Hepatitis A in the Eastern Mediterranean Region: a comprehensive review

Figures & data

Figure 1. Plain language summary.

Table 1. Inclusion and exclusion criteria.

	Inclusion criteria	Exclusion criteria
Population	Hepatitis A disease (not limited to risk groups or specific ages)	Populations with chronic diseases or underlying comorbidities that are not representative of the general population
Intervention	Not restricted by intervention	N.A.
Comparator	Not restricted by comparator	N.A.
Outcome	Proportion of HAV among all acute viral hepatitis (HAV IgM)	N.A.
	HAV seroprevalence (HAV IgG)
Study design	Primary peer-reviewed research observational studies	Non-primary research
	Cohort studies	Systematic reviews
	Case-control studies	Meta-analyses
	Cross-sectional studies	Narrative reviews (without methods)
	Ecological studies	Predictions via modeling methods
	Outbreak investigations	Case reports
	Periodic surveys	Letter to editor
	Non-peer-reviewed research	Newspaper
	Reports from national and regional databases or websites	Editorial
		Comment
		Opinions
Limits
Publication date	From 1980 onwards	All publications before 1980
Geographic scope	Afghanistan, Bahrain, Djibouti, Egypt, Islamic Republic of Iran, Republic of Iraq, Jordan, Kuwait, Lebanon, Libya, Morocco, Oman, Pakistan, Palestine, Qatar, Saudi Arabia, Somalia, Sudan, Syrian Arab Republic, Tunisia, United Arab Emirates, Yemen	All countries apart from those considered eligible
Language	English, French, Arabic	-

Note: HAV, hepatitis A virus; IgG, immunoglobulin G; IgM, immunoglobulin M; N.A, not applicable.

Figure 2. PRISMA flow diagram showing the study research and selection process.

Figure 3. Classification of included countries by income level and hepatitis a vaccination status.

Notes: NIP, national immunization program; UAE: United Arab Emirates.

Table 2. Demographic characteristics and HAV vaccination status of the 22 EMR countries.

COUNTRY	Geographic region	World bank classification (2017)^Citation14	GAVI eligibility (2017)^Citation140	HAV vaccination in NIP	Year of vaccination implementation	Availability of vaccine (private/public)	Recommendation status	Reimbursement
Afghanistan	Asia	LIC	Yes	No	N.A.	Private	-	No
Bahrain	Middle East	HIC	No	Yes	2012	Public	15 and 24 months High risk groups and travellers^Citation141	Reimbursed
Djibouti	Middle East	LMIC	NIP through GAVI support	No	-	-	No	-
Egypt	Africa	LMIC	No	No	-	Private	-	No
Iran, Islamic Republic Of	Asia	UMIC	No	No	-	Private	-	No
Iraq	Middle East	UMIC	No	High risk group	-	Private	-	No
Jordan	Middle East	UMIC	No	No	-	Private	-	No
Kuwait	Middle East	HIC	No	No	-	Private	Citizens born prior to 1990 and healthcare personnel^Citation141	No
Lebanon	Middle East	UMIC	No	No	-	Private	-	No
Libya	Africa	UMIC	No	No	-	-	No	-
Morocco	Africa	LMIC	No	No	-	Private	18 and 24 months	In private market: covered by insurance
Oman	Middle East	HIC	No	Yes	2020	Both	13 and 24 months	Reimbursed
Pakistan	Asia	LMIC	Yes	No	N.A.	Private	*	No
Palestine	Middle East	LIC	No	No	-	Private	18 and 24 months	No
Qatar	Middle East	HIC	No	Yes	2012	Both	12 and 18 months	Reimbursed
Saudi Arabia	Middle East	HIC	No	Yes	2008	Both	18 and 24 months	In private market: covered by insurance, Public: FoC for Saudi, non-Saudi and illegal immigrants
Somalia	Asia	LIC	Yes	No	-	-	-	-
Sudan, Republic of	Africa	LIC	Yes	No	-	-	-	No
Syrian Arab Republic	Middle East	LMIC	Yes	No	-	Private	-	No
Tunisia	Africa	LMIC	No	Yes	2019	Both	12 months and 6 years	In private market: covered by insurance, Public: FoC
United Arab Emirates	Middle East	HIC	No	No	-	Private	High risk groups and travelers^Citation141	No
Yemen	Middle East	LIC	Yes	No	-	-	-	-

*No local recommendations. Recommended by international bodies for HAV in case people are traveling to Pakistan.

