Outbreak of viral hepatitis B in a rural community in India linked to inadequately sterilized needles and syringes.

Outbreak of viral hepatitis B in a rural community in India linked to inadequately sterilized needles and syringes J. Singh,1 R. Bhatia,2 J.C. Gandhi,3 A.P. Kaswekar,4 S. Khare,5 S.B. Patel,6 V.B. Oza7 D.C. Jain,8 & J. Sokhey9 In India, virtually all outbreaks of viral hepatitis are considered to be due to faeco-orally transmitted hepatitis E virus. Recently, a cluster of 15 cases of viral hepatitis B was found in three villages in Gujarat State. The cases were epidemiologically linked to the use of inadequately sterilized needles and syringes by a local unqualified medical practitioner. The outbreak evolved slowly over a period of 3 months and was marked by a high case fatality rate (46.7%), probably because of concurrent infection with hepatitis D virus (HDV) or sexually transmitted infections. But for the many fatalities within 2-3 weeks of the onset of illness, the outbreak would have gone unnoticed. The findings emphasize the importance of inadequately sterilized needles and syringes in the trans- mission of viral hepatitis B in India, the need to strengthen the routine surveillance system, and to organize an education campaign targeting all health care workers including private practitioners, especially those working in rural areas, as well as the public at large, to take all possible measures to prevent this often fatal infection. Introduction In India, virtually all outbreaks of viral hepatitis are considered to be due to faeco-orally transmitted hepatitis non-A, non-B virus (HEV) (1-3). Out- breaks of viral hepatitis A have also been reported occasionally (1). In contrast, although there has been a sudden increase in cases of viral hepatitis B admitted to hospitals (4, 5), no outbreaks have been reported in the community setting in India. I Deputy Director, National Institute of Communicable Diseases (NICD), 22 Shamnath Marg, Dehli-110054, India. Requests for reprints should be sent to Dr Singh at this address. 2 Consultant (Microbiology), NICD, Delhi, India. 3Joint Director, Commissionerate of Health, Medical Services, and Medical Education, Government of Gujarat, Gandhinagar, India. 4Regional Deputy Director, Commissionerate of Health, Medical Services, and Medical Education, Government of Gujarat, Gandhinagar, India. 5Joint Director, NICD, Delhi, India. 6 Epidemiologist, Commissionerate of Health, Medical Services, and Medical Education, Government of Gujarat, Gandhinagar, India. 7Epidemic Medical Officer, Commissionerate of Health, Medical Services, and Medical Education, Government of Gujarat, Gandhinagar, India. 8 Joint Director, NICD, Delhi, India. 9 Director, NICD, Delhi, India. Reprint No. 5826 However, an unusual clustering of cases of viral hepatitis B was recently observed in rural areas of Mehasana district, Gujarat State, India. In this article, we describe the epidemiological importance of this outbreak. The outbreak was centred in three villages (Khata-Amba, Parsa, and Charadu), especially in Khata-Amba. Most of the population in the affected villages is engaged in occupations related to agricul- ture. Many people from Khata-Amba, including some of the patients, worked in nearby towns such as Surat and Ahmedabad, but came to the village every year around the time of Diwali (which in 1996 was on 10 November) to celebrate this festival. The district health authorities learned on 13 January 1997 that an adult male, who was a resident of Khata-Amba, had died from viral hepatitis on 7 January 1997. Many more cases were identified in a subsequent house-to-house survey in this village and in Parsa and Charadu. Since blood samples taken from patients were positive for hepatitis B surface antigen (HBsAg), the episode was investigated systematically. Materials and methods The age, sex, education level, occupation, place of work, date of onset of illness, signs and symptoms, and results of laboratory investigations were deter- Bulletin of the World Health Organization, 1998, 76 (1): 93-98 © World Health Organization 1998 93 J. Singh et al. mined for all the surviving patients. The patients, their family members, or doctors who had treated them were also interviewed in order to identify any of the