Hepatitis B and C in Juba, southern Sudan: results of a serosurvey

534 TRANSACTIONS

Hepatitis

OF ~ME

ROYAL SOCIETY OF TROPICAL MEDICINE AND HYGIENE (1994) 88, 534-536

B and C in Juba, southern

Sudan:

results of a serosurvey

Michael C. McCarthy’, Ahmed El-Tigani*, Ismail 0. KhalidZ and Kenneth C. Hyams3 LUS NavaZ Medical Research Unit No. 3, Cairo, &ypt; USA

2Ministty of Health, Khartoum, Sudan; 3Naval Medical Research Institute, Bethesda, Maryland,

Abstract To compare the epidemiology of hepatitis B virus (HEW) with hepatitis C virus (HCV) in a southern Sudanesepopulation, 666 out-patients attending 6 public clinics in the city of Juba were enrolled in a serosurvey. The average age of subjects was 16 years; 54% were female. Of the 651 samples tested for hepatitis 3 markers, HBsAg was found in 26% and anti-HBc in 67%. In contrast, only 2 1 (3%) of the 666 sampleswere positive for anti-HCV using a second generation immunoblot assay(RtBA-2). Seventeen(81%) of the 21 antiHCV-positive subjects were positive for anti-HBc, compared to 66% (418/630) of subjects negative for antiHCV (P=OeO7), None of the anti-HCV-positive subjects reported receiving a prior blood transfusion and only 5 subjects reported a history of jaundice. Nine of the 21 (43%) anti-HCV-positive subjects reported a history of scarification, compared to 23% (1481645)of anri-HCV-negative subjects (P=O,Ol). Hepatitis B infection was also associatedwith scarification by univariate analysis. However, after adjustment for age a history of scarification was not significantly associatedwith hepatitis C infection, but it was with HBV infection (odds ratio= l-5,, 95% CI l-O-2.5; P=O.O5). The findings of this study indicate that HCV infection is not highly endemic m this population and that the epidemiology of HCV differs from that of HBV. Introduction There is limited information about the epidemiology of infectious diseasesin southern Sudan, where a civil war spanning 3 decadeshas resulted in isolation and extreme novertv (FRAME. 1968: AHMED et al.. 1984). This region; bord&ing Kenya, Uganda and Zaire; is inhabited by several Nilotic tribes which are culturally distinct from those of northern Sudan. Typically, the population leads an agrarian life-style and the extended family lives in a cluster of mud huts. As a consequence of local customs and social conditions, the inhabitants of southern Sudan are at high risk for avariety of parenterally and sexual1 transmitted diseases.The traditions of scarification anB tattooing, which confer symbols of tribal distinction and sexual maturity, are still commonly practised. Also, dental extractions and artial tonsillectomy using crude instruments are perPormed at early ages for therapeutic purposes (WOODRUFF et al., 1983). Disposable needles and syringes are commonly re-used because of frequent shorta es of medical supplies, and surgical instruments are o$ten inadeauatelv sterilized due to a lack of electricitv. Many women are forced into prostitution becauseof poverty, and sexual contact with prostitutes is common among adult men. The objectives of this study were to determine the prevalence of antibodies to hepatitis B virus (HBV) and hepatitis C virus (HCV) in a southern Sudanesepopulation and to evaluate the risk factors associatedwith HBV and HCV seropositivity. Materials and Methods The study was conducted in the city of Juba, southern Sudan. During one week in June 1989, all patients attending 6 public health clinics were invited to participate in thesrrveg In. order to evaluate viral hepatitis infection. which earns at an earlv age in this region (HYAMS er al:, 1989), thi clinics selecied-for this stu& were those serving predominantly paediatric and adolescent patients. Informed consent was obtained from all subjects or their parents and institutional guide-lines for the protection of human subjects were followed. An epidemiological questionnaire was completed for all subjects and a venous blood sample was obtained. Questionnaires were administered by trained Sudanese Ministry of Health personnel fluent in local dialects. For paediatric subjects, responsesto questions were provided by an accompanying parent. Demographic information and any history of jaundice were elicited from all participants. Subjects were also questioned about potential risk Address for correspondence: Michael C. McCarthy, M.D., 1755 Park Road NW, Washington, DC 20010, USA.