FoC, free of charge; GAVI, the vaccine alliance; HIC, high-income countries; LIC, low-income countries; LMIC, low- middle- income countries; N.A., Not applicable; NIP, national immunization programs; UMIC, Upper-middle income countries; WHO-EMR, World Health Organization—Eastern Mediterranean Region.

Table 3. Occurrence of HAV among acute viral hepatitis cases (41 studies).

Studies by country	Data period, year(s)	Study population (number, age restrictions)	HAV, % (n)
Djibouti
Coursaget et al., 1998^Citation125	1992–1993	111 pts, 2–65 y	33% (37)
Egypt
Fouad et al., 2018^Citation85	2015–2017	268 pts, 1–18 y	97% (260)
Talaat et al., 2019^Citation89	2014–2017	9,321 pts, all ages	93.4% (7,806)
Hasan et al., 2016^Citation86	2007–2008	123 pts, 2–18 y	13.8% (17)
Eldin et al., 2010^Citation84	2007–2008	235 pts, 1–65 y	8.1% (19)
Meky et al., 2006^Citation88	2002–2005	47 community residents, 2–77 y	8.5% (4)
Talaat et al., 2010^Citation90	2001–2004	5,909 pts, all ages	28.5% (1,684)
Zakaria et al., 2007^Citation92	2001–2002 1983	200 pts, all ages 235 pts, all ages	34% (68) 2.1% (5)
Hyams et al., 1992^Citation87	1987–1988	73 outpatients, ≤13 y	41% (30)
Divizia et al., 1999^Citation83	1993	202 hospitalized pts, 1–73 y	10.4% (21)
Youssef et al., 2013^Citation91	n.r.	33 hospitalized children	33% (11)
Zaki Mel et al., 2008^Citation93	n.r.	162 children	34.1% (n.r)
Darwish et al., 1992^Citation82	n.r.	200 adult pts, 20–40 y	4.5% (9)
Iran
Karimi et al., 2015^Citation57	2010	70 pts	68.6% (48)
Iraq
Al-Naaimi et al., 2012^Citation114	2010–2011	2,629 pts, all ages	44.8% (1,206)
Turky et al., 2011^Citation117	2005–2006	2,975 pts, all ages	41% (1,219)
Marcus et al., 1993^Citation115	n.r.	107 pts, 1.5–65 y	40.2% (43)
Rassam et al., 1989^Citation116	n.r.	253 hospitalized pts, 3–65 y	15% (39)
Kuwait
Al-Kandari et al., 1986^Citation120	1983–1984	1,788 pts, all ages	1.5% (26)
Al-Kandari et al., 1987^Citation119	1980–1984	52 pregnant pts, 15–44 y	11.5% (6)
Lebanon
Shamma’a et al., 1984^Citation106	1980–1981	93 pts, >12 y	35.5% (33)
Pakistan
Khan et al., 2011^Citation99	2007–2008	89 pts, all ages	6.1% (4)
Ahmed et al., 2010^Citation97	1987–2007	346 outpatients, all ages	3.5% (12)
Waheed-uz-Zaman et al., 2006^Citation101	2003–2004	626 pts, all ages	40.6% (252)
Syed et al., 2003^Citation100	1994–1999	658 pts, 11 y and over	64.4% (424)
Haider et al., 1994^Citation98	1991	93 hospitalized pts, all ages	5.4% (5)
Qatar
Glynn et al., 1985^Citation138	1981	126 hospitalized pts, 13–52 y	5.5% (7)
Saudi Arabia
Al-Tawfiq et al., 2008^Citation32	2000–2005	1,214 pts, 1–94 y	10% (120)
Memish et al., 2003^Citation43	1999–2001 • 1999: • 2000: • 2001:	3,490 pts, all ages • 1,194 pts • 1,039 pts • 1,257 pts	8.2% (286) • 6.7% (80) • 6.9% (72) • 10.7% (134)
Fathalla et al., 2000^Citation40	1987–1999	683 pediatric pts	65% (641)
Ayoola et al., 2001^Citation37	1997–1998	246 pts, all ages	37% (91)
Arif et al., 1995^Citation34	1993–1994	133 pts, all ages	38.3% (51)
Yohannan et al., 1990^Citation46	1987	47 pts, <12 y	72% (34)
Al-Majed et al., 1990^Citation28	n.r.	23 pts, all ages	82.6% (19)
Al-Knawy et al., 1997^Citation27	n.r.	132 hospitalized pts, >3 y	81.8% (108)
Sudan
Hyams et al., 1991^Citation139	1987–1988	80 outpatients, <14 y	33.8% (27)
Syria
Al-Azmeh et al., 1999^Citation129	1995–1998	193 pts, >12 y	53.9% (104)
Tunisia
Neffatti et al., 2017^Citation110	2014–2015	92 pts, 1-62 y	21.7% (20)
Gharbi-Khelifi et al., 2012^Citation112	2006–2008	400 pts, 1-60 y	19.8% (79)
Hellera et al., 2014^Citation113	2004–2005	105 pts, 15–65 y	34.3% (36)
Yemen
Gunaid et al., 1997^Citation133	n.r.	78 pts, ≥13 y	5.1% (4)

