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The Relationship Between Fertility and Maternal Mortality Susan Zimicki Matemal mortality is much higher in developing than in developed countries (Mahler, 1987~. This is clearly a function of a number of factors, including the greater risk inherent in pregnancy and delivery owing to lack of adequate medical care; the greater prevalence of infectious diseases, which are cofactors in some deaths; and the higher incidence of pregnancy. Because high-mortality countries are those with the least reliable vital statistics, little information is available about levels and risk factors. Provision of family planning services has been proposed as one way to reduce maternal mortality (Rosenfield and Maine, 1985~. The argument is that use of family planning services will reduce the absolute number of pregnancies and will allow shifts in the timing of pregnancy from high-risk to lower-risk ages and from shorter to longer interbirth intervals. This paper will review the information available about the effects of parity, age, and birth intervals on maternal mortality and morbidity, with particular attention to some of the common complications of pregnancy and the major causes of death. Winikoff and Sullivan (1987) have examined limits of the possible effect of family planning programs in reducing maternal mortality, and Trussell and Pebley (1984) have quantified the possible impact of changing age and parity distributions on fertility. In addition to including more recently available population-based information, this paper considers in detail some of the Susan Zimicki is research director of the HealthCom Evaluation, Annenberg School of Communi- cations and Population Studies Center, University of Pennsylvania. 1

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2 SUSAN ZlMlCKI major mechanisms through which maternal mortality occurs and how they are related to fertility. DEFINITIONS AND MEASUREMENT ISSUES Measures A number of different measures of maternal mortality are commonly used, the most important being the maternal mortality ratio and the maternal mortality rate. The numerator for both is the same: the number of maternal deaths occurring in a given period. Most studies adhere to the International Classification of Disease, ninth revision (ICD-9), definition of maternal death in including the deaths of women within 42 days of termination of pregnancy. Some older studies may include deaths that occurred up to 90 days after the termination of pregnancy, in accordance with the Guide of Maternal Deaths Studies published by the American Medical Association (1964~. The maternal mortality ratio is the ratio of maternal deaths per live births (venously 1,000, 10,000, or 100,000; unless noted otherwise a metric of 1,000 is used for ratios and rates in this paper). Although the denominator should ideally be pregnancies, the impossibility of obtaining accurate counts of fetal losses and stillbirths has necessitated using live births. According to the World Health Organization (WHO) (1985), in countries with low induced-abortion rates, the number of live births is within 10 percent of the number of pregnancies. This ratio measures the probability of maternal death, the obstetric risk. The maternal mortality rate is simply a cause-specific death rate: maternal deaths/women of reproductive age (variously 10 to 49, 15 to 44, 15 to 49 years old). This rate is a function of the incidence of pregnancy as well as the risk inherent in pregnancy. Thus, the maternal mortality rate is linked to the maternal mortality ratio through the general fertility rate Births/1,000 women of reproduc- tive age). Two extensions of the maternal mortality rate have been used as measures of maternal mortality: (l) the proportion of all-cause mortality for women of reproductive age that is attributable to maternal mortality and (2) the lifetime risk of maternal mortality, calculated as reproductive-span maternal mortality rate (Measham and Herz, cited in Fortney, 1987~. It is important to consider the effects of age and fertility structure differences on these measures. Obstetric risk varies greatly with age, as does the incidence of pregnancy. Thus, populations that have different age structures andlor different age-specific fertility rates may have different crude maternal mortality ratios even when they have similar age-specific ratios (see Fortney, 1987, and Graham and Airey, 1988, for examples). Whether or not the crude ratios are different depends on whether the ages of highest obstetric risk are those in which the population or fertility differences reside. The crude maternal mortality rate and the measures based on it are even more sensitive to these structural differences.