factors for HBV and HCV transmission, including any history of blood transfusion, surgery, hospital admission, dental extraction, parenteral therapy for malaria or schistosomiasis, scarification, or tattooing. Additionally, interviewers were permitted to question study subjects over the age of 16 years about any previous sexually transmitted diseases (STDs), parenteral injections for STDs. and a historv of sexual relations with prostitutes. All sera were rested for the presence of antibody to HCV (anti-HCV) using a first generation enzyme-linked immunosorbent assay(ELISA) (Chiron Corporation, Emervville. California. USA). Sera that were repeatedlv reactive were then tested using a second eneraiion 4-a&tigen immunoblotting assay (RIBA- HCV 8 , Ortho Diagnostic Systems,New Jersey, USA). Sampleswith sufficient sera were also tested for the presence of total hepatitis B core antibody (anti-HBc) and hepatitis B surface antigen (HBsAg) using commercial enzyme immunoassay test kits (Abbott Laboratories, Abbott Park, Illinois, USA). Statistical analyses were performed using the SPSS/PC+software packages (SPSS Inc., Chicago, Illinois, USA). Proportions were compared using the ~2 test with Yates’s correction and Fisher s exact test. Comparisons of means (reported as -i-1 standard deviation) were made using Student’s t test. Significance was determined at the 0*05% probability level in all analyses. Separate multipIe logistic regression models were constructed with serological results for anti-HCV (RIBA- data), HBsAg and anti-HBc as the outcome variables. A backward, stepwise procedure was used to determine independent uredictors of HBV and HCV infections. and lirst-order mteraction was evaluated in all final mddels. For multivariate analysis, odds ratios (OR) and 95% confidence intervais (Cl) were reported for significant (P
53s

mission and frequent chronic HBV infection has been reported in studies from other developing countries (JACRanti-H& __---.-

F’ ,,’

I 40% t

/’

_’

,’ HBsAg

prevalenceof hepatitis B and C markers in Juba, Sudan.Numbersin parentheses(n) shownumbersof personstestedfor hepatitisC virus (HCV) markers;2%werenottestedfor hepatitisB.

Figure. Age-specific

among men compared to women (30% vs. 23%). By multivariate analysis, age (OR=l.O4, 95% CI 1.02-1.06; P
SON et al., 1991; SAEED er al., 1991; HYAMS et nl., 1992; WATTS et al., 1994), and suggeststhat the epidemiology

of HBV and HCV are substantially different in this region of Africa. By multivariate analysis, ritual scarification and age were found to be independently predictive of hepatitis B infection. This finding is consistent with orior studies which indicated that practices which pieice the skin using potentially contaminated instruments, such as scarification and tattooing. are associatedwith HBV infection in the Sudan (I&AMS et al., 1989). Since the practice of scarification is commonly performed during the early years of life, changes in the frequency of exposure to this risk factor may be one possible intervention for the prevention of HBV transmission. The lack of an association between markers of HBV infection and sexual contact with prostitutes or a history of STDs was an unexpected finding in this study. Sexual transmission of HBV has been reported from northern Sudan (MCCARTHY et al,, 1989a, 1989b). One possible explanation for this findmg may be the very high rate of HBV transmission before the advent of sexual activity. While the findings of this serosurvey suggest that HCV infection is not endemic in this population,, its true prevalence may have been underestimated since the study was focused on such a young population. Similarly, if antibodies to HCV are not always detectable or do not persist, as has been suggested 6y other studies (ALTER et al., 1989: AACH et d..

1991: YUKI et al..

i993), the tr& risk ‘of HCV infection &ay have bee; underestimated in this study. Although the small number of anti-HCV positive subjects found in this study limited the analysis of potential risk factors, the data do indicate that the e idemiology of HCV in Sudan is different from that of H !I V. Except for [he suggestion that HCV, like HBV, may be acquired through the practice of scarification, there appears to be substantially less HCV transmission than HBV infection in this African population. Much more investigation is needed to clarify the epidemiology of HCV in developing African countries. Prospective studies are needed to evaluate the true incidence of HCV infection and to assessrisk factors for its transmission. Acknowledgement

This researchwas supportedby rhe US Naval Researchand DevelopmentCommand, NMC, NCR, Bethesda, Maryland, work unit nos. 3M162770A870AR122 and 3M463105H29.

AA.335.

Disclaimer

The opinions and assertionscontainedherein are the rivate

ones of the authors and are not to be construed as officta T or re-

fleeting the viewsof the US Departmentof rhe Navy, the Department of Defense, or the SudaneseMinistry of Health. References

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Ahmed, S. A., Sanyal, R. K., Scedrou, P. & Ahmed, Md

(1984).HepatitisB surfaceantigenin south Sudan.Journal of

Communicable &senses, 16, 330-33 1. Alter, H. J., Purcell, R. H., Shih, J. W., Melpolder, J. C., Houghton, M., Choo, Q.-L. & Kuo, G. (1989). Detection of antibody to hepatitis C virus in prospectivelyfollowed transfusion recipients with acure and chronic non-A, non-B hepatitis. New EnglandJounzal of Medicine, 22,1494-1500. Frame, J. D. (1968). Hepatitis among missionaries in Ethiopia and Sudan.Journal ofAmerican Medicine, 203,99-107. Hyams, K. C.,, Al-Arabi, M. A., Al-Tigant, A. A., Messiter, J. F., Al-Gash, A. A. & George, J. F. (1989). Epidemiology of hepatitis B in the Gezira region of Sudan. American~~aurmal of Troptcal Medicine and Hygiene, 40,2O(J-206.