following risk factors for viral hepatitis B that may have been present from 6 months up to 15 days before the onset of illness: intramuscular/intrave- nous injections; blood transfusion; dental treatment; surgical operation; hospital admission for any cause; any chronic illness requiring frequent treatment; tattooing; and contact with a case of jaundice within or outside the family. It soon became apparent that a local unqualified medical practitioner had administered intramuscular injections for minor ailments to many patients around the time of the Diwali festival. All the local medical practitioners in the affected villages were therefore thoroughly interviewed to determine their qualifications and treatment practices, and two types of epidemiological studies were planned, as de- scribed below. * House-to-house surveys were carried out on 4-6 March 1997 in the three affected villages (Khata- Amba, Parsa and Charadu) and in one nearby village (Boru) that was not covered by the implicated medi- cal practitioner. Health workers went from house to house to collect any histories of jaundice since the Diwali festival (10 November 1996). * At least 75 apparently healthy persons from Khata-Amba had been given injections by the impli- cated medical practitioner in October-November 1996 and blood samples were collected at random from 31 of these individuals. An equal number of age- and sex-matched control samples were also col- lected from individuals who had never been given injections by this practitioner. Laboratory investigations Blood samples were drawn from all cases in the study villages who were reported to have had jaun- dice since the Diwali festival, as well as from their healthy contacts. Sera were separated in Civil Hospi- tal, Gandhinagar, and transported to the main labo- ratories of the National Institute of Communicable Diseases, Delhi, for testing for markers of viral hepa- titis. The sera of cases were tested using a macro- ELISA kit (enzyme-linked immunosorbent assay) (bead ELISA) (Abbott Laboratories, North Chi- cago, IL, USA) for IgM anti-HAV (hepatitis A vi- rus), IgM anti-HBc, HBsAg, anti-HCV (hepatitis C virus), and anti-HEV (hepatitis E virus). The sam- ples were also tested for IgM anti-HEV using ELISA kits (Genelabs Diagnostics, Singapore). All samples found positive for HBsAg were tested for anti-HDV. Serum samples from apparently healthy persons were tested for HBsAg and anti-HBc using bead ELISA (Abbott Laboratories, North Chicago, IL, USA). Results Details of the 15 individuals for whom there was evidence of hepatitis B are shown in Table 1. None of these individuals was positive for markers of HAV, HCV, and HEV; of 11 samples tested, 3 were positive for anti-HDV (hepatitis D virus). All the cases of viral hepatitis B were adults aged 319 years and nine were male. Seven patients died within 2-3 weeks of the onset of their illness (case fatality ratio, 47% (7/15)). At least three patients who died had evidence of sexually transmitted disease (penile ulcers), one of whom had worked in Surat away from his family for the previous 5 years. None of 15 patients with viral hepatitis B had a history of hospital admission, blood transfusion, in- travenous injections, tattooing, or dental treatment between 6 months and 15 days before the onset of illness. Two cases were related to each other (uncle- nephew) but in no other instances was there a history of contact with a case of jaundice within or outside family. One patient had bronchial asthma and an- other, hypertension. At least 10 of the 15 patients with viral hepatitis B were definitely/probably treated for minor ill- nesses by the implicated local practitioner (K.K.P.) and had received injectable drugs around Diwali. The remaining five patients or their relatives were not available or did not cooperate to elicit this information. K.K.P. claimed to have qualifications from the Gujarat Board in Ayurvedic and Unani medicine. However, he frequently treated patients with inject- able drugs, e.g. gentamicin, ampicillin, chloram- phenicol, or Deriphyllin; usually, he administered only one injection of antibiotic and then prescribed other drugs. He had a clinic at Parsa, where a boiler (for syringe and needles) was connected to an electric power point. In Khata-Amba