Hepatitis B Infection in Saudi Arabia
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1 Clinical Review Faleh Z. Al-Faleh, Facharzt From the Department of Medicine, College of Medicine, King Saud University, Riyadh. Address reprint requests and correspondence to Dr. Al-Faleh: Department of Medicine, College of Medicine, King Saud University, P.O. Box2925, Riyadh 11461, Saudi Arabia. Accepted for publication 2 May ABSTRACT This article on the hepatitis B virus (HBV) in Saudi Arabia reviews 24 articles on HBV which have been published in national and international journals. The data of 49,312 Saudi individuals have been analyzed. Some conclusions have been drawn about the prevalence of HBsAg and HBeAg, overall exposure of the population, and control of HBV infection. FZ Al-Faleh,. 1988; 8(6): MeSH KEYWORDS: Hepatitis B infection Hepatitis B virus (HBV) infection is one of the most common viral diseases in the world. Thanks to the serologic and immunologic tests which were developed following the discovery of HBsAg in 1964 by Blumberg et al, 1 a significant amount of data has accumulated in the world literature regarding the prevalence, the carrier state, the mode of transmission, and the mode of infection by HBV. Most of these data are related to the epidemiologic aspects of this infection and have highlighted several interesting differences in different populations. In Saudi Arabia, for the last 10 years, various studies of the hepatitis B surface antigen (HBsAg) prevalence have been conducted, and the results have been published both in national and international journals 2-14 (and M Al- Moagel, personal communication). A large amount of these data have been collected by analysis of blood drawn from blood donors and outpatient populations Recently, hepatitis B marker studies have also been published, 4,5,9,11 and comparison has been made in the HBsAg prevalence in different regions of Saudi Arabia. 8 This article is an attempt to review the data reported regarding the HBV infection in the Saudi population with the following objectives: (1) to present the current epidemiologic status of HBV in Saudi Arabia based on the already reported data; (2) to try to determine clues in the reported data regarding the routes of transmission of HBV in this part of the world and to try to compare local findings with the results reported from other countries; (3) to discuss the question of control strategy of HBV infection; and (4) to discuss recommendations for future studies. Current Epidemiologic Status of HBV in Saudi Arabia Table 1 shows the studies in the different areas which have been conducted and reported from Saudi Arabia. For simplicity, I have divided the studies according to three main geographic areas, namely, Central Province, Southwestern Province, and Eastern Province. To compare the three regions, the overall prevalence of HBsAg obtained by pooling samples from all reported studies is presented in Table 2. With the expected difference between males and females, studies giving no sex breakdown were not included in this table.
2 Table 1. HBsAg prevalence in different areas of Saudi Arabia. A total of 49,312 Saudi individuals have so far been screened for the HBV marker HBsAg. Most of these
3 individuals (33,632) belong to Riyadh in the Central Province of the country. The average overall prevalence of HBsAg in Saudi Arabia is estimated to be 8.3% (see Table 2), a figure which puts Saudi Arabia among the most highly endemic areas of HBV infection in the world. 23 Table 2 shows also the prevalence rate in the two sexes in different areas of Saudi Arabia. The available data confirm the male preponderance, 6,7,13 which agrees with the results reported from other parts of the world. The only exception is the study of El-Hazmi 8 in Gizan, where the prevalence of affected females is more than that of males. However, a more recent study in the same area by the same team (MAF El-Hazmi, personal communication) shows similar results to the study of Arya et al in Gizan. 7 If the results of only the male subjects are considered, it becomes obvious that the Southwestern Province and Eastern Province of Saudi Arabia can be classified as hyperendemic areas of the world. The HBV markers in addition to HBsAg, i.e., HBeAg, anti-hbs, and anti-hbc, have also been investigated in a few studies on Saudis. Table 3 shows the overall marker positivity rate in different areas of Saudi Arabia. These results demonstrate very interesting and important findings. It is clear from these results that the exposure ate of HBV infection ranges from 30% to 80% in different regions of Saudi Arabia, with an average of 50%. The highest exposure rate (i.e., 80%) is encountered in the Khaiber population. This exposure rate is very high and has significant implications to the transmission and the prevalence of hepatitis due to HBV infection. Table 2. Estimated prevalence of HBsAg in Saudi Arabia. Subjects Central Province Southwestern Province Eastern Province Total country* Males No. studied % HBsAg positive Females No. studied % HBsAg positive Total % HBsAg positive * Calculated as the weighted mean of the three provinces, using weighting proportional to population size 2:4:1 (Central Province: Southwestern Province: Eastern Province). Calculated as the mean of the male and female rates, weighted 1:1. Table 3. Overall marker positivity rate in different areas on different subjects. Study no. 1 Subjects Pregnant women, blood donors 2 Pregnant women, preschool children, blood donors No. of HBsAg subjects Sex positive (%) Method Area Reference 321 F 49.7 RIA Riyadh M F 38.7 ELISA Gizan M Outpatients 732 M 80.0 RIA Khaiber 8 10 M = 80.0 RIA Najran F F=72.0 RIA Riyadh Outpatients 145 ND* 51 RIA Al- 11 Hafouí Sickle cell trait 32 ND 50 RIA Al- 11 Hafouf Sickle cell disease 22 ND 28 RIA Al- 11 Hafouf 5 ß thalassemia 40 ND 75 RIA Riyadh 15 Sickle cell disease 54 ND 44 RIA Riyadh 15 Controls 120 ND 28 RIA Riyadh 15 Total 1291 F M 58.7 * Sex was not defined (ND).