HAV, hepatitis A virus; n, number of study participants who were anti-HAV positive; n.r., not reported; pts, patients; y, years.

Table 4. Seroprevalence of HAV (77 studies).

Studies by country	Data period, year(s)	Study population (number, age restrictions)	HAV seroprevalence (IgG), % (n*)
Afghanistan
Carmoi et al., 2009^Citation134	2008	102 anicteric pts, 5–65 y	99% (101) • <15 y: 91.7% • ≥15 y: 100%
Djibouti
Fox et al., 1988^Citation124	1987	400 healthy adults	98.5% (394)
Egypt
El-Karaksy et al., 2008^Citation77 and El-Karaksy et al., 2006^Citation78	2004	101 children with chronic liver disease (CLD), <18 y	85.1% (86) • <5 y: 62.1% • ≥5 y: 94.4%
Al-Aziz et al., 2008^Citation75	2002–2003	296 children with minor illnesses, 2.5–18 y	61.4% (181) • 2.5–6 y: 53.1% • 6–9 y: 56.4% • 9–18 y: 73.8%
Salama et al., 2007^Citation81	2003–2004	426 children with minor medical problems,3–18 y	86.2% (367) <6 y: 64.3% 6–10 y: 85.3% 11–15 y: 90.3% >15 y: 90%
Darwish et al., 1996^Citation76	1994	155 healthy community residents, 1–67 y	100% (155) • 1–3 y: 100% • ≤67 y: 100%
Kamel et al., 1995^Citation79	1992	1,259 healthy community residents, all ages	97.2% (1224) • 0–4 y: 92.7% • 5–9 y: 97.8% • 10–14 y: 97.9% • 15–19 y: 97.5% • 20–24 y: 96.6% • 25–29 y: 97.9% • 30–34 y: 95.5% • 35–39 y: 100% • 40–44 y: 93.3% • 45–49 y: 100% • 50–54 y: 97.6% • 55–59 y: 93.3% • 60–64 y:100% • 65–69 y: 100% • >70 y: 100%
Omar et al., 2000^Citation80	n.r.	228 community residents, preschool children	26.3% (60)
Iran
Mirzaei et al., 2016^Citation60	2014–2015	108 hemophilic pts, 4–85 y	77.8% (84)
Hesamizadeh et al., 2016^Citation53	2014	559 volunteer blood donors, >18 y	70.7% (395) • 18–27 y: 26.7% • 28–37 y: 59.8% • 38–47 y: 91.2% • >47 y: 94.8%
Hosseini Shokouh et al., 2015^Citation74	2012–2014	270, healthy medical students, 18–30 y	34.8% (94)
Vasmehjani et al., 2015^Citation73	2012–2013	159, CLD pts, 21–68 y	79.2% (126) • 21–30 y: 28.6% • 31–40 y: 91.4% • 41–50 y: 93.9% • <50 y: 95%)
Izadi et al., 2016^Citation55	2011–2013	1,554, healthy soldiers, 18–60 y	80.3% (1,248) • <20 y: 72.2% • 20–30 y: 79.1% • >30 y: 92.4%
Farajzadegan et al., 2014^Citation52	2003–2013	11,857 cumulative population of 16 studies (systematic review), all ages	51%–66%
Jahanbakhsh et al., 2018^Citation56	2012	569 homeless adults, 18–60 y	94.3% (nr) • <42 y: 90.3% • ≥42 y: 98.1%
Asaei et al., 2015^Citation48	2011–2012	1,030, healthy individuals, 0.5–95 y	66.2% (682) • 6–15 y: 18.3% • 16–29 y 79.4% • 30–55 y: 94.3% • ≥56 y: 98.2%
Bayani et al., 2013^Citation50	2011–2012	466 healthy healthcare workers	71% (330) • 20–29 y: 57.8% • 30–39 y: 77.1% • >40 y: 86.3%