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FERTILITY AND MATERNAL MORTALS 3 Unfortunately, nearly all studies report only crude maternal mortality ratios and rates, making comparisons across populations or even of the same population at successive times questionable. Sources of Data Maternal mortality is underestimated even in countries with excellent vital registration systems; official statistics from countries where maternal mortality is high seriously underestimate the true level (WHO, 1987~. Better data are avail- able from three sources: population-based studies, hospital population studies, and case series. Population-based studies provide the least biased estimates of maternal mortality. They allow nearly complete counts of live births and mater- nal deaths. Because of their prospective nature they include deaths that occur more than a week after delivery and probably include most of the deaths due to induced abortion. There are very few population-based studies concerning mater- nal mortality: six from Bangladesh (Chen et al., 1975; Lindpaintner et al.,1982; Khan et al., 1986a; Alauddin, 1987; Koenig et al., 1988; Faveau et al., 1988~; one from Ethiopia (Kwast et al., 1986~; one from Egypt (lPortney et al., 1985~;i one from the Gambia (Greenwood et al., 1987~; and one from Jamaica (Walker et al., 1985~. Preliminary results from a population-based study in India are available (Bhatia, 1985~. Although the Medical Research Council (MRC) project in the Gambia and the Machakos project are population laboratories that have yielded excellent information on a number of topics, maternal mortality in both areas has been almost completely eliminated because of care provided by the project (Lamb et al., 1984; Voorhoeve et al., 1979), and so these studies are not included. In addition, one hospital-based study from Lusaka, Zambia (Mhango et al., 1986), arguably covers a sufficient portion of the population (85 percent of births, 90 percent of deaths) to be considered a population-based study. Unfortunately, the number of deaths in each study is generally very small, so estimates by specific cofactors are unstable. With regard to morbidity the WHO collaborative studies on family- formation patterns and health provide population-based information about anemia and uterovaginal prolapse in nine countries (Omran et al., l981a,1981b). In addition, one study from Jerusalem (Harlap et al., 1971) concerns obstetric interventions, and one from the Philippines (Raymundo, 1987) concerns morbidity during the last pregnancy. Hospital population studies, particularly those from referral hospitals, provide less accurate estimates of the incidence of maternal mortality or morbidity than do population-based studies. They reflect the experience of only a proportion of the population during only part of the risk period at the time of and immediately after iThe companion study to the one carried out in Egypt was carried out in Bali. It is not included as a population-based study because the ascertainment rate of deaths was estimated as 50 percent at most. With that level of underestimation, it seems unlikely that the information is representative.

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4 SUSAN ZIMICK] pregnancy outcome. Many of the hospital-based studies report only the crude maternal mortality ratio and limit further analyses to the series of deaths. A few report case-fatality rates for various complications. If the assumption can be made that the deaths in hospitals are representative of all maternal deaths or the way in which they are unrepresentative can be identified, then some examination of the proportional contribution of various causes becomes worthwhile. Case series reports about a series of deaths, either due to any maternal cause or to a specific cause, such as ruptured uterus, eclampsia, or hepatitis-can provide valuable information about incidence and case-fatality rates. Unfortu- nately, most contain no description of the population from which the cases are drawn. However, series selected because of the presence of a risk factor (e.g., the Arkutu, 1978, series of primigravidae) rather than an outcome and those in which the maternal deaths are compared to a subsample of the hospitalized population represent one of the most efficient ways of obtaining information about maternal mortality. Problems of Measurement AS noted above, the maternal mortality ratio as defined by the WHO is already an approximation of the measure of interest. However, the more serious problems in measurement arise from incomplete ascertainment of either the number of deaths or the number of related live births. Deaths that occur before delivery, such as those due to ectopic pregnancy, may not be recognized as maternal deaths. Additionally, those due to induced abortion may be misrepresented because of shame or fear of prosecution: in one series of cases of women who came to a hospital with tetanus "all [22] postabortal cases followed criminal abortion, although in only 10 cases was the interference admitted by patients or their relations" (Adadevoh and Akinla, 1970~. Another group of deaths that is easily missed, especially in hospital-based studies, are those that occur some time after delivery. The population-based study in Tangail (Alauddin, 1987) shows 15 percent and that in Jamalpur (Khan et al., 1986a) shows 27 percent of deaths occurring more than a week after delivery. Depending on the time period of interest, retrospective population-based stud- ies may underestimate both maternal deaths and live births. A valid count of live births is generally less of a problem for prospective population-based studies but exists nevertheless. Comparison of the crude birth rate for the Jamalpur prospec- tive study with the national rate suggests an underreporting of up to 10 percent of the births (Khan et al., 1986a); the same comparison for the Tangail prospective study suggests underreporting of 27 percent (Alauddin, 1987~. The problem of estimation of the denominator is most crucial, however, with regard to hospital-based studies. In developing countries many women do not usually deliver in hospitals, although they may be brought there if the delivery is complicated. Hospital-based maternal mortality ratios in urban areas with easy

