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Viral hepatitis as a major cause of maternal mortality in Addis Ababa, Ethiopia
Inr. J. C;ynuecol. Clbstet., 1987, 25: 99-106 International
Federation
VIRAL ADDIS
of Gvnaecology
& Obstetrics
HEPATITIS AS A MAJOR ABABA, ETHIOPIA
B.E. KWAST*
CAUSE
OF MATERNAL
MORTALITY
IN
and J.A. STEVENS
Emory University School of Medicine, Atlanta, Georgia 30322 and Research and Statistics Branch, Division of Reproductive Health, Center for Health Promotion and Education, Centers for Disease Control, Atlanta, Georgia 30333 (USA) (Received (Accepted
August llth, 1986) September 1 lth, 1986)
Abstract
through education, better hygiene, proved sanitation are discussed.
Kwast BE and Stevens JA (Emory University School of Medicine, Atlanta, Georgia 30322, formerly Addis Ababa University, Ethiopia and Research and Statistics Branch, Division of Reproductive Health, Center for Health Promotion and Education, Centers for Disease Control, Atlanta, Georgia 30333, USA) Viral hepatitis as a major cause of maternal mortality. Int J Gynaecol Obstet 25: 99-106, 1987 Causes of maternal mortality were investigated in Addis Ababa, Ethiopia, from September 1981 to September 1983. Viral hepatitis ranked third among the leading causes of maternal mortality behind septic abortion and puerperal sepsis. There were 26 deaths from viral hepatitis during the 2-year study period for a hospital maternal mortality rate of 91 .(I per 100,000 live births. Although 30% of women who died of all maternal causes received antenatal care in Addis Ababa, only 13% of women who died from viral hepatitis in our hospital study received antenatal care. Low socio-economic status (SES) has been shown to be associated with low antenatal care utilization and with an increased risk of protein malnutrition. Malnut&ion is considered a predisposing factor for liver damage. Suggestions for reducing hepatitis transmission and maternal mortality 0020-7292/87/$03.50 (9 1987 International Federation Puhlkhed and Printed in Ireland
of Gynaecologv
& Obstetrics
and im-
Keywords:
Ethiopia; hepatitis; Viral Maternal mortality; Non-A, Non-B hepatitis; Confidential inquiries; Folk beliefs.
Introduction Women who contract viral hepatitis during pregnancy, especially during the second and third trimesters, are more likely to die from the disease than are non-pregnant women. Maternal mortality associated with viral hepatitis has been described in the developing countries of Ghana, Libya, China, Iran, Nepal, India, Ethiopia and Nigeria [2,6,8,9,13,20,2 I ,23,27]. Thr: case fatality rates observed for pregnant women with viral hepatitis ranged from IO% to 45%. However, the contribution of viral hepatitis to overall maternal mortality has not been well documented. The maternal mortality rate from viral hepatitis and its rank in comparison with other main causes was studied in Addis Ababa, Ethiopia, from September IOX I to September 1983. This paper presents descriptive data regarding maternal mortality resulting from viral hepatitis, information about the folk beliefs surrounding
IO0
Kwast and
Stevens
the causation and treatment of this disease, and three case histories illustrating the effect of these beliefs on the utilization of appropriate medical care. Rackground
The Ethiopian capital, Addis Ababa, located at an altitude of 2408 m, had a population of 1,154,459 as of July 1982 [16]. The population growth rate of 5% per year has resulted in critical problems, especially housing and sanitation. The mean per capita income in Addis Ababa is estimated at U.S. $75 per month [23]. The Ethiopian Ministry of Health has a policy of providing medical care free of charge for persons with a monthly per capita income of less than U.S. $25. This may be understood as defining a group with the lowest SES. In 198 1, 79% of Addis Ababa’s population lived under disadvantaged conditions [ 121. It was estimated in 1981 that only 6% of the country’s population had access to safe water. The Ethiopian government’s goal is to supply 35% of the rural and all of the urban population with safe drinking water by the year 1990 [26]. Cultural
beliefs
Jaundice associated with hepatitis has long been recognized in a number of Ethiopian provinces, including Shoa Province, where Addis Ababa is located. Hepatitis, called “yewof beshta” (bird’s disease), is believed to be transmitted by a “big night bird,” either by its urine falling on a person outside at night or early in the morning or simply by the bird circling above the person three times. The bird, described as having a wingspan resembling a pair of outstretched hands, is actually a bat [l]. Traditional treatment consists of eating a variety of boiled roots or leaves or eating a mixture of dried bat meat and herbs. The superstitions regarding causation and treatment of jaundice associated lnt J Gynaecol
Obstet 25
with hepatitis keep people from seeking appropriate ‘and timely medical treatment. Methods
The study of maternal mortality associated with viral hepatitis in Ethiopia was conducted as part of a Maternal Mortality Review Committee under the auspices of the medical faculty of Addis Ababa University. From September 1981 to September 1983, data on 198 maternal deaths were collected from the records of five city hospitals, the only institutions offering obstetric services under the Ministry of Health’s administration. The methodology of the confidential inquiry, modeled on the British system, has been described elsewhere [ 151. Of the 198 maternal deaths, 26 were classified as being associated with viral hepatitis. This diagnosis was determined by a physician from the detailed history and the clinical examination taken at the time of admission. Criteria for diagnosis of viral hepatitis included the manner of onset of jaundice-specifically, whether it was preceded by acute febrile illness or associated with loss of appetite, vomiting, gastrointestinal upsets, and general malaise. No serological tests were done. Serum transaminase was determined for five patients, bilirubin levels were determined for three and alkaline phosphatase was patients, determined for four patients. The 26 maternal deaths associated with viral hepatitis did not include any deaths from fulminating puerperal septicemia, relapsing fever, eclampsia, or possible malaria. None had a history of previous blood transfusion. Results
The five city hospitals registered 28,583 live births and 26 maternal deaths from viral hepatitis during the 2-year study period. The hospital maternal mortality rate for viral hepatitis was 91.0 per 100,000 live births.
Viral hepatitis and maternal
Of the 26 maternal deaths from viral hepatitis, 16 occurred in the first year of the study and 10 in the second year. The distribution of deaths from 1981 through 1983 did not show a seasonal variation. Table I gives selected characteristics of the women who died from viral hepatitis compared with hospitalized women who died of all other causes. Fourteen viral hepatitis patients (54%) were 30 years old or older versus 49 (28%) of patients in the comparison group. Twenty-seven percent of the women who died from hepatitis was para 6+ compared with 12% of women who died from other causes. The mean per capita income, known for 13 women who died of hepatitis, was to U.S. $20 per month. equivalent The average level of education, known Table 1. Selected characteristics of women who died from viral hepatitis compared with all women who died from other causes, Addis Ababa, September 1981-September 1983.
