International Journal of Infectious Diseases
Volume 14, Issue 2 , Pages e115-e120, February 2010

Incidence trends of viral hepatitis A, B, and C seropositivity over eight years of surveillance in Saudi Arabia

  • Ziad A. Memish

      Affiliations

    • Department of Infection Prevention and Control, King Abdulaziz Medical City, PO Box 22490, Riyadh 11426, Saudi Arabia
    • Corresponding Author InformationCorresponding author. Tel.: +966 1 2520088x43720; fax: +966 1 2520437.
    • ,
  • Bandar Al Knawy

      Affiliations

    • Division of Gastroenterology/Hepatology, Department of Internal Medicine, King Abdulaziz Medical City, Riyadh, Saudi Arabia
    • ,
  • Aiman El-Saed

      Affiliations

    • Department of Infection Prevention and Control, King Abdulaziz Medical City, PO Box 22490, Riyadh 11426, Saudi Arabia

Received 15 February 2009; received in revised form 25 March 2009; accepted 29 March 2009. published online 22 June 2009.

Corresponding Editor: William Cameron, Ottawa, Canada

Article Outline

Summary 

Objectives

In Saudi Arabia, viral hepatitis ranked the second most common reportable viral disease in 2007, with almost 9000 new cases diagnosed in that year. The objective of this study was to determine the incidence trends of viral hepatitis seropositivity among the population served by the National Guard Health Affairs (NGHA) hospitals in the central, eastern, and western Saudi Arabia regions.

Methods

The surveillance system at King Abdulaziz Medical City in Riyadh receives weekly reports of laboratory confirmed hepatitis A virus (HAV), hepatitis B virus (HBV), and hepatitis C virus (HCV) cases from all NGHA-served regions. In this study the viral hepatitis surveillance data for the period from January 2000 through December 2007 were analyzed.

Results

Between 2000 and 2007, a total of 14 224 seropositive cases of viral hepatitis were reported to the surveillance system. The average annual incidence of seropositivity per 100 000 served population was highest for HBV (104.6), followed by HCV (78.4), and lowest for HAV (13.6). Saudis had higher HBV and HAV incidence, but lower HCV incidence compared to non-Saudis. Over the eight years (2000–2007), the incidence of all three viral hepatitis types showed a 20–30% declining trend. Only HAV incidence followed a clear seasonal cyclic pattern.

Conclusions

Despite the declining trend over the eight-year period, viral hepatitis, especially that caused by HBV and HCV, remains a major public health problem in Saudi Arabia, and has probably been underestimated in previous reports. There is a need for more comprehensive prevention strategies.

Keywords: Hepatitis, Viral, Incidence, Surveillance, Epidemiology, Saudi Arabia

 

Back to Article Outline

Introduction 

Viral hepatitis is caused by infection with any of at least five distinct viruses, of which hepatitis A virus (HAV), hepatitis B virus (HBV), and hepatitis C virus (HCV) are the three most commonly identified worldwide. This disease represents a major public health problem in Saudi Arabia. According to the Saudi Ministry of Health (MOH) data, viral hepatitis ranked the second most common reportable viral disease after chickenpox in 2007, with almost 9000 new cases diagnosed in that year (52% HBV, 32% HCV, and 16% HAV).1 In Saudi Arabia, HBV and HCV are major causes of disease requiring liver transplantation and of hepatocellular carcinoma, resulting in the need for considerable healthcare resources.2, 3, 4

The epidemiology of viral hepatitis in Saudi Arabia has undergone major changes, concurrent with major socioeconomic developments over the last two to three decades. Since the 1980s, Saudi Arabia has been known as a high HBV endemic area.5 However, starting in 1990, HBV vaccine has been administered to all Saudi infants/children.6 This has been associated with a reportable decline in hepatitis B surface antigen (HBsAg) seroprevalence, mainly in children.1, 6, 7, 8 HCV remains a major public health problem in Saudi Arabia, especially among certain high risk groups.9, 10 Moreover, the reported high rate of decline in HCV in some prevalence studies over the last decade9, 11 has not been confirmed in a recent large incidence report,12 nor in the Saudi MOH data.1 Recently, HAV vaccine has been added to the Saudi list of infant/childhood immunizations. Universal immunization against HAV in Saudi Arabia was recently recommended after a shift in the HAV epidemiology in the country, reducing it from a classic high endemic area to a low/moderate endemic area.13, 14