536 Hyams,K. C., Phillips, I. A., Moran, A. Y., Tejada, A., Wig-

nall, F. S. % Escamilla, J. (1992). Seroprevalence of hepatitis C anribod in Peru.Joumat ofMedical Virology, 3?,127-132. Jackson, J. B Guay, L., Goldfarb, J., Olness, K., Ngugwas, C., Mmiro,‘)F., Kataaha, F. & Allain, J. P. (1991). Hepatitis C$uantibody in HIV-l infected Ugandan mothers. Lancet,

McCaithy,‘M. C., Hyams, K. C.) El-Tiganni, A. A., El-Dabi, M. A., Ef-Tayeb, M. S., Khahd, 1. O., George, J, F., Constantine, N. T. & Woody, J. N. (1989a). HIV-l and hepatitis B transmission in Sudan. AIDS, 3,725-729. McCarthy, M. C., Burans, J. P., Constantine, N. T., EI-Tiganni, A. A., El-Tayeb, M. S., El-Dabi, M. A., Fahkry, J. G., Woody, J. N. & Hyams, K. C. (1989b). Hepatitis B and HIV in Sudan: a serosurvt far hepatitis B and human immunodeficiency virus anribo %es among sexually active heterosexuals. American Journal of Tropical Medicine and Hygiene, 41,72&731.

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TRANSACTIONS OF THE ROYAL SOCIETY OF TROPICAL MEDICINE AND HYGIENE (1994) 88, 536

;ShortReport Hepatitis C virus antibodies prostitutes in Niger

in

Michel Develouxl, Daniel Meynardl, Alain Dupontl and Eric DelaporteZ IH&tal National, B.P. 11436, Niumey, Niger; 2INSERM lJ13IIMEA, 190 Boulevard MacDonald 75019 Paris, France In developed countries hepatiris C virus (HCV) infection is transmitted mainly parenterally. The importance of sexual transmission is still controversial but is generally considered to be very low in developed countries (BRESTERS et al., 1993; OSMOND et al., 1993). In Gabon a high HCV prevalence rate (9%) has been reported in the general population; blood transfusion and parenteral exposure were not risk factors for HCV infection, suggesting that the epidemiology of HCV could be different in Africa (DELAPORTE et al., 1993). In a previous report from Niger, we showed that the prevalence of HCV in pregnant women and blood donors was zero and 0.5% respectively (DEVELOUX et al., 1992). In order to determine whether populations with high risk sexual behaviour are a hi h risk group for HCV infection we studied a group oB 250 female prostitutes in Niamey, Ni er, in 1990; a blood sample was collected from each 4 ter informed consent. For screening purpose a sandwich enzyme-linked immunosorbent assay was used (Innotest HCV AB@, Innogenetic NV, Antwerp, Belgium). This test uses microwells coated with specific HCV antigens: 2 epitopes of non-structural proteins (NS4 and NS5) and 4 epitopes of structural proteins (Cl, C2, C3, C4). Positive sera were tested for confirmation using a line immunoassay (Inno-LIA HCV Ab@, Innogenetics NV), which consists of nylon strips coated with the 6 synthetic peptides mentioned above. A serum reacAddress for correspondence: Eric Delaporte, Bd Macdonald, 75019 Paris,France.

INSERM

U13, 190

tive to at least one peptide was considered positive. Among the 250 prostitutes, 19 (76st 3.3) had antibodies to HCV. In this population the HIV prevalence was 29.2%, whereas in pregnant women and blood donors the human immunodeficiency virus (HIV) prevalence was less than 1%. In the prostitutes, HCV and HIV infection were significantly associated(x2=42.45, P
Bresters, D., Mauser-Bunschoten, E. I’., Reesink, H. W., Roosendaal, G., van der Poel, C. L., Chalumeau, R., Janser, P., Weegink, C. J., Cuypers, H. T., Lelie, P. N. & van den Berg, H. M. (1993). Sexual transmission of hepatitis C virus. Lancet, 342,21C-211. Delaporte, E., Thiers, V., Dazza, M. C., Romeo,R., Mlika-Cabanne, N., A tel, I.., Schrijvers, D., B&hot, C. & Larouzb, B. (1983). High level of hepatitis C endemicity in Gabon, equatorial Africa. Trfinsackons of the Royat Society of Tropical Medicine and Hygiene, 87,636637. Develoux, +, Meynard, D. & Delaporte, E. (1992). Low rate of hepatms C virus antibodies in blood donors and pregnant women from Ni er. l’runsactionsof the Royat Socieryof Tropical Medicine and”Hygrene, 86,553. Osmond, D. H., Padian, N., Sheppard, H. W., Glas, S., Shiboshi, S. C. & Reingold, A. (1993). Risk factors for he atitis C virus seropositivity in heterosexual couples. 3ourna Pof the American MedicalAssociation,

269,361-365.

Received 7 February 1994; revised31 May 1994; accepted

for publication 31 May 1994