Characteristics
Viral hepatitis n=26 (%)
All other n= 172
causes (%)
Age (years) 14-19 20-24 25-29 30-34 235 unknown
0 5 4 9 5 3
(19) (16) (35) (19) (11)
35 42 38 19 30 8
(24) (22) (11) (18) (5)
Parity 1 2-3 4-5 zh unknown
3 7 4 7 5
(11) (27) (16) (27) (19)
63 41 24 21 23
(37) (24) (14) (12) (13)
Antenatal care yes no unknown
2 14 10
(0)
(8) (54) (38)
36 62 74
(20)
(21) (36) (43)
2 3 7 14
(8) (12) (27) (54)
6 24 33 109
(3) (14) (19) (63)
IOI
for 12 women, was 2 years of elementary school, although two women had some secondary school education. Information on water sources and on toilet facilities was known for 11 and 13 families, community standpipes were respectively: used by nine families (82%) and river water by two families (18%); pit latrines were used by eight families (62%) and open fields by five families (38%). Characteristics related to gestation and labor are described in Table II. Six deaths occurred in late pregnancy before the start of labor (antepartum). Two women died before giving birth during labor (intrapartum), and 16 died after having spontaneous vertex deliveries. Most patients had signs and symptoms of encephalopathy and gastrointestinal and genitourinary tract bleeding. The mean hemoglobin level, known for 10 women, was 12.6%. Five of 19 patients for whom this information was known had hepatomegaly and four developed positive chest findings after adTable II. of women September
Selected characteristics who died from viral 19X1-September 1983.
from labor and delivery hepatitis, Addis Ahaba.
Characteristics
Number
Gestation 2nd trimester 3rd trimester unknown
2 20 .l
Admission-onset of labor in labor on admission ~6 h 6-12 h 12-18 h not applicable (died antepartum) delivered at home unknown
interval
(n = 26) --
3 2 3
I 6 3 x
interval
Admission-death
Family Planning used aware/not used awareness not known/not used no information
mortality
(h)
61
2
2-23
5
24-36
5
37-48
h
49-120
3
unknown
5 --
Inr .I Ciynaecol Obster
2.5
102
Kwast
and Stevens
mission. Patients sought medical care late, a mean of 10 days after the onset of symptoms. All but two patients were afebrile and in precomatose or comatose states on admission. The consequences of these delays and of the high frequency of coma was a mean admission-to-death interval of 33 h. All women who delivered had spontaneous onset of labor. Of those women who went into labor after admission, the mean admission-to-onset of labor interval was 8 h. Eight women had severe postpartum hemorrhage. Of the 16 women who delivered, 10 had stillbirths, and 2 of the 6 live births died within 24 h after delivery. Fetal wastage was 75%. The following case histories illustrate the impact of the folk beliefs about viral hepatitis on maternal health at the time this study was conducted. Case one A 2%year-old, para 3 woman was admitted in a prehepatic coma 4 days after home delivery of a full-term, live female baby who was attended by a traditional birth attendant. The woman and her husband had no formal education. Their monthly per capita income was equivalent to U.S. $18. A history revealed that the patient had discoloration of the sclera and dark yellow urine for 8 days. One day before admission the patient had become restless, irritable, and confused. Physical examination revealed a blood pressure of 120/60 mmHg and a pulse rate of 72 beats/min. The patient was afebrile, her lungs were clear, there was no hepatomegaly, her uterus was well contracted, and there was no vaginal bleeding. There was some central nervous system depression. Laboratory findings were hemoglobin 10.8 g%, leucocytes 14,80O/ml, and platelets 131,00O/ml. Hemoparasites for relapsing fever and malaria were negative. The patient became confused and restless during the next 24 h and went into a deep coma. Forty-eight hours after admission she Int J Gynaecol Obsrer 2.5
had convulsions. The patient died 55 h after admission, on the sixth postnatal day. Home visits were carried out as time permitted. The family was visited several months later to learn more about their living conditions and the survival of the child. The people lived in close proximity in a typical compound where small houses enclosed a courtyard. Water was obtained from a community standpipe. Toilet facilities consisted of a shared pit latrine. Neighbors explained that the deceased woman’s infant daughter was well and that a collective effort was made to care for her children when the father was away. It was learned that the deceased woman had bled heavily after delivery. The neighbors had noticed her illness with the characteristic yellow eyes and dark urine. Although they had known pregnant women to die from “bird’s disease,” they did not believe the hospital could treat it effectively.
