoy B, Aydogan A, Dincoguz A, Sinan Meral M, Turul T. The seroprevalence of anti-HAV among 0-16-year-olds referred to pediatric outpatients clinics of a hospital. J Trop Pediatr. 1998;44(1):55–56. doi:10.1093/tropej/44.1.55.
  • Sac RU, Bostanci I, Dallar Y, Cihan G, Atli O. Hepatitis A seroprevalence and demographics in Turkish children in Ankara. Pediatr Int. 2009;51(1):5–8. doi:10.1111/j.1442-200X.2008.02671.x.
  • Arif M, Al-Faleh FZ, Al-Frayh AR, Ramia S. Reduction in the prevalence of antibody to hepatitis A virus among young Saudi adults: implications for hepatitis A vaccine. Saudi J Gastroenterol. 1995;1(2):93–96.
  • Al-Knawy B, El-Mekki AA, Yarbough PO. The role of hepatitis E virus infection among patients with acute viral hepatitis in southern Saudi Arabia. Ann Saudi Med. 1997;17(1):32–34. doi:10.5144/0256-4947.1997.32
  • Ghabrah TM, Stickland GT, Tsarev S, Yarbough P, Farci P, Engle R, Emerson S, Purcell R. Acute viral hepatitis in Saudi Arabia: seroepidemiological analysis, risk factors, clinical manifestations, and evidence for a sixth hepatitis agent. Clin Infect Dis. 1995;21(3):621–627. doi:10.1093/clinids/21.3.621
  • Ramia S, Antibody against hepatitis A in Saudi Arabians and in expatriates from various parts of the world working in Saudi Arabia. J Infect. 1986;12(2):153–155. doi:10.1016/s0163-4453(86)93633-9
  • Talukder MA, Waller DK, Nixon P, Al-Admawy AM. Prevalence of antibody to hepatitis A virus in a Saudi Arabian hospital population. J Infect Dis. 1983;148(6):1167. doi:10.1093/infdis/148.6.1167
  • Nalbantoglu B, Donma MM, Ozdilek B, Karasu E, Nalbantoglu A. Shifting epidemiology of hepatitis a infection and vaccination status of children aged 6 months-12 years: time for mass vaccination. Iran J Pediatr. 2013;23:276–80.
  • Yüksek SK, Tezer H, Parlakay A, Gülhan B, Kara A, Çiftçi E, Tapısız A, Çelik M, Özdemir H, Aykaç K, et al. Impact of the mandatory Hepatitis A immunization program: before and after the vaccine in Ankara, Central of Turkey. Turk J Pediatr. 2019;61(5):677–85. doi:10.24953/turkjped.2019.05.006.
  • Kader Ç, Göçmen AY, Demir MI, Çolak NY, Gök SE, Arkan FI, Sara MY, Erbay A. Hepatitis A immunity in Yozgat, Turkey. Ann Saudi Med. 2019;39(1): 37–41. doi:10.5144/0256-4947.2019.37
  • Karadeniz A, Akduman Alaşehir E. Seroepidemiology of hepatitis viruses, measles, mumps, rubella and varicella among healthcare workers and students: Should we screen before vaccination? J Infect Public Health. 2020;13(4):480–484. doi:10.1016/j.jiph.2020.01.309
  • Köse Ş, Ödemiş I, Çelik D, Gireniz Tatar B, Akbulut I, Çiftdoğan DY. Hepatitis A, B, C and HIV seroprevalence among Syrian refugee children admitted to outpatient clinics. Infez Med. 2017;25(4):339–343.
  • Yentür Doni N, Şimşek Z, Gürses G, Yıldız Zeyrek F, Akbaba M. The knowledge and high seroprevalence of hepatitis A in a high-risk group (agricultural reproductive-aged women) in the southeastern region of Turkey. Turk J Med Sci. 2017;47(4):1055–1060. doi:10.3906/sag-1505-22
  • Viral Hepatitis Prevention Board. Epidemiology of viral hepatitis in Turkey. Antwerp (Belgium): VHPB; 2010, p. 26. https://www.vhpb.org/files/html/Meetings_and_publications/Viral_Hepatitis_Newsletters/vhv18n2.pdf.
  • Atabek ME, Fyndyk D, Gulyuz A, Erkul I. Prevalence of anti-HAV and anti-HEV antibodies in Konya, Turkey. Health Policy (New York). 2004;67(3):265–69. doi:10.1016/s0168-8510(03)00123-4.
  • Özden HT. Hepatitis A seroprevalence in patients with chronic viral hepatitis in Konya, Turkey. Eur J Gastroenterol Hepatol. 2016;28(3):333–37. doi:10.1097/meg.0000000000000547.
  • Tulek N, Ozsoy M, Moroglu C, Cagla Sonmezer M, Temocin F, Tuncer Ertem G, Sebnem Erdinc F. Seroprevalence of Hepatitis A Virus Antibodies among the Patients with Chronic Hepatitis B in Turkey. Euroasian J Hepatogastroenterol. 2015;5(2):95–97. doi:10.5005/jp-journals-10018-1143.
  • Saglik Bakanligi TC Hepatit A asi Uygulamasi Ust Yazisi. [accessed 2020 July 10]. https://dosyaism.saglik.gov.tr/Eklenti/12472,20121008-1509-hskdan-hepatit-a-asisinin-uygulanmasi-hakkinda-yazipdf.pdf?0.
  • Dogru AO, David RM, Ulugtekin N, Goksel C, Seker DZ, Sozen S. GIS based spatial pattern analysis: children with Hepatitis A in Turkey. Environ Res. 2017;156:349–57. doi:10.1016/j.envres.2017.04.001.