With few exceptions,6, 15 the published rates of viral hepatitis in Saudi Arabia have mainly been based on prevalence studies. While these studies may be good for measuring viral hepatitis burden, they have limited ability to measure the actual disease risk in the community or the effectiveness of immunization programs. These prevalence studies are typically retrospective, have small sample sizes, evaluate selected populations, or cover localized geographic areas. Together with the different methods used, these limitations may impede the ability to study temporal trends in viral hepatitis rates. The objective of the current study was to report the incidence trends of viral hepatitis seropositivity, using a standardized methodology, for the population served by the National Guard Health Affairs (NGHA) hospitals in different regions of Saudi Arabia between 2000 and 2007.

Back to Article Outline

Methods 

Four NGHA hospitals (approximately 2000 beds in total) and 73 primary care centers provide medical care for almost a million National Guard employees and their dependents (spouses, children, and parents) in the central, eastern, and western regions of Saudi Arabia. The population served by the NGHA (97% Saudi) represents about 4% of the total population of Saudi Arabia (23.7 million in 2006) and has an annual growth rate of 2.9%. The care provided by the NGHA hospitals and primary care centers ranges from primary and preventive care to tertiary care.

The Department of Infection Prevention and Control at King Abdulaziz Medical City (KAMC) in Riyadh, Saudi Arabia has a surveillance system that receives weekly reports of reportable infectious diseases, including viral hepatitis caused by HAV, HBV, and HCV, from all NGHA-served regions. The surveillance methodology used was consistent throughout the study period. A case was considered ‘suspected viral hepatitis’ if the World Health Organization (WHO)-recommended acute viral hepatitis clinical case definition was met.16 The case definition was considered met when there was an acute illness that typically included acute jaundice, dark urine, anorexia, malaise, extreme fatigue, and right upper quadrant tenderness. Only viral hepatitis cases that were laboratory confirmed, regardless of clinical signs and symptoms, were reported to the KAMC surveillance system. A case was considered to be HAV-positive if tests for anti-HAV immunoglobulin M (IgM) were positive, considered HBV-positive if tests for HBsAg were positive, and considered HCV-positive if tests for anti-HCV were positive, using ELISA. Seropositive cases of viral hepatitis were reported by laboratory personnel as part of intensive passive surveillance, which took place in multiple situations including the recruitment of new military or civilian employees, when medical care for a related condition was sought, during antenatal care (HBV only), in those attending hemodialysis units, in those undergoing organ transplantation or donating blood, or during the conducting of an outbreak investigation (mainly HAV).

For the purpose of this report, viral hepatitis surveillance data for the period from January 2000 through December 2007 were analyzed. Incidence trends refer to rates over time of newly diagnosed seropositive cases of viral hepatitis. The incidence rate for a specified type of viral hepatitis for a certain year and/or demographic group (gender, age group, nationality, or NGHA region of reporting) was calculated by dividing the number of reported seropositive cases for that type of viral hepatitis for that year and/or demographic group by the corresponding estimated NGHA-served population for that year and/or demographic group, then multiplied to give the rate per 100 000. The incidences over the eight years of surveillance (2000–2007) were plotted to detect any upward or downward trends. Duplicate cases (the same person reported more than one time with the same type of hepatitis) were not included in the analysis.

Epi Info software (version 6.04; CDC, Atlanta, GA, USA) was used to manage the surveillance database. Demographic characteristics including age, gender, nationality, and reporting NGHA region were compared between those with reported HAV, HBV, and HCV. Differences in incidence by demographic characteristics for each viral hepatitis type were examined. The Chi-square test was used to test for significant differences in categorical variables, while analysis of variance (ANOVA) or the Kruskal–Wallis test, as appropriate, were used to test for significant differences in continuous variables. All p-values were two-tailed. A p-value of <0.05 was considered as significant. SPSS software (version 15.0; SPSS Inc., Chicago, IL, USA) was used for all statistical analyses.