Case two A 24-year-old women, gravida 3, para 2, had developed jaundice and loss of appetite for which she took traditional medicine. When the medicine proved ineffective, she went to the district hospital 12 days after first experiencing symptoms. She was admitted to the district hospital but after 2 days was referred to a city hospital 80 km away when she started to become confused. The patient arrived at the city hospital in hepatic coma secondary to infectious hepatitis. She was febrile. Her blood pressure was 110/70 mmHg and her pulse rate was 140 beats/min. Her lungs were clear. Central nervous system examination revealed hyperextension and rigidity of both upper and lower extremities and neck rigidity. The fundal height corresponded to 36 weeks gestation. There was no audible fetal heart beat. Eighteen hours after admission the patient’s chest was full of secretions and she was bleeding from the nasopharynx. Labor
Viral hepatitis and maternal mortality
had started but there was antepartum hemorrhage and the patient went into shock. An hour later, the patient was in the second stage of labor but had not given birth when she died, 20 h after admission. No home visit was carried out because the women came from outside Addis Ababa. Case three
A 23-year-old woman, gravida 3, para 2, had received regular antenatal care beginning at 16 weeks gestation. She was 1.6 m tall and had gained 6 kg during her pregnancy. She was married and had an 1 lth grade education. Her husband was a college graduate with a technical job who earned the equivalent of $300 in U.S. currency per month. On admission, the patient gave a history of 6 days of fever, loss of appetite, vomiting, change of urine color, and pruritis. Her son had jaundice at that time. The physical examination revealed mild jaundice. Her blood pressure was 1 lo/90 mmHg and her pulse was 96 beats/min. The liver was palpable 2 cm below the right costal margin. The patient was in labor. The size of the uterus corresponded to 39 weeks gestation, the fetal lie was longitudinal, and the presentation was cephalic. The head was engaged and the fetal heart rate was 132 beats/min. Labor progressed well, and 11 h after admission the patient had a spontaneous vertex delivery of a live male infant weighing 3350 g. The placenta and membranes were expelled with minimal blood loss. Postdelivery treatment included prophylactic intravenous infusion of 5% dextrose/water with vitamin Blz. However, 24 h after delivery the patient developed bloody diarrhea. She was fully conscious and was kept on bed rest. The following day she complained of abdominal pain and backache. Eighty-four hours after delivery the patient developed a hepatic precomatose condition. Laboratory findings were hemoglobin 1 I .W”, SGOT 2 150 Cabaud units/ml, SGPT 610 Cabaud units/ml, total
I 03
bilirubin 10 mg/ 100 ml, and direct bilirubin 5.8 mg/lOO ml. She was transfused with two units of blood but on the fifth postnatal day she became comatose. Chest examination revealed scattered rhonchi. There was rigidity in the upper extremities. Gastric aspirate produced 400 ml of coffee-ground material. The patient died on the fifth postnatal day. During the home visit 9 months later, it was learned that the infant of the deceased women was healthy. The deceased women’s mother knew that her daughter had had “bird’s disease,” which the mother knew could be fatal in pregnant women. Because both’ women believed that the modern health system had no cure, the daughter had taken traditional medicine for the illness. Discussion
The hospital maternal mortality rate for viral hepatitis during the study period was 91.0 per 100,000 live births, whereas the maternal mortality rate in the city of Addis Ababa was 76.5 per 100,000 as determined through a household sample survey [16]. This difference would be expected because women who deliver at home and develop complications are likely to be admitted to a hospital. Table III demonstrates that viral hepatitis and ruptured uterus each ranked as the third highest cause of maternal mortality in Addis Ababa. This is consistent with studies from Nigeria, Ghana, Malawi, and South Africa [2,3,7,20], which have ranked viral hepatitis among the six leading causes of maternal mortality. Most of the Ethiopian population experiences hepatitis A as a mild disease anti-HAV antibodies in and develops childhood, as evidenced by the demographic and serologic survey of viral hepatitis in 1983 [25]. This study found a hepatitis B marker prevalence of 42% overall and 76% among those over 14 years of age. Viral hepatitis in Addis Ababa appears to be endemic. There were 16 maternal deaths Int .I Gvnaecol
Obstet 2.5
104
Kwast and Stevens
Tabk III. study.
Comparison of maternal mortality rates (MMR) per 100,000 live births from major causes by country and year of
Country
Ethiopia Malawi” Nigeriai’ South Africa’ Nigeria“.’ Ghana’
Year of study
1981-1983 1977 1976-1977 1973-1975 1962-1971 1963-1967
Causes Septic abortion
Puerperal sepsis
Viral hepatitis
Ruptured uterus
Eclampsia
Hemorrhage
164.4 9.4
94.5 23.5 58.5 115.3 58.3 68.2
91.0 2.3 45.0 96.1 125.6 88.1
91.0 44.7 58.5 3.8 31.4 93.x
70.0 2.3 49.5 53.8 31.4 99.5
52.5 49.4 63.0 42.2 98.7 179.0
57.6 53.9 93.8
“See Ref. 6. “See Ref. 2. ‘See Ref. 4. “See Ref. 20. ‘MMR from severe anaemia: 152.6. ‘See Ref. 1.
from viral hepatitis during the first study year and 10 maternal deaths during the second year. No peaks occurred during the study period. Also, this study did not show a seasonal variation in the maternal deaths from viral hepatitis, although such a variation was seen in two other studies where high mortality rates resulted from epidemics [3,27]. Therefore, identifying the type of hepatitis is essential to apply appropriate intervention measures. Infections from non-A, non-B hepatitis as well as from hepatitis B are the most likely causes of hepatitis mortality during pregnancy [6,9,17,19,22]. Outbreaks of non-A, non-B hepatitis were reported among Ethiopians in Somalian and Sudanese the camps in 1985, showing refugee presence in these countries of a virus similar to the one in India (Mark A. Kane, pers. commun.). In early 1986, outbreaks of hepatitis, thought to be hepatitis B, were reported from relief shelters in Ethiopia (Mark A. Kane, pers. commun.). Studies should be continued and should incorporate serologic testing to determine the occurrence of different serological agents. Deaths from hepatitis B can be prevented by the appropriate use of hepatitis B vacInt J Gynaecol
Obstet 2.5
tine. Treatment of newborns could prevent acquisition of the disease and could eventually reduce maternal infection. Unfortunately, the current cost of hepatitis B vaccine prohibits its general use in Ethiopia. Hepatitis B is efficiently transmitted through unsterile needles and medical and dental equipment. Improving the sterilization procedures for needles and other medical items would have some impact on reducing mortality and morbidity from this disease. The possibilities for prevention of non-A, non-B hepatitis are more favorable. The form of this disease present in northern Africa and the Indian subcontinent has a fecal-oral route of transmission; improving hygiene and providing safe water would be viable intervention strategies [4,14,22]. Examining the safety of the present water system, as well as increasing the availability of safe water, is critical for this approach to be effective. Education is also an essential aspect of any preventive approach but will not succeed without sensitivity and respect for cultural attitudes. Folk beliefs surrounding hepatitis often conflict with a person’s perception of disease transmission. This in turn interferes with potential improvements in