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FERTILITY AND MATERNAL MORTALS 5 access are probably overestimates because a larger proportion of more difficult than normal deliveries is represented among deliveries. This tendency for hospi- tal populations to overrepresent abnormal or complicated cases is exacerbated in the case of referral or teaching hospitals in large cities, which receive not only all the self-referred emergency deliveries but also patients referred by other health facilities. As most hospital reports are generated by teaching or referral hospitals, the reported maternal mortality ratios are likely to be overestimates. One study reported two ratios, the first 16.7, calculated on the basis of hospital births, the second, 3.9, on the basis of births in the city (Rag, 1975~.2 Unfortunately, the number of births in the hospital catchment population often cannot be ascertained or estimated; this might happen, for example, if there are several hospitals in a city. The representativeness of the hospital population can be assessed using two observations that are frequently reported: the proportion of admissions that are emergency or unhooked and the proportion of deaths that occur soon after admis- sion. In areas where access to a hospital is restricted (because of distance, cost, or social barriers), a greater proportion of women experiencing difficulty during delivery will die at home. Ratios reported by these hospitals may represent underestimates; in addition to the advantage of medical care at the time of delivery, the population delivering in hospitals may have had greater than average exposure to antenatal care and may represent a more socioeconomically advan- taged portion of the population. One extreme example is from the Medical Research Council (MRC) study area in the Gambia: the maternal mormlity ratio for the period 1951-1975 was reported as about 10 (Billewicz and McGregor, 1981), but during 8 years after the establishment of a continuous medical service there were no maternal deans, although 16 would be expected if the established ratio had prevailed (Lamb et al., 1984~. An additional problem of smaller rural facilities is that caseloads are often insufficient to produce stable estimates of morality. While estimates of maternal mortality ratios from hospital-based studies may be biased, they provide a useful supplement to the few estimates ob~ne`1 from population-based studies. However, because of the very small numbers of deaths identified in population-based studies,3 using hospital-based studies is crucial for examination of the causal mechanisms involved in high maternal mortality. 2In the light of the probable large effect of selection bias, the problem of maternal mortality ratios calculated using deliveries rather than live births in the denominator is minor, but a number of hospital reports (and one population-based study: Greenwood et al., 1987) use deliveries. While this is more correct epidemiologically, as it is a better estimate of the population at nsk, it deviates from the . . . . . ntematlona. . c ,elmlt~on. gibe total number of deaths reported in the nine identified population-based studies is 936; 630 of these come from two countries Egypt and Jamaica with the lowest and third lowest reported maternal mortality rates in the series.

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6 SUSAN ZIMICK] If all the maternal deaths from an area occur in a hospital, the proportion of mortality associated with each cause of interest can be determined accurately (apart from classification bias), even when the maternal mortality ratio cannot be determined. This situation probably occurs more frequently when a large propor- tion of the population is already delivering in a hospital for example, in Lusaka (Mhango et al., 1986~. When it does not occur, three types of deaths are most likely to be excluded. First, many early-pregnancy deaths occur at home: in Addis Ababa 6 of 13 aboriion-associated deaths occurred at home. Some hospital studies explicitly exclude all early-pregnancy deaths (e.g., Chi etal.,l981; Hartfield, 1980) as well as those occurring after the woman has been discharged from the hospital, while a few simply do not report any (Balachandran cited in Armon, 1977; D'Cruz et al., 1986a). The second type of death apt to be omitted from hospital statistics comprises those due to indirect causes-not resulting from the complications of pregnancy itself but rather from a condition that is aggravated by pregnancy or one that is completely unrelated, such as a motor vehicle accident. Kwast et al. (1986) report hospital deaths for 67 percent of those dying of obstetric causes but only 38 percent of those dying of indirect causes. Even if they die in hospitals, women who die of indirect causes may, for example, die in the medical ward and never come to the attention of those who report "maternal mortality." Finally, women are more apt to be seen in a hospital if the delivery complication "affords relatives the time to discuss the merits of hospital admission" (Hartfield, 1980) and the hospital is sufficiently close to the woman's home. One way to estimate this effect is to examine the ratio of deaths from obstructed labor and hemorrhage to those from hypertensive disease; this ratio tends to be much higher in hospital- based studies than in population-based ones. In addition to these types of inclusion bias, hospital series reports are also subject to classification bias. For example, deaths resulting from cephalopelvic disproportion and abnormal presentations leading to prolonged labor and uterine rupture might be classified as due to ruptured uterus if the rupture is identified, as due to hemorrhage if extravaginal bleeding is a prominent feature, or to sepsis if death is delayed some time after the onset of labor. Many maternal deaths are associated with a number of complications; for example, of 219 deaths in Zaria only 86 could be attributed to a single condition, while the rest were associated with two or more (Harrison and Rossiter, 1985~. This then is the situation: maternal mortality is inherently difficult to measure; the summary measures commonly used obscure any differences between popula- tions that might be due to fertility patterns as opposed to other sources of risk; the best (though still flawed) data come from a few extremely small studies in restricted geographic areas; and the largest source of data is subject to selection and classification biases that cannot easily be controlled for because they are unquantifiable except in He very particular circumstances of each study. Even with these drawbacks, fairly clear patterns are apparent both in terms of the