Back to Article Outline

Results 

During the eight years of surveillance (2000–2007), a total of 14 224 seropositive cases of viral hepatitis were reported to the KAMC surveillance system. HBV was the most frequent viral hepatitis type reported (n=7572, 53%), followed by HCV (n=5675, 40%) and HAV (n=981, 7%) (Table 1). The NGHA-served population ranged from about 816 000 in 2000 to 998 000 in 2007, with an average annual served population of 904 000 during the study period. The age of viral hepatitis cases was significantly different between the different viral types (p<0.001), with HAV in the youngest (11.0±10.5 years), followed by HBV (37.2±16.2 years), and HCV in the oldest (49.9±17.2 years) (Table 1). Those aged ≥15 years represented 18.1% of HAV cases, 97.9% of HBV cases, and 98.6% of HCV cases (Table 1). Gender, nationality, and reporting NGHA region were significantly different between the different types of viral hepatitis (p<0.001 for each). The majority of HBV and HAV, but not HCV cases, were male. The majority of hepatitis cases were reported in those of Saudi nationality, and the majority of cases were reported from the Central NGHA region (Table 1).

Table 1. Demographic characteristics of HAV, HBV, and HCV seropositive cases reported to the King Abdulaziz Medical City surveillance system between 2000 and 2007
HAVHBVHCVp-Valuea
Mode of yearly rank among reportable infectious diseases9th2nd3rdp<0.001b
Total number of cases98175725675p<0.001
Age, years (mean±SD)11.0±10.537.2±16.249.9±17.2p<0.001c

Cases by age group, n (%)
<15 years803 (81.9%)162 (2.1%)81 (1.4%)p<0.001
≥15 years178 (18.1%)7410 (97.9%)5594 (98.6%)

Cases by gender, n (%)
Males542 (55.2%)4540 (60.0%)2834 (49.9%)p<0.001
Females439 (44.8%)3032 (40.0%)2841 (50.1%)

Cases by nationality, n (%)
Saudi965 (98.4%)7394 (97.6%)5391 (95.0%)p<0.001
Non-Saudi16 (1.6%)182 (2.4%)284 (5.0%)

Cases by NGHA region, n (%)
Central584 (59.5%)4695 (62.0%)4118 (72.6%)p<0.001
Western222 (22.6%)2258 (29.8%)1153 (20.3%)
Eastern175 (17.8%)623 (8.2%)404 (7.1%)

HAV, hepatitis A virus; HBV, hepatitis B virus; HCV, hepatitis C virus; SD, standard deviation; NGHA, National Guard Health Affairs.

aTesting differences between viral hepatitis types using the Chi-square test unless stated otherwise.

bKruskal–Wallis test.

cANOVA (analysis of variance) test.

The average annual seropositivity incidence was highest for HBV (104.6 per 100 000), followed by HCV (78.4 per 100 000), and lowest for HAV (13.6 per 100 000) (Table 2). The eight-year (2000–2007) incidence trends (per 100 000) for HAV, HBV, and HCV seropositivity were studied (Figure 1, Figure 2, Figure 3). HAV incidence was almost 7-fold higher in those who were aged <15 years compared to those who were aged ≥15 years (annual average incidence of 27.9 vs. 4.1 per 100 000; p<0.001). HAV incidence was significantly higher in males than females, Saudis than non-Saudis, and in the central and eastern regions than the western region (Table 2). Over these eight years, the incidence of HAV seropositivity decreased by 30% (11.4 per 100 000 in 2000 vs. 8.0 per 100 000 in 2007; Figure 1). When the incidence was stratified by age group, HAV incidence decreased by 42% in those aged <15 years and increased by 61% in those aged ≥15 years. All age groups experienced a markedly increased HAV incidence in 2004 compared to 2003 (outbreak), which was cleared by 2007 in all age groups combined and in those who were <15 years old, but not in those who were aged ≥15 years (Figure 1). HAV incidence followed a seasonal cyclic pattern, with peaks in March and September (Figure 4).