village he went from house to house to treat patients, and claimed to carry one syringe and many needles to give injections, asking for hot water to rinse the syringe before giving an injection. The villagers, however, claimed that he carried only one syringe and one needle on his visits to Khata-Amba and rinsed these in hot water before giving injections. From time to time, he also went to Charadu village to treat patients. Another local practitioner (M.S.P.) who claimed to have received a medical degree in April WHO Bulletin OMS. Vol 76 199894 Viral hepatitis B outbreak in India Table 1: Details of viral hepatitis B cases identified during the study outbreaka Serostatus: Age Date of onset Patient (years) Sex Village of symptoms Outcome Date of death IgM HBcb Anti-HDV J.B.D. 35 M Khata-Amba 2 Jan. 1997 Died 7 Jan. 1997 NDc ND V.D.C. 55 M Khata-Amba 15 Jan. 1997 Recovered - +ve -ve S.K.P. 21 M Khata-Amba 1 Dec. 1996 Recovered - +ve -ve H.L.D. 25 M Ahmedabadd 4 Jan. 1997 Died 12 Jan. 1997 ND ND S.P.D. 55 F Khata-Amba Jan. 1997 Recovered - +ve -ve (first week) S.G.C. 35 F Khata-Amba 16 Jan. 1997 Died 25 Jan. 1997 ND ND M.J.D. 19 M Khata-Amba 24 Jan. 1997 Died 7 Feb. 1997 +ve -ve J.P.D. 25 M Suratd Jan. 1997 Died 9 Feb. 1997 ND ND (last week) N.M.D. 30 M Khata-Amba Jan. 1997 Recovered - +ve -ve (3rd week) R.N.C. 19 F Khata-Amba 25 Feb. 1997 Recovered - +ve -ve J.K.P. 30 F Parsa 3 Feb. 1997 Recovered - +ve +ve R.P.P. 60 F Parsa 18 Feb. 1997 Died 7 Mar. 1997 +ve +ve J.P.P. 80 M Parsa 25 Feb. 1997 Died 9 Mar. 1997 +ve +ve B.V.T. 45 M Charadu 24 Nov. 1996 Recovered - +ve -ve R.M.T. 38 F Charadu 4 Feb. 1997 Recovered - +ve -ve a All patients were positive for HBsAg and had raised serum bilirubin levels. b All samples positive for IgM HBc were negative for IgM HAV, anti-HCV, and anti-HEV. c ND = not done. dVisited native village (Khata-Amba) around 10 November 1996 and given injections by K.KP. 1995, had been practising in Khata-Amba for 7 months when the study was carried out. He treated patients in his clinic only, he also prescribed injec- tions, but reportedly used only disposable syringes and needles. Nevertheless, he was aware of the importance of boiling syringes and needles before giving injections. As shown in Table 2, house-to-house surveys by paramedics revealed 14, 3, and 2 cases of jaundice, respectively, in Khata-Amba, Parsa, and Charadu. Of these cases, two in Khata-Amba were considered not to have clinical jaundice by a medical Table 2: Attack rate of jaundice in four villages covered by Itadara primary health centre, Mehasana district, 10 November 1996-March 1997 Population No. of jaundice Attack rate Village surveyed cases (per 1000) Khata-Amba 2360 122a 5.08 Parsa 3031 3 0.99 Charadu 3889 2 0.51 Boru 3552 0 0 a Two cases were later not confirmed as being due to hepatitis B virus. officer and two additional cases had no labora- tory evidence of viral hepatitis B. No case of jaun- dice was discovered in Boru village. The attack rate of jaundice in Khata-Amba (5.1 per 1000 popu- lation) was significantly higher than that in Parsa (1 per 1000), Charadu (0.5 per 1000), or Boru (0 cases). As shown in Table 3, the prevalence of HBsAg or anti-HBc among apparently healthy persons in Khata-Amba was about 42% (13/31) for individ- uals who had received injections from K.K.P. in October-November 1996. In contrast in the con- trol group (those who never had injections from K.K.P.) none of the samples was positive for HBsAg and 13% (4/31) were positive for anti-HBc. This difference was statistically significant irrespective of whether HBsAg alone or both markers were considered. The reported data on viral hepatitis from Itadara primary health care centre, Mehasana dis- trict, and Gujarat State over the period 1991-96 are shown in Table 4. Since the immunological markers of viral hepatitis are not easily available, the data can not be stratified according to type of viral hepatitis. Nevertheless, the case fatality rate has never been more than 4% during this period. Interestingly, Itadara primary health centre reported only one case, in 1995. WHO Bulletin OMS. Vol 76 1998 95 Table 3: HBsAg seropositivity among study villages apparently healthy persons in the No. positive for: No. Village tested HBsAg Anti-HBc Persons given Khata-Amba 31 