Rabiee et al., 2013^Citation63	2011	1,813, healthy university students	39.8% (722)
Shoaei et al., 2012^Citation69	2010–2011	117, chronic hepatitis C pts	94.9% (111) • ≤30 y: 93.1% • 31–40 y: 93.3% • 41–50 y: 100% • 51–60 y: 100% • ≥61 y: 100%
Vakili et al., 2014^Citation72	2010	1,028, healthy 1^st year medical students,17-27 y	68.5% (704)
Saffar et al., 2012^Citation67	2010	984, community residents, 1–30 y	19.2% (189) • 1–2.9 y: 5.7% • 3–6.9 y: 9.1% • 7–10.9 y: 20.4% • 11–17.9 y: 34.8% • 18–30 y: 68.4%
Mostafavi et al., 2016^Citation62 and Hoseini et al., 2016^Citation54	2009–2010	2,494, national health survey participants,10–18 y	50.4%–78.8% across provinces 64% (1,597)
Sofian et al., 2010^Citation70	2009	1,065, pediatric hospital pts, 0.5–20 y	61.6% • 0.5–1.9 y: 61.5% • 2–5.9 y: 51.7% • 6–10.9 y: 52.9% • 11–15.9 y: 65.2% • 16–20 y: 85.0%
Taghavi et al., 2011^Citation71	2008–2009	1,050, pre-marriage lab analysis, 15–63 y	88.2% (927) • <20 y: 79.3% • 20–30 y: 91.3% • >30 y: 99%
Ramezani et al., 2011^Citation64	2008	351, blood donors, 17–60 y	94.9% (333)
Saneian et al., 2014^Citation68	2007	361, healthy medical students	75.3% (272)
Alian et al., 2011^Citation47	2007	1,034, community residents, 1–25 y	38.9% (402) • 1–5 y: 8.9% • 5–15 y: 15.8% • 15–25 y: 64.3%
Mohebbi et al., 2012^Citation61	2006–2007	551, community residents, 1–83 y	90.0% (496) • <30 y: 85.7% • 30–60 y: 90.7% • >60 y: 93.9%
Merat et al., 2010^Citation59	2006	1,869, community residents, 18–65 y	86%
Davoudi et al., 2010^Citation51	2005–2006	247 HIV+, 5–74 y	96.3% (238)
Ataei et al., 2008^Citation49	2006	816, community residents, >6 y	8.3%
Roushan et al., 2007^Citation65	2004–2005	392, HBsAg+ pts, 10–70 y	82.1% (332) • 10–19 y: 59.4% • 20–29 y: 89.8% • >29 y: 97.5%
Mehr et al., 2004^Citation58	2002	1,018, children in pediatric hospital, 0.5–15 y	22.3% (227)
Saberifiroozi et al., 2005^Citation66	n.r.	204, pts in liver clinic, adults	98% (200)
Jordan
Hayajneh et al., 2015^Citation127	2008	3,066, community residents, 0–85 y	51% • ≤1 y: 24% • 1–2 y: 26% • 2–4 y: 32% • 5–9 y: 44% • 10–14 y: 63% • 15–19 y: 78% • >20 y: 94%
Kuwait
Alkhalidi et al., 2009^Citation118	2003–2004	2,851, healthy adults	28.6% (816) • 18–27 y: 24.2% • 28–40 y: 51% • 41–60 y: 56.5%
Lebanon
Melhem et al., 2015^Citation104	2012–2013	283, blood donors	72% • 19–29 y: 60% • 30–39 y: 77% • 40–49 y: 94% • 50–59 y: 91%
Bizri et al., 2006^Citation102	1999–2000	902, school children, 14–18 y	71.3% (643)