Table 2. Average annual incidence of HAV, HBV, and HCV seropositivity per 100 000 NGHA-served population between 2000 and 2007 by demographic characteristicsa
HAVHBVHCV
Average annual incidence13.6104.678.4

Incidence by age group
<15 years27.95.62.8
≥15 years4.1169.8128.2
p<0.001p<0.001p<0.001

Incidence by gender
Males14.7123.076.8
Females12.485.580.1
p=0.008p<0.001p=0.110

Incidence by nationality
Saudi13.7105.376.8
Non-Saudi7.484.0130.7
p=0.012p=0.002p<0.001

Incidence by NGHA region
Central14.2113.899.8
Western11.4115.659.0
Eastern15.153.834.9
p=0.006p<0.001p<0.001

HAV, hepatitis A virus; HBV, hepatitis B virus; HCV, hepatitis C virus; NGHA, National Guard Health Affairs.

aTesting differences using the Chi-square test.

  • View full-size image.
  • Figure 4. 

    Seasonal variation in the incidence of seropositive cases of HAV, HBV, and HCV reported to the King Abdulaziz Medical City surveillance system between 2000 and 2007.

The incidence of HBV seropositivity was almost 30-fold higher in those who were aged ≥15 years compared to those who were <15 years (annual average incidence of 169.8 vs. 5.6 per 100 000; p<0.001). HBV incidence was significantly higher in males than females, Saudis than non-Saudis, and in central and western regions than the eastern region (Table 2). Between 2000 and 2007, HBV incidence decreased by 21% for all age groups combined (from 124.3 to 98.1 per 100 000), by 19% for those who were aged ≥15 years (from 195.9 to 158.7 per 100 000), and by 78% for those who were aged <15 years (from 16.7 to 3.6 per 100 000) (Figure 2). There was no clear seasonal variation in HBV incidence (Figure 4).

The incidence of HCV seropositivity was almost 45-fold higher in those who were aged ≥15 years compared to those who were aged <15 years (annual average incidence of 128.2 vs. 2.8 per 100 000; p<0.001). HCV incidence was similar in males and females, but higher in non-Saudis than Saudis and in the central region than in the other regions (Table 2). During the eight-year study period, HCV incidence decreased by 30% (from 98.0% to 68.4% per 100 000). The reduction was generally similar in those who were aged <15 and ≥15 years (23% and 31%, respectively (Figure 3)). There was no clear seasonal variation in HCV incidence (Figure 4).

Back to Article Outline

Discussion 

The current study reports for the first time, the eight-year incidence trends of HAV, HBV, and HCV seropositive viral hepatitis in a large population served by the NGHA hospitals in the central, eastern, and western regions of Saudi Arabia. The consistency of the surveillance methodology throughout the study period, including the diagnostic tests used, probably reduces the possibility of biased upward or downward trends. Between 2000 and 2007, the incidence of viral hepatitis seropositivity for all three virus types showed 20–30% declining trends. Similarly, a comprehensive review of prevalence studies of viral hepatitis conducted in Saudi Arabia in the 1980s and 1990s showed a more than 50% decline in all viral hepatitis types.8 The age group that included children <15 years was that which showed the greatest HBV incidence decline, probably due to the universal infant/child immunization program started in 1990 in Saudi Arabia.17 The modest HCV incidence reduction, which was similar in those aged <15 and ≥15 years, may be explained by the improved safety of blood products, strict infection control precautions for high risk medical services such as hemodialysis and dental services, enforcing premarital blood screening, and finally increased awareness of dangerous practices such as needle-sharing among drug abusers, cautery, and blood letting. The HAV incidence reduction was driven mainly by the decline in incidence in children aged <15 years who suffered the major part of the disease burden. This reduction may be attributed to the improvements in environmental sanitation that have accompanied major socioeconomic developments in Saudi Arabia over recent decades.13

Despite the declines in incidence, the current report confirms that seropositive viral hepatitis, especially that caused by HBV and HCV, remains a major public health problem in Saudi Arabia, and was probably underestimated by the national surveillance system. For example, when comparing the 2007 incidence from this study with the 2007 Saudi MOH data,1 the incidences of HBV and HCV were 5- to 6-fold higher in our study (98.1 vs. 18.6 per 100 000 for HBV and 68.4 vs. 11.7 per 100 000 for HCV). HAV incidence, on the other hand, was roughly similar (8.0 in our study vs. 5.7 per 100 000), and the 2004 HAV outbreak shown in this report was documented in the Saudi MOH data, at a lower magnitude though.1 Supporting our observation of national underestimation of HBV and HCV risk in Saudi Arabia, a recent report from the eastern region estimated the average annual incidence as 9.5 for HAV, 46.0 for HBV, and 37.7 for HCV per 100 000 population served by hospitals of the Saudi Aramco Medical Services Organization.15 Irrespective of the report used, the incidence of seropositive viral hepatitis in Saudi Arabia is remarkably higher than the incidence in the USA,18 which has one of the world's lowest rates, pointing to the scope of the problem in Saudi Arabia and the need for more comprehensive prevention strategies.