4 The antigen HBeAg is closely related to the concentration of Dane particles in serum and is considered as an important marker of infectivity in a given population. The prevalence of HBeAg has been determined in several studies conducted in Saudi Arabia. Table 4 presents the HBeAg prevalence in different areas of Saudi Arabia. A slight difference is encountered in the population from different regions, and in patients with viral or bacterial serology the prevalence is as high as 26%. These results differ markedly from the findings reported from Taiwan and Korea where HBeAg in HBsAg-positive population ranges between 30% and 80%. 24 In addition, if we exclude the study of Waller et al, 25 which represents a very selected population (i.e., positive viral or bacterial serology), in all the other studies the HBeAg prevalence does not exceed 9%. 26 Certain populations, such as those receiving regular blood transfusions, patients on hemodialysis, patients with liver diseases and chronic active hepatitis, patients undergoing cholecystotomy, and preschool children born to HBsAg-positive mothers, are considered as the high-risk groups since they have a greater chance of acquiring HBsAg. In Saudi Arabia, several studies have reported the prevalence of HBsAg in high-risk populations. In Table 5 the HBsAg prevalence in the high-risk populations is summarized. The most interesting figures are those of the association of HBV infection and liver diseases. Transmission Route of HBV Infection in Saudi Arabia Several studies in Saudi Arabia have tried to study the transmission route of HBV infection. 2,4,7,16 They have all demonstrated that perinatal transmission is unlikely, or at least its role is minimal. It has now been proved, beyond any doubt, that HBV is transmitted by several routes in both the developed and less developed world. Infection acquired through close personal contact is far more common than that acquired through needles or transfusions. 29 In animal experiments, it has been shown that, besides blood and blood products, saliva, semen, and urine can transmit the infection. 26,30 Francis et al 29 reviewed the literature about the epidemiologic pattern of HBV transmission. They concluded that in countries of Asia and sub-sahara Africa, HBV infection occurs commonly early in life, but the mode of transmission is different. While in Taiwan, Korea, and Japan, perinatal transmission is the most common route following the high rate of HBeAg positivity, in Africa, horizontal transmission seems to be the dominant route. The low HBeAg positivity of HBsAg-positive mothers here in Saudi Arabia, the low HBsAg positivity of infants under 1 year of age, and the rapid increase of HBV infection between 1 and 12 years old 4,5 speak more for horizontal transmission of HBV infection. Al-Admawy et al 4 showed in their study of HBsAg acquisition in Riyadh that it was significantly greater in children up to 5 years old than in older children and adults. Fathalla et al 5 showed in their study of 168 preschool Saudi children born to HBsAg-positive mothers that acquisition of infection increased rapidly between the ages of 10 weeks and 5 years from 3.6% to 14.6%. The question arises as to what happens to these age groups to make them more susceptible to HBV infection. Francis et al 29 have suggested that serum-sharing associated with close personal contact and oozing from dermatologic lesions occurring during early childhood are the most common modes of HBV transmission in hyperendemic settings. However, in addition to this factor, I think in Saudi Arabia the folk medicine practices, the large families and joint family system, low standards of hygiene among the population, and the common habit to have infants and children kissed by everyone are factors which have contributed to increased prevalence of HBV infection. Saliva, urine, and blood could be involved in this transmission. On the other hand, Talukder et al 3 and Arya et al 7 have produced evidence that in Saudi Arabia there are two peaks for HBV exposure. One is in infancy and early childhood and the other is around 30 years of age. The second peak could be attributed to heterosexual transmission (marriage age in Saudi Arabia begins normally around the age of 17 years) in addition to the abovementioned factors. Study no. Table 4. Prevalence of HBsAg in different areas at different subjects. HBsAg positive (%) Method Area Reference Subjects No. of subjects Sex 1 Inpatients 44 ND* 9 RIA Referred patient to KFSH 2 Blood donors, pregnant women, preschool children 45 ND 9 ELISA Gizan 7 17