Viral hepatitis and maternal
health behaviors and delays the receipt of timely medical care, as demonstrated by this study. Comparison of antenatal care use (Table I) suggests that women who died of viral hepatitis utilized these services less than did controls. Of all the hospitalized women who died of maternal causes other than hepatitis, 67% had not received antenatal care. The percentage was higher among the women who died from hepatitis but was the same for women who delivered in hospitals and survived. In contrast with this hospital population, a household survey found antenatal care coverage in Addis Ababa as a whole was 30% among women who died of maternal causes both in and out of the hospital and 70% among women who survived [16]. There also appears to have been a difference between the two groups in their use of family planning, although these data are difficult to interpret because no information was available for a large percentage of the women. Low SES has been shown to be related to comparatively low utilization of antenatal care [ 1.51. Information on income for 13 women showed that 11 had monthly per capita incomes below the Addis Ababa mean of U.S. $75 and therefore had low SES. Motivating women to attend antenatal clinics will contribute to improved maternal health. Although antenatal care will not directly prevent hepatitis, contact with a maternity service will benefit women by providing information in a number of areas: sanitation and hygiene, family planning, and health education and risk factors during pregnancy. Protein malnutrition, often found in con-
junction with low SES, is considered a predisposing factor for hepatocellular damage from hepatitis [6, lo]. In this study, 1 1 out of 13 women were of low SES and probably at risk for malnutrition, although anthropometric measurements were not determined. The literature reports that maternal mor-
mortality
105
tality is exceptionally high among women with hepatitis during the third trimester, following spontaneous labor and delivery [9,11]. Megafu, in Nigeria, has described a considerable reduction in mortality following induced labor in the third trimester [18]. Additional research is needed to determine if inducing labor in the third trimester might be a productive approach to decreasing these maternal deaths. One must be cautious in drawing conclusions based on hospital data because the population differs from the community at large. Continued research into viral hepatitis, further education of health care personnel regarding hepatitis transmission, and the provision of adequate health facilities with the laboratory staff and equipment for typing the disease are all important factors in understanding and ultimately controlling viral hepatitis. Conclusions
The high maternal mortality and fetal wastage attributable to viral hepatitis clearly shows that the problem of viral hepatitis in pregnancy needs to be addressed. Viral hepatitis will become of even greater relative importance as the other major causes of maternal mortality, i.e. septic abortion, puerperal sepsis, ruptured uterus, and eclampsia, decline through the implementation of preventive strategies. Education, application of good hygiene, provision of safe water, and improvement in basic sanitation will all help prevent disease transmission. If the target of providing safe water for 35% of the rural population and all of the urban population by 1990 is accomplished by the Ethiopian government, it will go a long way toward reducing maternal mortality from viral hepatitis. Acknowledgments
The authors express thanks to Mark A. Kane, M.D., M.P.H., Centers for Disease Int J Gynaecol
Obstet 25
106
K wast and Stevens
Control, Atlanta, for his helpful discussion and criticism; to the members of the Maternal Mortality Review Committee: Widad Kidane-Mariam, M.D., Adane Gossa, M.D., Mekonnen Bekele, M.D., Seyoum Yoseph, M.D., and Leteberhan Mehari, R.N., R.M.; to Professor Edemariam Tsega and Frances Lester, M.D.; to the staff responsible for the hepatitis patients at the Black Lion Hospital and the Yekatit 12 Hospital in Addis Ababa; to all consultant obstetrician/gynecologists of the hospitals under the administration of the Ministry of Health for making case records available; and to Carol Cummings, Emory University School of Medicine, Atlanta, for secretarial help. References
13 Kane MA, Bradley DW. Shrestha SM, et al.: Epidemic non-A. non-B hcpatiti\ in Nepal. J Am Mcd A\soc 2.-i.?: 3140, 1984. 14 Khuroo, MS: Study of an epidemic of non-A, non-B hepatitis: Possibility of another hepatitis \ irus distinct from post-transfusion non-A. non-B type. Am J Med hX: 818. 1980. IS Kwast BE. Kidane-Mariam W. Saed EM. Fowkc\ FGR: Report on maternal health in Addis Ababa, Radda Barnen (Swedish Save the Children Federation). P.O. Box 3457, Addis Ababa, Ethiopja. lYX4. 16 Kwast BE, Kidane-Mariam W, Saed EM. Fowkes FGR:
17 18 19 20
Abate G: Ethiopian Traditional Medicine (Addis Ababa University, Addis Abaha, Ethiopia) Vol. 1, pp 334-339. 1980. Ampofo DA: Causes of maternal deaths and comments. Maternity hospital, Accra. W Afr Med J 1X: 75, 1969. Balachanran V: Maternal mortality in Kaduna 19641972. Nig Med .I 5: 366, 1975. Balayan MS, Andjaparidze AC, Savinskaya SS. et al.: Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology 20: 23, 1983. Barford DAG, Parkes JR: Maternal mortality: A survey of 118 maternal deaths and the avoidable factors involved. S Afr Med J 51: 101, 1977. Borhanmanesh F, Haghighi P, Hekmat K, Rezaizadeh K, Ghavami AC: Viral. hepatitis during pregnancy. Gastroenterology 64: 304, 1973. 7 Bullough CHW: Analysis of maternal deaths in the central region of Malawi. East Afr Med J 58: 25, 1981. 8 Chen R-J: Maternal Mortality in Shanghai, China. Presented at Interregional meeting on Prevention of Maternal Mortality, Geneva. November I l-l S. IYXS (FHE. PMM/85.9.2). Y Christie AB, Aref, MK, Allan AA, El-Muntasser IH, El Nagen M: Pregnancy hepatitis in Libya. Lancet 2: X27. 1976. IO Daneshbod K, Borazjani CR. Sajadi H, Hamidzadeh MM: Survey of maternal deaths in South Iran: Analysis of 96 autopsies. J Obstet Gynaecal Br Commonw 70: 1103, 1970. I I Dawn CS, Gupta N, Poddar DL: Avoidable factor\ in maternal deaths. J. Indian Med Assoc .59: 101, 1072.
Int J Gynaecol
12 Donohue JJ: Some facts and figures on urhani/.ation in the developing worlds. In Assignment Children 57/5X. UNICEF, 1211 Geneva IO. IYX2.
Obstet 25
21
22
23
24 25
26 27
Epidemiology of maternal mortality in Addis Ababa: a community based study. Ethiop Med J 23: 7. IYXS. Megafu U: Causes of maternal deaths at the UNTH, Enugu. 1971-1972. W Afr Med J 23: X7, 1975. Megafu U: Jaundice. East Afr Med J 58: SOI. IYXl. Ogunbode 0: Jaundice during pregnancy in Ibadan. Nigeria. Int J Gynaecol Ohstet 16: 289. 1970. Ojo OA, Savage VY: A ten year review of maternal mortality rates in University <‘allege. Ibadan, Nigeria. Am J <;ynecol Ohstct I IX: .S17. I Y74. Rao KB: Maternal mortality in a teaching hospital in Southern India: A 13 year study. Obstet Gynecol Jh: 397, 197s. San-S, Myint-M-S: Epidemiological criteria as indication ol non-A. non-B hepatitis in ;I community. I_ancet 2: 828, 1985. I’he (‘it! (‘ouncil Addis Ahaha. Ethiopia: Progl-amme the Outline I 14X-bI YX7): A pt-ogramme of
Address for reprints: Barhara E. Kwast, M.T.I).. Maternal and Child Health World
Health Organization
1211 Geneva 27 Switzerland
.