a 7 (23)b 6 (25)a injection by K.K.P. Persons never given Khata-Amba 31 0 4 (13) injection by K.K.P. Unaffected village Boru 10 0 (0) Not tested Contacts of cases Charadu, 24 1 (4) Not tested Khate-Amba, and Parsa Health workersc Khata-Amba 3 0 (0) Not tested a Only 24 samples (negative for HBsAg) were tested for anti-HBc. b Figures in parentheses are percentages. c Includes the two private practitioners (K.K.P. and M.S.P.) and one other health worker. Table 4: Reported cases and deaths from viral hepatitis in Itadara primary health centre (PHC), Mehasana district, and Gujarat State, 1991-96 PHC Itadara: Mehasana district: Gujarat State: Year Cases Deaths CFRa Cases Deaths CFR Cases Deaths CFR 1991 0 0 0 176 4 2.3 6816 195 2.9 1992 0 0 0 62 0 0 4407 135 3.1 1993 0 0 0 76 3 3.9 8825 176 2.0 1994 0 0 0 149 3 2.0 7701 168 2.2 1995 1 0 0 778 5 0.6 4867 89 1.8 1996 0 0 0 69 6 8.7 6282 89 1.4 Total 1 0 0 1310 21 1.6 38898 852 2.2 a CFR = case fatality rate. Discussion Our epidemiological and laboratory findings confirm the outbreak of viral hepatitis B, which centred mainly in Khata-Amba village. The outbreak was epidemiologically linked to the use of inadequately sterilized needles and syringes by an unqualified medical practitioner. At least 10 of 15 patients with viral hepatitis B were definitely/probably treated for minor illnesses by a local unqualified medical practitioner and ad- ministered injectable drugs around the time of the Diwali festival (10 November 1996). The remaining patients or their relatives were either not available for interview or did not cooperate to enable us to elicit this information. A total of 13 of 31 (42%) blood samples collected from apparently healthy persons who had also received injections from K.K.P. were also positive for HBsAg or anti-HBc. In contrast, only 4 of 31 (13%) samples collected from those who had never received injections from K.K.P. were positive for anti-HBc; none of these was posi- tive for HBsAg. Similarly, a house-to-house survey did not reveal any case of hepatitis in Boru village, which had similar demographic characteristics but which was not visited by K.K.P. The outbreak was marked by a high case fatality rate (46.7%). A total of 3 of 11 samples from viral hepatitis B cases were positive for anti-HDV: two of three fatal cases whose serum samples were avail- able for testing by NICD were positive for anti- HDV. Co-infection with hepatitis B and D viruses (IgM-HBc positive) as well as superinfections (IgM- HBc negative) have been reported to cause both WHO Bulletin OMS. Vol 76 1998 J. Singh et al. 96 Viral hepatitis B outbreak in India fulminant hepatitis and high mortality rates (5, 6). Therefore, concurrent infections with hepatitis B and D viruses may, at least partly, explain the high case fatality rates observed in this outbreak (5). However, at least three additional patients who died had evidence of sexually transmitted diseases, and reportedly had penile ulcers that were being treated by K.K.P. Had it not been for the high mortality rate, the outbreak would have gone unnoticed, and rein- forced the impression that community outbreaks of viral hepatitis B do not occur in India. Many cases had already occurred by the time the health authori- ties identified the first death in Khata-Amba village. In fact, while carrying out this study we found an- other cluster of viral hepatitis B cases centred in Dholasan, a village about 40km from Khata-Amba, which had not been identified and reported through the routine surveillance system; this outbreak was also later confirmed as viral hepatitis B. The data on viral hepatitis (Table 4) also indicate the low sensitivity of the routine surveillance system. On av- erage, about 200 cases of viral hepatitis are reported every year from Mehasana district (population >3 million), whereas community-based studies estimate that its incidence is around 1 per 1000 population (7). Our results also document the indiscriminate use of drugs, especially antibiotics by unqualified practitioners, who are a common feature of country areas in India. Pathogens, e.g. Salmonella typhi, rap- idly develop resistance to low doses of antimicrobials (8). This is another area for serious concern, which requires continuous monitoring and appropriate use of