The higher incidence shown in this report may be due to the intensive passive surveillance undertaken in the well-defined NGHA population that occurred in multiple situations, including the recruitment of new military or civilian employees, when medical care for a related condition was sought, during antenatal care (HBV only), in those attending hemodialysis units, in those undergoing organ transplantation or donating blood, or during the conducting of an outbreak investigation (mainly HAV). This exhaustive surveillance may have detected more cases than would be expected from less intensive surveillance, especially as the laboratory-based diagnosis of HBV and HCV used in this and other reports, detects newly developed as well as previously undetected chronic cases. In addition, the incidence of seropositive viral hepatitis could actually be higher in the military population than in the rest of the Saudi population.19, 20, 21

The current report shows that HBV was the most frequent cause of viral hepatitis seropositivity, followed by HCV, and lastly by HAV. Supporting our findings, prevalence studies on Saudi blood donors over the last decade have shown higher HBV prevalence (1.5–2.6%) compared to HCV prevalence (0.4–1.1%).11, 22, 23 However, while the incidence of HAV seropositivity was the lowest among the three studied viral hepatitis types, prevalence studies have consistently shown HAV to be the most prevalent viral hepatitis type. HAV prevalence was recently estimated to be 29%,14 which is at least 50% lower than that reported a decade earlier.13, 24 This can be explained by the fact that the surveillance methodology used here and in other surveillance systems, frequently misses many asymptomatic and sporadic cases common in endemic areas. Interestingly, only HAV incidence followed a clear seasonal cyclic pattern, with peaks in March and September. A similar pattern has been described in other countries.25, 26 This may be related to more children being exposed during the mid-year, and summer vacations spent in more endemic areas abroad.

In conclusion, this report describes the incidence trends of seropositive viral hepatitis in a large population from different regions of Saudi Arabia. Over the last eight years, the incidences of all three types of viral hepatitis (caused by HAV, HBV, and HCV) have shown 20–30% declining trends. Nevertheless, the current report confirms that viral hepatitis, especially that caused by HBV and HCV, remains a major public health problem in Saudi Arabia, and has probably been underestimated in previous reports. There is a need for more comprehensive prevention strategies. It is probably going to take two to three decades before viral hepatitis prevalence reflects the full stable effect of any prevention programs. The effectiveness of such prevention programs can best be measured by incidence studies.

Conflict of interest: No conflict of interest to declare.