Ph.D.
Federation
VIRAL ADDIS
of Gvnaecology
& Obstetrics
HEPATITIS AS A MAJOR ABABA, ETHIOPIA
B.E. KWAST*
CAUSE
OF MATERNAL
MORTALITY
IN
and J.A. STEVENS
Emory University School of Medicine, Atlanta, Georgia 30322 and Research and Statistics Branch, Division of Reproductive Health, Center for Health Promotion and Education, Centers for Disease Control, Atlanta, Georgia 30333 (USA) (Received (Accepted
August llth, 1986) September 1 lth, 1986)
Abstract
through education, better hygiene, proved sanitation are discussed.
Kwast BE and Stevens JA (Emory University School of Medicine, Atlanta, Georgia 30322, formerly Addis Ababa University, Ethiopia and Research and Statistics Branch, Division of Reproductive Health, Center for Health Promotion and Education, Centers for Disease Control, Atlanta, Georgia 30333, USA) Viral hepatitis as a major cause of maternal mortality. Int J Gynaecol Obstet 25: 99-106, 1987 Causes of maternal mortality were investigated in Addis Ababa, Ethiopia, from September 1981 to September 1983. Viral hepatitis ranked third among the leading causes of maternal mortality behind septic abortion and puerperal sepsis. There were 26 deaths from viral hepatitis during the 2-year study period for a hospital maternal mortality rate of 91 .(I per 100,000 live births. Although 30% of women who died of all maternal causes received antenatal care in Addis Ababa, only 13% of women who died from viral hepatitis in our hospital study received antenatal care. Low socio-economic status (SES) has been shown to be associated with low antenatal care utilization and with an increased risk of protein malnutrition. Malnut&ion is considered a predisposing factor for liver damage. Suggestions for reducing hepatitis transmission and maternal mortality 0020-7292/87/$03.50 (9 1987 International Federation Puhlkhed and Printed in Ireland
of Gynaecologv
& Obstetrics
and im-
Keywords:
Ethiopia; hepatitis; Viral Maternal mortality; Non-A, Non-B hepatitis; Confidential inquiries; Folk beliefs.
Introduction Women who contract viral hepatitis during pregnancy, especially during the second and third trimesters, are more likely to die from the disease than are non-pregnant women. Maternal mortality associated with viral hepatitis has been described in the developing countries of Ghana, Libya, China, Iran, Nepal, India, Ethiopia and Nigeria [2,6,8,9,13,20,2 I ,23,27]. Thr: case fatality rates observed for pregnant women with viral hepatitis ranged from IO% to 45%. However, the contribution of viral hepatitis to overall maternal mortality has not been well documented. The maternal mortality rate from viral hepatitis and its rank in comparison with other main causes was studied in Addis Ababa, Ethiopia, from September IOX I to September 1983. This paper presents descriptive data regarding maternal mortality resulting from viral hepatitis, information about the folk beliefs surrounding
IO0
Kwast and
Stevens
the causation and treatment of this disease, and three case histories illustrating the effect of these beliefs on the utilization of appropriate medical care. Rackground
The Ethiopian capital, Addis Ababa, located at an altitude of 2408 m, had a population of 1,154,459 as of July 1982 [16]. The population growth rate of 5% per year has resulted in critical problems, especially housing and sanitation. The mean per capita income in Addis Ababa is estimated at U.S. $75 per month [23]. The Ethiopian Ministry of Health has a policy of providing medical care free of charge for persons with a monthly per capita income of less than U.S. $25. This may be understood as defining a group with the lowest SES. In 198 1, 79% of Addis Ababa’s population lived under disadvantaged conditions [ 121. It was estimated in 1981 that only 6% of the country’s population had access to safe water. The Ethiopian government’s goal is to supply 35% of the rural and all of the urban population with safe drinking water by the year 1990 [26]. Cultural
beliefs
Jaundice associated with hepatitis has long been recognized in a number of Ethiopian provinces, including Shoa Province, where Addis Ababa is located. Hepatitis, called “yewof beshta” (bird’s disease), is believed to be transmitted by a “big night bird,” either by its urine falling on a person outside at night or early in the morning or simply by the bird circling above the person three times. The bird, described as having a wingspan resembling a pair of outstretched hands, is actually a bat [l]. Traditional treatment consists of eating a variety of boiled roots or leaves or eating a mixture of dried bat meat and herbs. The superstitions regarding causation and treatment of jaundice associated lnt J Gynaecol
Obstet 25
with hepatitis keep people from seeking appropriate ‘and timely medical treatment. Methods
The study of maternal mortality associated with viral hepatitis in Ethiopia was conducted as part of a Maternal Mortality Review Committee under the auspices of the medical faculty of Addis Ababa University. From September 1981 to September 1983, data on 198 maternal deaths were collected from the records of five city hospitals, the only institutions offering obstetric services under the Ministry of Health’s administration. The methodology of the confidential inquiry, modeled on the British system, has been described elsewhere [ 151. Of the 198 maternal deaths, 26 were classified as being associated with viral hepatitis. This diagnosis was determined by a physician from the detailed history and the clinical examination taken at the time of admission. Criteria for diagnosis of viral hepatitis included the manner of onset of jaundice-specifically, whether it was preceded by acute febrile illness or associated with loss of appetite, vomiting, gastrointestinal upsets, and general malaise. No serological tests were done. Serum transaminase was determined for five patients, bilirubin levels were determined for three and alkaline phosphatase was patients, determined for four patients. The 26 maternal deaths associated with viral hepatitis did not include any deaths from fulminating puerperal septicemia, relapsing fever, eclampsia, or possible malaria. None had a history of previous blood transfusion. Results
The five city hospitals registered 28,583 live births and 26 maternal deaths from viral hepatitis during the 2-year study period. The hospital maternal mortality rate for viral hepatitis was 91.0 per 100,000 live births.
Viral hepatitis and maternal
Of the 26 maternal deaths from viral hepatitis, 16 occurred in the first year of the study and 10 in the second year. The distribution of deaths from 1981 through 1983 did not show a seasonal variation. Table I gives selected characteristics of the women who died from viral hepatitis compared with hospitalized women who died of all other causes. Fourteen viral hepatitis patients (54%) were 30 years old or older versus 49 (28%) of patients in the comparison group. Twenty-seven percent of the women who died from hepatitis was para 6+ compared with 12% of women who died from other causes. The mean per capita income, known for 13 women who died of hepatitis, was to U.S. $20 per month. equivalent The average level of education, known Table 1. Selected characteristics of women who died from viral hepatitis compared with all women who died from other causes, Addis Ababa, September 1981-September 1983.