Kalaajieh et al., 2000^Citation103	1996–1998	740, pediatric clinic pts, 0.5–15 y	29.3% (217) • 0.5–6 y: 14.7–21% • 7–15 y: 37.6–40.1%
Sacy et al., 2005^Citation105	1999–2000	606, healthy volunteers visiting or working in four hospitals, 1–30 y	43.2% (262) • 1–5 y: 10.5% • 6–10 y: 27.7% • 11–15 y: 57.4% • 16–20 y: 70.1% • 21–30 y: 78.1%
Shamma’a et al., 1982^Citation107	n.r.	772, mixed sample of pts	• Lebanese adults: 97.7% (474/485) • Pediatric group: 79.5% (136/171) • Foreign adults: 38.8% (45/116)
Libya
Gebreel et al., 1983^Citation135	1979–1981	400, school children, 3–18 y	60%–100%
Morocco
Bouskraoui et al., 2009^Citation136	2005–2006	150, children, 0.5-14 y	51% • ≤6 y: 45.2% • >6–14 y: 70.3%
Palestine
Yassin et al., 2001^Citation137	n.r.	396, school children, 6–14 y	93.7% • 6 y: 87.8% • 14 y: 97.5%
Pakistan
Aziz et al., 2007^Citation95	2002–2004	380, children from squatter settlements,<18 y	≥14 y: 100%
Agboatwalla et al., 1994^Citation94	1990–1991	258, healthy children (239) and adults (19)	55.8% (144) • <5 y: 41% (98/239) • 30–50 y: 100% (19/19)
Hamid et al., 2002^Citation96	n.r.	233, adult outpatients with CLD	• 97.8% (228)
Saudi Arabia
Alshabanat et al., 2013^Citation31	2006–2010	44,679, viral hepatitis pts, all ages	17% (7,566)
Al-Faleh et al., 2008^Citation21	2007–2008	1,357, school children, 16–18 y	18.6% (253)
El-Gilany et al., 2010^Citation39	2006–2007	950, children attending regular vaccination schedule, 1–6 y	33.8% (321)
Almuneff, et al., 2006^Citation29	2001–2005	4,006, healthcare workers	67%
Almuneef et al., 2006^Citation30	2005	2,399, all ages	28.9% (694) • <8 y: 7.1% • 8–11 y: 14.5% • 12–15 y: 30.6% • ≥16 y 52%
Jaber, 2006^Citation41	2004	527, aged 4–14 y	•28.7%
Al-Ghamdi et al., 2004^Citation26	2003	650, children − 1st year primary school	8.2% (53)
Fathalla et al., 2000^Citation40	1987–1999	11,674, healthy children and adults (18–50 y)	86% (10,029) • children: 65% • adults: 78.8% Detailed in children: • <6 y: 3% • 6–<8 y: 62% • 8–<10 y: 71% • 10–<12 y: 83% • 12–<18 y: 93%
Al-Faleh et al., 1999^Citation24	1997	5,355, community residents, children 1–12 y	25% (1,331) • 1–2 y: 16% • 3–4 y: 22% • 5–6 y: 25% • 7–8 y: 29% • 9–10 y: 34% • 11–12 y: 34%
Khalil et al., 1998^Citation42	1995–1996	592, children in regular appointments or inpatient care, <16 y	30.2% (179) • 0.5–2 y: 12.5% • 3–4 y: 14.7% • 5–6 y: 20.3% • 7–8 y: 40.4% • 9–10 y: 32% • 11–12 y: 44.3% • 13–15 y: 48.6%
Al Rashed, 1997^Citation23	1989	4,375, community residents, children, 1–10 y	52.4%
Ashraf et al., 1986^Citation35	1985	55, hemodialysis pts, all ages	100%