antimicrobials in clinical practice. In conclusion, our findings emphasize the fol- lowing: the importance of inadequately sterilized needles and syringes in the transmission of viral hepatitis B in India; the need to strengthen the rou- tine surveillance system; and the need to organize a health education campaign targeting all health care workers, including private practitioners, especially those in rural areas, and the public at large, to take all possible measures to prevent the spread of this often fatal infection. Resume Flambee de cas d'hepatite B liee a une sterilisation insuffisante des aiguilles et des seringues dans une communaute rurale de l'Inde, 1997 La quasi-totalit6 des flambees d'hepatite virale sur- venant en Inde sont consid6r6es comme dues a une transmission f6co-orale du virus de l'h6patite E. Le virus de l'hepatite B n'a jamais 6t6 mis en cause dans des flamb6es observees dans la communaute. Ce rapport d6crit un groupement inhabituel de 15 cas d'h6patite B dans trois villages adjacents du district de Mehsana, dans l'Etat du Gujerat. La flamb6e s'est developp6e lentement, sur une p6riode de trois mois. Les 15 cas concernaient des adultes de plus de 19 ans, dont neuf de sexe masculin. Sept malades sont d6c6d6s dans les 2 a 3 semaines suivant le d6but de la maladie, ce qui repr6sente un taux de letalite de 47% (7/15). Aucun des cas n'6tait positif pour les marqueurs de l'h6patite A, C ou E. Trois prelevements sur 11 6taient positifs pour l'anticorps anti-hepatite D (HDV); deux des trois cas mortels pour lesquels on disposait d'6chantillons s6rologiques 6taient positifs pour I'anti-HDV. Aucun des malades n'avait d'ant6c6dents d'hospitalisation, de transfusion sanguine, d'injec- tions intraveineuses, de tatouage ou de soins dentaires dans les six mois prec6dant le d6but de la maladie, a 1'exception des 15 derniers jours. Deux cas presentaient un lien de parente (oncle et neveu); les autres cas n'avaient eu aucun contact avec un cas d'ictbre que ce soit au sein ou en dehors de la famille. En revanche, au moins 10 des 15 malades avaient 6t6 trait6s ou probablement trait6s pour des affections mineures par un pra- ticien local non qualifi6 (K.K.P.) et avaient re,u des injections de m6dicaments au moyen d'aiguilles et de seringues insuffisamment st6rilis6es. Les autres malades (ou membres de leur famille) n'ont pu etre interrog6s ou ont refus6 de donner ce type d'information. De plus, 13 6chantillons de sang sur les 31 (42%) pr6lev6s chez des sujets apparem- ment en bonne sant6 mais ayant egalement recu des injections pratiqu6es par K.K.P. ont 6te trouv6s positifs pour l'HBsAg ou l'anti-HBc, alors que seule- ment 13% d'un nombre 6gal d'6chantillons pr6lev6s chez des sujets n'ayant jamais recu d'injections par K.K.P. 6taient positifs pour I'anti-HBc, et aucun d'entre eux n'6tait positif pour l'HBsAg. La diff6- rence entre les deux groupes 6tait statistiquement significative, que l'on considere seulement I'HBsAg ou les deux marqueurs. Sans cette forte mortalit6, la flamb6e serait pass6e inaper,ue et aurait renforc6 I'idee selon laquelle il n'existe pas de flamb6es d'h6patite B en Inde. De nombreux cas 6taient d6ja survenus lorsque les autorit6s sanitaires ont eu connaissance du premier deces associ6 a cette flamb6e. En effet, lors de 1'enquete, les auteurs ont rencontr6 un autre groupe de cas d'hepatite B centre sur un village 6loign6; cette flamb6e, non encore identifi6e et WHO Bulletin OMS. Vol 76 1998 97 J. Singh et al. rapportee par le systeme de surveillance de routine, a par la suite et6 identifi6e comme etant due a l'hepatite B. Cette 6tude souligne le r6le des aiguilles et seringues insuffisamment sterilis6es dans la transmission de l'hepatite B en Inde, la n6cessit6 de renforcer le systeme de surveillance de rou- tine et la n6cessit6 d'organiser une campagne d'6ducation sanitaire destin6e a tous les agents de soins de sant6 y compris les praticiens ind6pendants, en particulier dans les regions rurales, ainsi qu'au grand public, afin que toutes les mesures soient prises pour 6viter cette infection mortelle. References 1. Tandon BN, Gandhi BM, Joshi YK. Etiological spectrum of viral hepatitis and prevalence of markers of hepatitis A and B infection in north India. 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