Characteristics
Viral hepatitis n=26 (%)
All other n= 172
causes (%)
Age (years) 14-19 20-24 25-29 30-34 235 unknown
0 5 4 9 5 3
(19) (16) (35) (19) (11)
35 42 38 19 30 8
(24) (22) (11) (18) (5)
Parity 1 2-3 4-5 zh unknown
3 7 4 7 5
(11) (27) (16) (27) (19)
63 41 24 21 23
(37) (24) (14) (12) (13)
Antenatal care yes no unknown
2 14 10
(0)
(8) (54) (38)
36 62 74
(20)
(21) (36) (43)
2 3 7 14
(8) (12) (27) (54)
6 24 33 109
(3) (14) (19) (63)
IOI
for 12 women, was 2 years of elementary school, although two women had some secondary school education. Information on water sources and on toilet facilities was known for 11 and 13 families, community standpipes were respectively: used by nine families (82%) and river water by two families (18%); pit latrines were used by eight families (62%) and open fields by five families (38%). Characteristics related to gestation and labor are described in Table II. Six deaths occurred in late pregnancy before the start of labor (antepartum). Two women died before giving birth during labor (intrapartum), and 16 died after having spontaneous vertex deliveries. Most patients had signs and symptoms of encephalopathy and gastrointestinal and genitourinary tract bleeding. The mean hemoglobin level, known for 10 women, was 12.6%. Five of 19 patients for whom this information was known had hepatomegaly and four developed positive chest findings after adTable II. of women September
Selected characteristics who died from viral 19X1-September 1983.
from labor and delivery hepatitis, Addis Ahaba.
Characteristics
Number
Gestation 2nd trimester 3rd trimester unknown
2 20 .l
Admission-onset of labor in labor on admission ~6 h 6-12 h 12-18 h not applicable (died antepartum) delivered at home unknown
interval
(n = 26) --
3 2 3
I 6 3 x
interval
Admission-death
Family Planning used aware/not used awareness not known/not used no information
mortality
(h)
61
2
2-23
5
24-36
5
37-48
h
49-120
3
unknown
5 --
Inr .I Ciynaecol Obster
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mission. Patients sought medical care late, a mean of 10 days after the onset of symptoms. All but two patients were afebrile and in precomatose or comatose states on admission. The consequences of these delays and of the high frequency of coma was a mean admission-to-death interval of 33 h. All women who delivered had spontaneous onset of labor. Of those women who went into labor after admission, the mean admission-to-onset of labor interval was 8 h. Eight women had severe postpartum hemorrhage. Of the 16 women who delivered, 10 had stillbirths, and 2 of the 6 live births died within 24 h after delivery. Fetal wastage was 75%. The following case histories illustrate the impact of the folk beliefs about viral hepatitis on maternal health at the time this study was conducted. Case one A 2%year-old, para 3 woman was admitted in a prehepatic coma 4 days after home delivery of a full-term, live female baby who was attended by a traditional birth attendant. The woman and her husband had no formal education. Their monthly per capita income was equivalent to U.S. $18. A history revealed that the patient had discoloration of the sclera and dark yellow urine for 8 days. One day before admission the patient had become restless, irritable, and confused. Physical examination revealed a blood pressure of 120/60 mmHg and a pulse rate of 72 beats/min. The patient was afebrile, her lungs were clear, there was no hepatomegaly, her uterus was well contracted, and there was no vaginal bleeding. There was some central nervous system depression. Laboratory findings were hemoglobin 10.8 g%, leucocytes 14,80O/ml, and platelets 131,00O/ml. Hemoparasites for relapsing fever and malaria were negative. The patient became confused and restless during the next 24 h and went into a deep coma. Forty-eight hours after admission she Int J Gynaecol Obsrer 2.5
had convulsions. The patient died 55 h after admission, on the sixth postnatal day. Home visits were carried out as time permitted. The family was visited several months later to learn more about their living conditions and the survival of the child. The people lived in close proximity in a typical compound where small houses enclosed a courtyard. Water was obtained from a community standpipe. Toilet facilities consisted of a shared pit latrine. Neighbors explained that the deceased woman’s infant daughter was well and that a collective effort was made to care for her children when the father was away. It was learned that the deceased woman had bled heavily after delivery. The neighbors had noticed her illness with the characteristic yellow eyes and dark urine. Although they had known pregnant women to die from “bird’s disease,” they did not believe the hospital could treat it effectively.