5 3 Blood from patients 200 ND 26 RIA Riyadh 24 who had viral or bacterial serology study 4 Pregnant women 139/4890 F 8 ELISA Jeddah 16 * Sex was not defined (ND). Study no. Subjects 1 Liver diseases Table 5. HBsAg prevalence in different areas of Saudi Arabia in a high-risk population. No. of subjects Sex HBsAg positive (%) Method Area Reference Suspected of liver disease 70 M 28.6 RPHA Riyadh 6,13 F 9.0 Chronic active hepatitis 69 M 55.0 RIA Riyadh F 42.0 Patients undergoing cholecystotomy 90 M 44.4 ELISA Riyadh F Hemoglobinopathies Sickle cell trait 32 ND* 9.37 RIA Al-Hafouf 11 Sickle cell disease 22 ND 4.54 RIA Al-Hafouf 11 ß-thalassemia 40 ND 13.0 RIA Riyadh 15 Sickle cell disease 54 ND 6.0 RIA Riyadh 15 3 Hemodialysis patients 120 ND 8.3 RPHA Riyadh M Al-Moagel, personal communication 4 Preschool Saudi children (0 5 years) born to HBsAg- positive mothers * Sex was not defined (ND). 168 ND 8.3 RIA Eastern Province Strategy for HBV Infection Control It is very alarming to have a nationwide carrier rate of 8.3% which reaches almost 10% in the Southwestern Province. In a population of 10 million persons, this means that about 800,000 are affected by HBV. The correlation between hepatocellular carcinoma and HBV is well documented. 25 In high incidence areas (such as China and Japan), 35% to 40% of patients with hepatocellular carcinoma have evidence of HBV infection. The relative risk to develop hepatocellular carcinoma has been calculated for 22,707 male government employees of Taiwan and found be 223 times greater in HBsAg carriers. However, an updated study has calculated the risk to 104 times. 31,32 We now increasingly see in hospital settings cases of cirrhosis and hepatocellular carcinoma in advanced stages. The relation of the early HBV infection and development of hepatocellular carcinoma has been stressed. 33 Therefore, the only hope to decrease this morbidity and mortality for the new generation is the vaccine. Its efficacy has been established worldwide. The question is when should the vaccine be administered and to whom? As we have seen in reviewing the reported data, it seems that in Saudi Arabia we are dealing mostly with the horizontal transmission route. The infection, as we have mentioned before, seems to occur here in two peaks. The first is early childhood starting from the first year. A large-scale program for HBV vaccination should be integrated with other vaccination programs which usually start at the age of 3 months. All children should be given the vaccine so that at the age of 1 to 1½ years, the program is completed; a booster dose should be given after 5 years. 23,34-36 For the adult peak, the control program should include mandatory screening of blood donors and promoting good hygiene by more public education. Selected risk groups should be identified and vaccinated and so should their close contacts. 5
6 Recommendations for Future Studies After reviewing all these data, I think there is no need for further large-scale studies of the prevalence of HBsAg in most areas of Saudi Arabia. However, one should still evaluate data coming from areas of Saudi Arabia which have not yet been screened. The screening of blood donors, a procedure already practiced in all of the hospitals in Saudi Arabia, will fulfill this objective. Further studies should concentrate on the high-risk population and children to determine further evidence for the mode of transmission of HBV and eventually to identify the risk factors leading to increased infection. In addition, there should be studies to determine efficacy of the vaccine in the Saudi population, especially in infants and the high-risk population. References 1. Blumberg GS, Alter HJ, Visnich S. A "new" antigen in leukemia sera. JAMA 1965;191; Ramia S, Abdul-Jabbar F, Bakir TM, Hossain A. Vertical transmission of hepatitis B surface antigen in Saudi Arabia. Ann Trop Paediatr 1984;4(4): Talukder MA, Gilmore R, Bacchus RA. Prevalence of hepatitis B surface antigen among male Saudi Arabians. J Infect Dis 1982;146(3): Al-Admawy AM, Talukder MA, Gilmore R. Prevalence and acquisition rates of hepatitis BsAg in Riyadh Al-Kharj Hospital Programme. Saudi