  • Ceyhan M, Yildirim I, Kurt N, Uysal G, Dikici B, Ecevit C, Aydogan A, Koc A, Yasa O, Koseoglu M, et al. Differences in hepatitis A seroprevalence among geographical regions in Turkey: a need for regional vaccination recommendations. J Viral Hepat. 2008;15(Suppl 2):69–72. doi:10.1111/j.1365-2893.2008.01034.x.
  • Demiray T, Koroglu M, Jacobsen KH, Ozbek A, Terzi HA, Altindis M. Hepatitis A virus epidemiology in Turkey as universal childhood vaccination begins: seroprevalence and endemicity by region. Turk J Pediatr. 2016;58(5):480–91. doi:10.24953/turkjped.2016.05.004.
  • Ergonul O, Tulek N, Kayi I, Irmak H, Erdem O, Dara M. Profiling infectious diseases in Turkey after the influx of 3.5 million Syrian refugees. Clin Microbiol Infect. 2020;26(3):307–12. doi:10.1016/j.cmi.2019.06.022.
  • Armstrong GL, Billah K, Rein DB, Hicks KA, Wirth KE, Bell BP. The economics of routine childhood hepatitis A immunization in the United States: the impact of herd immunity. Pediatrics. 2007;119(1):e22–29. doi:10.1542/peds.2006-1572.
  • Gözü Pirinççioğlu A, Adıgüzel S, Özekinci T. Seropositivity of Hepatitis A in Children Aged 7-14 Years in Diyarbakir Province Center. Med Sci Monit. 2018;24:936–943. doi:10.12659/msm.906861
  • Karacaer Z, Tosun S, Batırel A, Şahin S, Altaş İ, Uysal S, Erol S, Ceran N, Albayrak A, Yıldız İE, et al. Changes in acute viral hepatitis epidemiology in the Turkish adult population: A multicenter study. Turk J Gastroenterol. 2018;29(2):177–182. doi:10.5152/tjg.2018.17431
  • Ceran N, Yuksel Kocdogan F, Mert D, Erdem I, Dede B, Adaleti R, Ozyurek S, Karagul E, Goktas P. Hepatitis A seroprevalence in children and young adults in Istanbul, Turkey: seroprevalence change and associated factors. J Viral Hepat. 2012;19(1):72–76. doi:10.1111/j.1365-2893.2011.01454.x
  • Karaman S, Karaman K, Kızılyıldız BS, Ceylan N, Kaba S, Parlak M, Beger B, Ceylan A. Seroprevalence of hepatitis a and associated factors among 1–15 year old children in Eastern Turkey. Int J Clin Exp Med. 2015;8(10):19394–19399.
  • Alhan E, Kozanoglu B, Tumgor G, Celik U, Yaman A, Bozdemir N. Epidemiological shift of hepatitis A in central Adana, Turkey. Turk J Gastroenterol. 2014;25 Suppl 1:6–8. doi:10.5152/tjg.2014.4163
  • Halicioglu O, Akman SA, Tatar B, Atesli R, Kose S. Hepatitis A seroprevalence in children and adolescents aged 1–18 years among a low socioeconomic population in Izmir, Turkey. Travel Med Infect Dis. 2012;10(1):43–47. doi:10.1016/j.tmaid.2012.01.001
  • Kurugol Z, Aslan A, Turkoglu E, Koturoglu G. Changing epidemiology of hepatitis A infection in Izmir, Turkey. Vaccine. 2011;29(37):6259–6261. doi:10.1016/j.vaccine.2011.06.069
  • Ince OT, Yalçin SS, Yurdakök K, Ozmert EN. Hepatitis A seroprevalence among infants aged 12 months in Ankara. Turk J Pediatr. 2011;53(1):114–116.
  • Coskun O, Erdem H, Gul HC, Eyigun CP. Changes in hepatitis A prevalence rates between 1998 and 2007 in Eskisehir, Turkey. Int J Infect Dis. 2008;12(6):e141. doi:10.1016/j.ijid.2008.02.005
  • Kaya D, Guler E, Ekerbicer HC, Dilber C, Karabiber H, Guler S, Davutoglu M, Ciragil P. Hepatitis A seroprevalence and its relationship with environmental factors in children of different age groups in Kahramanmaras, Eastern Mediterranean region of Turkey. J Viral Hepat. 2007;14(12):830–834. doi:10.1111/j.1365-2893.2007.00886.x
  • Kaya AD, Ozturk CE, Yavuz T, Ozaydin C, Bahcebasi T. Changing patterns of hepatitis A and E sero-prevalences in children after the 1999 earthquakes in Duzce, Turkey. J Paediatr Child Health. 2008;44(4):205–207. doi:10.1111/j.1440-1754.2007.01248.x
  • Tosun S, Ertan P, Kasirga E, Atman U. Changes in seroprevalence of hepatitis A in children and adolescents in Manisa, Turkey. Pediatr Int. 2004;46(6):669–672. doi:10.1111/j.1442-200x.2004.01969.x
  • Kanra G, Tezcan S, Badur S, Turkish National Study Team. Hepatitis A seroprevalence in a random sample of the Turkish population by simultaneous EPI cluster and comparison with surveys in Turkey. Turk J Pediatr. 2002;44(3):204–210.
  • Sıdal M, Unüvar E, Oğuz F, Cihan C, Önel D, Badur S. Age-specific seroepidemiology of hepatitis A, B, and E infections among children in Istanbul, Turkey. Eur J Epidemiol. 2001;17(2):141–144. doi:10.1023/A:1017524630372
  • Lemon SM, Ott JJ, Van Damme P, Shouval D. Type A viral hepatitis: a summary and update on the molecular virology, epidemiology, pathogenesis and prevention. J Hepatol. 2018;68(1):167–84. doi:10.1016/j.jhep.2017.08.034.

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