Case two A 24-year-old women, gravida 3, para 2, had developed jaundice and loss of appetite for which she took traditional medicine. When the medicine proved ineffective, she went to the district hospital 12 days after first experiencing symptoms. She was admitted to the district hospital but after 2 days was referred to a city hospital 80 km away when she started to become confused. The patient arrived at the city hospital in hepatic coma secondary to infectious hepatitis. She was febrile. Her blood pressure was 110/70 mmHg and her pulse rate was 140 beats/min. Her lungs were clear. Central nervous system examination revealed hyperextension and rigidity of both upper and lower extremities and neck rigidity. The fundal height corresponded to 36 weeks gestation. There was no audible fetal heart beat. Eighteen hours after admission the patient’s chest was full of secretions and she was bleeding from the nasopharynx. Labor
Viral hepatitis and maternal mortality
had started but there was antepartum hemorrhage and the patient went into shock. An hour later, the patient was in the second stage of labor but had not given birth when she died, 20 h after admission. No home visit was carried out because the women came from outside Addis Ababa. Case three
A 23-year-old woman, gravida 3, para 2, had received regular antenatal care beginning at 16 weeks gestation. She was 1.6 m tall and had gained 6 kg during her pregnancy. She was married and had an 1 lth grade education. Her husband was a college graduate with a technical job who earned the equivalent of $300 in U.S. currency per month. On admission, the patient gave a history of 6 days of fever, loss of appetite, vomiting, change of urine color, and pruritis. Her son had jaundice at that time. The physical examination revealed mild jaundice. Her blood pressure was 1 lo/90 mmHg and her pulse was 96 beats/min. The liver was palpable 2 cm below the right costal margin. The patient was in labor. The size of the uterus corresponded to 39 weeks gestation, the fetal lie was longitudinal, and the presentation was cephalic. The head was engaged and the fetal heart rate was 132 beats/min. Labor progressed well, and 11 h after admission the patient had a spontaneous vertex delivery of a live male infant weighing 3350 g. The placenta and membranes were expelled with minimal blood loss. Postdelivery treatment included prophylactic intravenous infusion of 5% dextrose/water with vitamin Blz. However, 24 h after delivery the patient developed bloody diarrhea. She was fully conscious and was kept on bed rest. The following day she complained of abdominal pain and backache. Eighty-four hours after delivery the patient developed a hepatic precomatose condition. Laboratory findings were hemoglobin 1 I .W”, SGOT 2 150 Cabaud units/ml, SGPT 610 Cabaud units/ml, total
I 03
bilirubin 10 mg/ 100 ml, and direct bilirubin 5.8 mg/lOO ml. She was transfused with two units of blood but on the fifth postnatal day she became comatose. Chest examination revealed scattered rhonchi. There was rigidity in the upper extremities. Gastric aspirate produced 400 ml of coffee-ground material. The patient died on the fifth postnatal day. During the home visit 9 months later, it was learned that the infant of the deceased women was healthy. The deceased women’s mother knew that her daughter had had “bird’s disease,” which the mother knew could be fatal in pregnant women. Because both’ women believed that the modern health system had no cure, the daughter had taken traditional medicine for the illness. Discussion
The hospital maternal mortality rate for viral hepatitis during the study period was 91.0 per 100,000 live births, whereas the maternal mortality rate in the city of Addis Ababa was 76.5 per 100,000 as determined through a household sample survey [16]. This difference would be expected because women who deliver at home and develop complications are likely to be admitted to a hospital. Table III demonstrates that viral hepatitis and ruptured uterus each ranked as the third highest cause of maternal mortality in Addis Ababa. This is consistent with studies from Nigeria, Ghana, Malawi, and South Africa [2,3,7,20], which have ranked viral hepatitis among the six leading causes of maternal mortality. Most of the Ethiopian population experiences hepatitis A as a mild disease anti-HAV antibodies in and develops childhood, as evidenced by the demographic and serologic survey of viral hepatitis in 1983 [25]. This study found a hepatitis B marker prevalence of 42% overall and 76% among those over 14 years of age. Viral hepatitis in Addis Ababa appears to be endemic. There were 16 maternal deaths Int .I Gvnaecol
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Kwast and Stevens
Tabk III. study.
Comparison of maternal mortality rates (MMR) per 100,000 live births from major causes by country and year of
Country
Ethiopia Malawi” Nigeriai’ South Africa’ Nigeria“.’ Ghana’
Year of study
1981-1983 1977 1976-1977 1973-1975 1962-1971 1963-1967
Causes Septic abortion
Puerperal sepsis
Viral hepatitis
Ruptured uterus
Eclampsia
Hemorrhage
164.4 9.4
94.5 23.5 58.5 115.3 58.3 68.2
91.0 2.3 45.0 96.1 125.6 88.1
91.0 44.7 58.5 3.8 31.4 93.x
70.0 2.3 49.5 53.8 31.4 99.5
52.5 49.4 63.0 42.2 98.7 179.0
57.6 53.9 93.8
“See Ref. 6. “See Ref. 2. ‘See Ref. 4. “See Ref. 20. ‘MMR from severe anaemia: 152.6. ‘See Ref. 1.
from viral hepatitis during the first study year and 10 maternal deaths during the second year. No peaks occurred during the study period. Also, this study did not show a seasonal variation in the maternal deaths from viral hepatitis, although such a variation was seen in two other studies where high mortality rates resulted from epidemics [3,27]. Therefore, identifying the type of hepatitis is essential to apply appropriate intervention measures. Infections from non-A, non-B hepatitis as well as from hepatitis B are the most likely causes of hepatitis mortality during pregnancy [6,9,17,19,22]. Outbreaks of non-A, non-B hepatitis were reported among Ethiopians in Somalian and Sudanese the camps in 1985, showing refugee presence in these countries of a virus similar to the one in India (Mark A. Kane, pers. commun.). In early 1986, outbreaks of hepatitis, thought to be hepatitis B, were reported from relief shelters in Ethiopia (Mark A. Kane, pers. commun.). Studies should be continued and should incorporate serologic testing to determine the occurrence of different serological agents. Deaths from hepatitis B can be prevented by the appropriate use of hepatitis B vacInt J Gynaecol
Obstet 2.5
tine. Treatment of newborns could prevent acquisition of the disease and could eventually reduce maternal infection. Unfortunately, the current cost of hepatitis B vaccine prohibits its general use in Ethiopia. Hepatitis B is efficiently transmitted through unsterile needles and medical and dental equipment. Improving the sterilization procedures for needles and other medical items would have some impact on reducing mortality and morbidity from this disease. The possibilities for prevention of non-A, non-B hepatitis are more favorable. The form of this disease present in northern Africa and the Indian subcontinent has a fecal-oral route of transmission; improving hygiene and providing safe water would be viable intervention strategies [4,14,22]. Examining the safety of the present water system, as well as increasing the availability of safe water, is critical for this approach to be effective. Education is also an essential aspect of any preventive approach but will not succeed without sensitivity and respect for cultural attitudes. Folk beliefs surrounding hepatitis often conflict with a person’s perception of disease transmission. This in turn interferes with potential improvements in