Ashraf et al., 1986^Citation36	1984–1985	395, healthy blood donors or minor illness pts, all ages	89% (353) • <0.5 y 65.5% • 0.5–2 y: 60% • 3–5 y: 83.3% • 6–12 y: 97.8% • >13 y: 100%
Babaeer et al., 2011^Citation38	n.r.	1,050, pts, >2 y	33.1% (348) • 2–5 y: 17% • 6–9 y: 21.1% • 10–14 y: 28.8% • 15–19 y: 27.2% • 20–24 y: 34.3% • 25–29 y: 38.2% • 30–34 y: 47.7% • >35 y: 49.2%
Al-Faleh et al., 2010^Citation22	n.r.	1,157, school children, 16–18 y	16.4% (190)
Arif, 1996^Citation33	n.r.	1,418, community residents, all ages	68.0% (964) 1–12 y: Riyadh, 24.7%; Gizan, 35.1% >13 y: Riyadh, 77.6%; Gizan, 90.9%
Ramia, 1986^Citation45	n.r.	1,015, Riyadh residents, all ages	82.5% (837) • <1 y: 67.9% • 1–4 y: 38.6% • 5–9 y: 61.3% • 10–15 y: 81.5% • 16–19 y: 83.5% • 20–29 y: 91% • 30–39 y: 93.5% • ≥40 y: 95%
Somalia
Hassan-Kadle et al., 2018^Citation121	[4 studies published from 1984 to1994]	Participants in the 4 studies, all ages	90.2% • <1 y: 61.5% • 1–10 y: 91.9% • 11–19 y: 96.3% • 20–39 y: 91.3% • ≥40 y: 87%
Bile et al., 1992^Citation122	n.r.	672, children in 2 residential institutions, <18 y	By institution: • 96% (Shebeli) • 59% (Societe Organization Sociale)
Mohamud et al., 1992^Citation123	n.r.	593, 0-83 y	•90%
Syria
Antaki et al., 2000^Citation128	n.r.	849, all ages	89% (754) • 1–5 y: 50% • 6–10 y: 81% • 11–15 y: 95% • 16–20 y: 94% • 21–30 y: 97% • 31–40 y: 98% • 41–50 y: 100%
Tunisia
Neffatti et al., 2017^Citation110	2014–2015	216 pregnant women, 19-46 y	98.6% (212)
Louati et al., 2009^Citation109	2000 & 2007	376 blood donors, 18–30 y		2000	2007
			18–20 y	91.9%	80.6%
			21–25 y	93.7%	84.9%
			>26 y	99.2%	92.1%
			Total	94.9%	85.9%
Rezig et al., 2008^Citation111	n.r.	2,482, community residents, children and young adults	87.9% (2,180) • 5- <10 y: 83.9% • 10–15: 90.5% • 16–25 y: 91.9%
Letaief et al., 2005^Citation108	2002	2,400, school children, 5–20 y	60% • 5–10 y: 44% • 10–15 y: 58% • 15–20 y: 83%
United Arab Emirates
Sheek-Hussein et al., 2012^Citation130	2011–2012	261, healthy medical students	21%
Sharar et al., 2008^Citation131	2004–2005	367 children attending hospital, 1–12 y	20.1% (74) • 1–6 y: 10.2% • 6–12 y: 31.5%
Yemen
Bawazir et al., 2010^Citation132	2005	538, pts attending hospitals, all ages	86.6% (466) • 0–1 y: 53% • <18 y: 80.8% • ≥18 y: 98.8%

CLD, chronic liver disease; HAV, hepatitis A virus; HBsAg, surface antigen of the hepatitis B virus; HIV, human immunodeficiency virus; IgG, immunoglobulin G; n, the number of study participants who were anti-HAV positive (* if available); n.r. not reported; pts, patients; y, year(s).

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