Back to Article Outline

References 

  1. Ministry of Health of Saudi Arabia. A review of health situation. The annual health statistics book. Saudi Arabia: Ministry of Health; 2007. Available at: http://www.moh.gov.sa/statistics/index.html.(accessed May 2009).
  2. Al-Sebayel M, Khalaf H, Al-Sofayan M, Al-Saghier M, Abdo A, Al-Bahili H, et al. Experience with 122 consecutive liver transplant procedures at King Faisal Specialist Hospital and Research Center. Ann Saudi Med. 2007;27:333–338
  3. Ayoola EA, Gadour MO. Hepatocellular carcinoma in Saudi Arabia: role of hepatitis B and C infection. J Gastroenterol Hepatol. 2004;19:665–669
  4. Mansoor I. Experience of liver disease at a University Hospital in Western Saudi Arabia. Saudi Med J. 2002;23:1070–1073
  5. Andre F, Hepatitis B. epidemiology in Asia, the Middle East and Africa. Vaccine. 2000;18(Suppl 1):S20–S22
  6. Madani TA. Trend in incidence of hepatitis B virus infection during a decade of universal childhood hepatitis B vaccination in Saudi Arabia. Trans R Soc Trop Med Hyg. 2007;101:278–283
  7. Ayoola AE, Tobaigy MS, Gadour MO, Ahmad BS, Hamza MK, Ageel AM. The decline of hepatitis B viral infection in southwestern Saudi Arabia. Saudi Med J. 2003;24:991–995
  8. Al-Faleh FZ. Changing pattern of hepatitis viral infection in Saudi Arabia in the last two decades. Ann Saudi Med. 2003;23:367–371
  9. Shobokshi OA, Serebour FE, Al-Drees AZ, Mitwalli AH, Qahtani A, Skakni LI. Hepatitis C virus seroprevalence rate among Saudis. Saudi Med J. 2003;24(Suppl 2):S81–S86
  10. Karkar A, Hepatitis C. in dialysis units: the Saudi experience. Hemodial Int. 2007;11:354–367
  11. Bashawri LA, Fawaz NA, Ahmad MS, Qadi AA, Almawi WY. Prevalence of seromarkers of HBV and HCV among blood donors in eastern Saudi Arabia, 1998-2001. Clin Lab Haematol. 2004;26:225–228
  12. Madani TA, Hepatitis C. virus infections reported in Saudi Arabia over 11 years of surveillance. Ann Saudi Med. 2007;27:191–194
  13. Tufenkeji H, Hepatitis A. shifting epidemiology in the Middle East and Africa. Vaccine. 2000;18(Suppl 1):S65–S67
  14. Almuneef MA, Memish ZA, Balkhy HH, Qahtani M, AlOtaibi B, Hajeer A, et al. Epidemiologic shift in the prevalence of hepatitis A virus in Saudi Arabia: a case for routine hepatitis A vaccination. Vaccine. 2006;24:5599–5603
  15. Al-Tawfiq JA, Anani A. Profile of viral hepatitis A, B, and C in a Saudi Arabian hospital. Med Sci Monit. 2008;14:CR52–CR56
  16. World Health Organization. Department of Vaccines and Biologicals. WHO-recommended standards for surveillance of selected vaccine-preventable diseases. Geneva: World Health Organization; 2003. Available at: http://www.who.int/vaccines-documents/DocsPDF06/843.pdf.(accessed May 2009).
  17. Al-Faleh FZ, Al-Jeffri M, Ramia S, Al-Rashed R, Arif M, Rezeig M, et al. Seroepidemiology of hepatitis B virus infection in Saudi children 8 years after a mass hepatitis B vaccination programme. J Infect. 1999;38:167–170
  18. Wasley A, Grytdal S, Gallagher K . Centers for Disease Control and Prevention. Surveillance for acute viral hepatitis—United States, 2006. MMWR Surveill Summ. 2008;57:1–24
  19. Bauduceau O, Berlioz A, Buisson Y. [Hepatitis B, C, and E in New Caledonia. Seroepidemiologic study in military recruits]. Med Trop (Mars). 2000;60:167–170
  20. Memish Z, Qasim L, Abed E, AlBasheer A, Aldraihim A, Knawy B, et al. Pattern of viral hepatitis infection in a selected population from Saudi Arabia. Mil Med. 2003;168:565–568
  21. Franco E, Giambi C, Ialacci R, Coppola RC, Zanetti AR. Risk groups for hepatitis A virus infection. Vaccine. 2003;21:2224–2233
  22. El-Hazmi MM. Prevalence of HBV, HCV, HIV-1, 2 and HTLV-I/II infections among blood donors in a teaching hospital in the central region of Saudi Arabia. Saudi Med J. 2004;25:26–33
  23. Mehdi SR, Pophali A, Al-Abdul Rahim KA. Prevalence of hepatitis B and C and blood donors. Saudi Med J. 2000;21:942–944
  24. Al Rashed RS. Prevalence of hepatitis A virus among Saudi Arabian children: a community-based study. Ann Saudi Med. 1997;17:200–203
  25. Suslov IM, Tkachenko GM, Kalenchuk AA, Astakhov AS. [Epidemiological analysis of hepatitis A morbidity]. Zh Mikrobiol Epidemiol Immunobiol. 1988;39–43
  26. Battikhi MN, Battikhi EG. The seroepidemiology of hepatitis A virus in Amman. Jordan. New Microbiol. 2004;27:215–220

PII: S1201-9712(09)00187-8

doi:10.1016/j.ijid.2009.03.027

International Journal of Infectious Diseases
Volume 14, Issue 2 , Pages e115-e120, February 2010

Article Tools

* Image Usage & Resolution