Viral hepatitis and maternal
health behaviors and delays the receipt of timely medical care, as demonstrated by this study. Comparison of antenatal care use (Table I) suggests that women who died of viral hepatitis utilized these services less than did controls. Of all the hospitalized women who died of maternal causes other than hepatitis, 67% had not received antenatal care. The percentage was higher among the women who died from hepatitis but was the same for women who delivered in hospitals and survived. In contrast with this hospital population, a household survey found antenatal care coverage in Addis Ababa as a whole was 30% among women who died of maternal causes both in and out of the hospital and 70% among women who survived [16]. There also appears to have been a difference between the two groups in their use of family planning, although these data are difficult to interpret because no information was available for a large percentage of the women. Low SES has been shown to be related to comparatively low utilization of antenatal care [ 1.51. Information on income for 13 women showed that 11 had monthly per capita incomes below the Addis Ababa mean of U.S. $75 and therefore had low SES. Motivating women to attend antenatal clinics will contribute to improved maternal health. Although antenatal care will not directly prevent hepatitis, contact with a maternity service will benefit women by providing information in a number of areas: sanitation and hygiene, family planning, and health education and risk factors during pregnancy. Protein malnutrition, often found in con-
junction with low SES, is considered a predisposing factor for hepatocellular damage from hepatitis [6, lo]. In this study, 1 1 out of 13 women were of low SES and probably at risk for malnutrition, although anthropometric measurements were not determined. The literature reports that maternal mor-
mortality
105
tality is exceptionally high among women with hepatitis during the third trimester, following spontaneous labor and delivery [9,11]. Megafu, in Nigeria, has described a considerable reduction in mortality following induced labor in the third trimester [18]. Additional research is needed to determine if inducing labor in the third trimester might be a productive approach to decreasing these maternal deaths. One must be cautious in drawing conclusions based on hospital data because the population differs from the community at large. Continued research into viral hepatitis, further education of health care personnel regarding hepatitis transmission, and the provision of adequate health facilities with the laboratory staff and equipment for typing the disease are all important factors in understanding and ultimately controlling viral hepatitis. Conclusions
The high maternal mortality and fetal wastage attributable to viral hepatitis clearly shows that the problem of viral hepatitis in pregnancy needs to be addressed. Viral hepatitis will become of even greater relative importance as the other major causes of maternal mortality, i.e. septic abortion, puerperal sepsis, ruptured uterus, and eclampsia, decline through the implementation of preventive strategies. Education, application of good hygiene, provision of safe water, and improvement in basic sanitation will all help prevent disease transmission. If the target of providing safe water for 35% of the rural population and all of the urban population by 1990 is accomplished by the Ethiopian government, it will go a long way toward reducing maternal mortality from viral hepatitis. Acknowledgments
The authors express thanks to Mark A. Kane, M.D., M.P.H., Centers for Disease Int J Gynaecol
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K wast and Stevens
Control, Atlanta, for his helpful discussion and criticism; to the members of the Maternal Mortality Review Committee: Widad Kidane-Mariam, M.D., Adane Gossa, M.D., Mekonnen Bekele, M.D., Seyoum Yoseph, M.D., and Leteberhan Mehari, R.N., R.M.; to Professor Edemariam Tsega and Frances Lester, M.D.; to the staff responsible for the hepatitis patients at the Black Lion Hospital and the Yekatit 12 Hospital in Addis Ababa; to all consultant obstetrician/gynecologists of the hospitals under the administration of the Ministry of Health for making case records available; and to Carol Cummings, Emory University School of Medicine, Atlanta, for secretarial help. References
13 Kane MA, Bradley DW. Shrestha SM, et al.: Epidemic non-A. non-B hcpatiti\ in Nepal. J Am Mcd A\soc 2.-i.?: 3140, 1984. 14 Khuroo, MS: Study of an epidemic of non-A, non-B hepatitis: Possibility of another hepatitis \ irus distinct from post-transfusion non-A. non-B type. Am J Med hX: 818. 1980. IS Kwast BE. Kidane-Mariam W. Saed EM. Fowkc\ FGR: Report on maternal health in Addis Ababa, Radda Barnen (Swedish Save the Children Federation). P.O. Box 3457, Addis Ababa, Ethiopja. lYX4. 16 Kwast BE, Kidane-Mariam W, Saed EM. Fowkes FGR:
17 18 19 20
Abate G: Ethiopian Traditional Medicine (Addis Ababa University, Addis Abaha, Ethiopia) Vol. 1, pp 334-339. 1980. Ampofo DA: Causes of maternal deaths and comments. Maternity hospital, Accra. W Afr Med J 1X: 75, 1969. Balachanran V: Maternal mortality in Kaduna 19641972. Nig Med .I 5: 366, 1975. Balayan MS, Andjaparidze AC, Savinskaya SS. et al.: Evidence for a virus in non-A, non-B hepatitis transmitted via the fecal-oral route. Intervirology 20: 23, 1983. Barford DAG, Parkes JR: Maternal mortality: A survey of 118 maternal deaths and the avoidable factors involved. S Afr Med J 51: 101, 1977. Borhanmanesh F, Haghighi P, Hekmat K, Rezaizadeh K, Ghavami AC: Viral. hepatitis during pregnancy. Gastroenterology 64: 304, 1973. 7 Bullough CHW: Analysis of maternal deaths in the central region of Malawi. East Afr Med J 58: 25, 1981. 8 Chen R-J: Maternal Mortality in Shanghai, China. Presented at Interregional meeting on Prevention of Maternal Mortality, Geneva. November I l-l S. IYXS (FHE. PMM/85.9.2). Y Christie AB, Aref, MK, Allan AA, El-Muntasser IH, El Nagen M: Pregnancy hepatitis in Libya. Lancet 2: X27. 1976. IO Daneshbod K, Borazjani CR. Sajadi H, Hamidzadeh MM: Survey of maternal deaths in South Iran: Analysis of 96 autopsies. J Obstet Gynaecal Br Commonw 70: 1103, 1970. I I Dawn CS, Gupta N, Poddar DL: Avoidable factor\ in maternal deaths. J. Indian Med Assoc .59: 101, 1072.
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12 Donohue JJ: Some facts and figures on urhani/.ation in the developing worlds. In Assignment Children 57/5X. UNICEF, 1211 Geneva IO. IYX2.
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Epidemiology of maternal mortality in Addis Ababa: a community based study. Ethiop Med J 23: 7. IYXS. Megafu U: Causes of maternal deaths at the UNTH, Enugu. 1971-1972. W Afr Med J 23: X7, 1975. Megafu U: Jaundice. East Afr Med J 58: SOI. IYXl. Ogunbode 0: Jaundice during pregnancy in Ibadan. Nigeria. Int J Gynaecol Ohstet 16: 289. 1970. Ojo OA, Savage VY: A ten year review of maternal mortality rates in University <‘allege. Ibadan, Nigeria. Am J <;ynecol Ohstct I IX: .S17. I Y74. Rao KB: Maternal mortality in a teaching hospital in Southern India: A 13 year study. Obstet Gynecol Jh: 397, 197s. San-S, Myint-M-S: Epidemiological criteria as indication ol non-A. non-B hepatitis in ;I community. I_ancet 2: 828, 1985. I’he (‘it! (‘ouncil Addis Ahaha. Ethiopia: Progl-amme the Outline I 14X-bI YX7): A pt-ogramme of
Address for reprints: Barhara E. Kwast, M.T.I).. Maternal and Child Health World
Health Organization
1211 Geneva 27 Switzerland
.
Ph.D.