Med J 1987;8(2): Fathalla SS, Namnyak SS, Al-Jama AA, Rabaria-Bautista MM. The prevalence of HBsAg in healthy subjects residing in the Eastern Province of Saudi Arabia. Saudi Med J 1985;6(3): Jamjoom GA, Ramia S, Bakir T, et al. A two-year survey of diagnostic virus laboratory services of King Saud University Hospitals, Riyadh. Saudi Med J 1986;7(2): Arya SC, Ashraf SJ, Parande CM, et al. Hepatitis B virus in Gizan, Saudi Arabia. J Med Virol 1985; 17(3): EL-Hazmi MAF. Hepatitis B markers in Saudi Arabia: a comparative study in different regions. Ann Saudi Med 1986;6(3): El-Hazmi MAF, Al-Faleh FZ, Warsy AS. Epidemiology of viral hepatitis among the Saudi population: 1. A study of viral markers in Khaiber. Saudi Med J 1986;7(2): El-Hazmi MA, Ramia S. Epidemiology of delta agent infection in Arabia: geographical distribution and prevalence of antidelta. Vox Sang 1986,50(4): Al-Faleh FZ. Prevalence of viral hepatitis markers in patients with sickle cell gene. Ann Saudi Med 1987;7(2): Takieddine FN, Tufenkeji HT, Sheth KV, Ghandour MH. Prevalence of HBV markers in adult Saudis in relation to age and sex. Ann Saudi Med 1986;6(3): Jamjoom GA, Higham R. Prevalence of viral hepatitis type B surface antigen (HBsAg) in patients with liver disease and in the general patient population at King Abdul Aziz Hospital, Riyadh. Proceedings of the 5th Saudi medical meeting, Riyadh, 1980: Ramia S, Hossain A, Bakir TM, et al. Prevalence and subtype of hepatitis B surface antigen (HBsAg) in the Saudi population. Trop Geogr Med 1986;38(1): Babiker MA, Bahakim HM, El-Hazmi MA. Hepatitis B and A markers in children with thalassaemia and sickle-cell disease in Riyadh. Ann Trop Paediatr 1986;6(1): Basalamah AH, Serebour FE, Kazim I. Hepatitis B prevention in Saudi Arabia. Proceedings of the 8th Saudi medical meeting, Riyadh, Sheth KV, Godwin JT. Hepatitis B serological markers in Saudi Arabian patient population and their implications for health care workers. Ann Saudi Med 1986;6(2): Habayeb S. Twenty-five months' epidemiological observations at King Faisal Military Hospital, Khamis Mushayt. Saudi Med J 1982;3(l): Habayeb SJ. Hepatitis B vaccination (letter to the editor). Saudi Med J 1984;5(2): Abdurrahman MB. Hepatitis B infection and immunization: a review. Saudi Med J 1984;5(4): Laajam MA, Al-Mofleh IA, Al-Faleh FZ, et al. Upper gastrointestinal endoscopy in Saudi Arabia: analysis of 6386 procedures. Q J Med 1988;66(249):21-5.
7 22. Shobokshi O, Serebour F. Hepatitis B: a Saudi Arabian problem. Abstracts of the 5th Saudi medical meeting, Riyadh, Chopra S. Acute viral hepatitis. American Gastroenterology Association meet the professor annual meeting, 19 May 1986, San Francisco. 24. Arthur MJ, Hall AJ, Wright R. Hepatitis B, hepatocellular carcinoma, and strategies for prevention. Lancet 1984;1(8377): Waller DK, Nixon P, Talukder MAS, Al-Admawy AMO. A survey of the prevalence of "e" antigen infectivity marker in HBsAg positive hospital patients. Saudi Med J 1984;5(2): Karayiannis P, Novick DM, Lok AS, et al. Hepatitis B virus DNA in saliva, urine, and seminal fluid of carriers of hepatitis B e antigen. Br Med J 1985;290(6485): Kingston ME, Ali MA, Atiyeh M, Donnelly RJ. Diagnosis of chronic active hepatitis: a review of 100 cases. King Faisal Spec Hosp Med J 1984;4(1): Mofti AB, Al-Tameem MM, Al-Khudairy NN, et al Experience with elective cholecystectomy in King Khalid University Hospital. Ann Saudi Med 1987;7(2): Francis DP, Favero MS, Maynard JE. Transmission of hepatitis B virus. Semin Liver Dis 1981;1(1): Galambos JT. Transmission of hepatitis B from providers to patients: how big is the risk? Hepatology 1986;6(2): Bassendine MF. Aetiological factors in hepatocellular cancer. Baillieres Clin Gastroenterol 1987;1(1): Beasley RP, Hwang LY, Lin CC, Chien CS. Hepatocellular carcinoma and hepatitis B virus: a prospective study of 22,707 men in Taiwan. Lancet 1981;2(8256): Zuckerman AJ, Harrison TJ. Hepatitis B virus chronic liver disease and hepatocellular carcinoma. Postgrad Med J 1987;63(suppl 2): Koretz RL. Hepatitis: serious papers, funny papers. In: Gitnick G, ed. Current hepatology. 6th vol. Chicago: Year Book Medical Publishers, 1986;6-7, Filg W. Die aktive Schutzimpfung gegen Hepatitis B Internist 1985;26: Little PJ. Hepatitis B vaccination. Saudi Med J 1983;4(1):1-4.
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