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FERTILITY AND MATERNAL MORTALl7Y 7 geography of level and causal components and with reference to the relation between fertility and maternal mortality. WORLD PATTERNS Population and hospital-based studies from countries selected because they had several studies show distinct differences in the levels of maternal mortality in different regions CTable 1~. The highest mortality ratios are from the population- based studies in the Gambia, where the overall ratio is probably between 10 and 20 per 1,000 births. Hospital studies from Nigeria and a population-based study from eastern Senegal (Pison, 1989) suggest that the risk in West Africa is gener- ally high, though perhaps closer to 10 than 20. The next highest mortality occurs in South Asia; from the population studies in Bangladesh and the population and hospital studies in India, a maternal mortality ratio of 4 to ~ seems most likely. Indonesia and Ethiopia probably have similar levels. The information from Tanzania suggests that the risk is slightly lower there, probably around 2 to 4, and the studies from South Africa suggest the same level. The three hospital-based studies in Lusaka, Zambia, are very consistent, and maternal mortality- at least in the city, where rates of prenatal care and hospital delivery are very high (Mhango et al., 1986) is most likely in the range of 1 to 2. The ratios now seen in Lusaka are beginning to approach those seen in Latin American countries in the early 1960s. More recent studies have shown ratios 10 times lower. Thus, if developing country regions are ranked by risk of childbearing, West Africa is clearly the area of highest risk, followed by South Asia, northern East Africa, and southern Africa. Latin America is clearly the region of lowest risk. ASPECTS OF FERTILITY AS RISK FACTORS FOR MATERNAL MORTALITY Fertility can be described in terms of age of first occurrence, total number of events, and interval between them. All of these factors are susceptible to family planning interventions; contraception can be used to delay the first pregnancy, lengthen the interval between binhs, and reduce the total number of pregnancies. Par ity/Gr av id ity The event that puts a woman at risk of maternal mortality is conception. Strictly, the relationship between fertility and maternal mortality should be de scribed in terms of pregnancies. Some risks (e.g., hemorrhage from ruptured ectopic pregnancy, complications of induced abortion, amplification of the risk of infectious diseases) accrue to pregnancy well before delivery, while others are

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8 SUSAN ZIMICK] TABLE 1 Matemal Mortality Ratio Per 1,000 Binhs From Selected Countries City Population Hospital Year Reference Gambia Ethiopia Tanzania Gambia Indonesia Bangladesh India Keneba Mandua North Bank Addis Addis Ababa Addis Ababa Kilimanjaro Dar es Salaam Moshi Mwanza Lusaka Lusaka Lusaka South Africa Pietennantzburg Durban 12 hospitals Bali Matlab Matlab Matlab Tangail Jamalpur Calcutta Calcutta Madurai Bombay urban Bombay rural Anantapur rural 8.7 Anantapur urban 5.5 Bogota 1.3 Call 2.2 Caracas 1.0 Cumana Ribeirao Preto Sao Paula Campinas Santiago Santiago Colombia Brazil Chile 10.5 9.5 22.0 4.6 7.2 7.7 5.7 5.1 5.7 6.2 8.4 5.9 3.9 16.5 4.0 2.4 0.6 0.9 3.2 1951-75 Billewicz and McGregor (1981) 1951-75 Billewicz and McGregor (1981) 1981-83 Greenwood et al. (1987) 7.8 1980 (Frost) cited in Kwast et al. (1986) 1981-83 6.9 1981-83 3.2 1971-77 2.1 1974-77 2.6 198~81 2.3 1982 1.5 1974 1.6 1974-78 1.2 1982-83 1.5 1973-75 2.1 1975-82 3.9 1977-80 198~82 1967~8 1968-70 1982 0.3 0.3 Kwast et al. (1986) Kwast et al. (1986) Armon (1979) M~navalye et al. (1980) Janowitz et al. (1984) Janowitz et al. (1984) (Hickey) cited in Hanfield (1980) Parole) cited in Boerrna (1987) Mhango et al. (1986) Barford and Parlces (1977) Melrose (1984) Chi et al. (1981) Fortney et al. (1985) Chen et al. (1975) Chen et al. (1975) Iindpaintner et al. (1982) 1982-83 Alauddin (1987) 1982-83 Khan et al. (1986) 195~58 Dawn et al. (1972) 1966 68 Dawn et al. (1972) 196(}72 Rao (1975) 1961~9 Shah et al. (1971) 1961 -69 Shah et al. (1971) 1984-85 Bhatia (1985) 1984~5 Bhatia (1985) 1962~4 Puffer and Griffith (1967) 1962~4 Puffer and Griffith (1967) 1962~4 Puffer and Griffith (1967) 1978-80 Janowitz et al. (1982a) 1962-64 Puffer and Griffith (1967) 1962~6 Puffer and Griffith (1967) 1977-79 Janowitz et al. (1982b) 1962~4 Puffer and Griffith (1967) 1977-78 Janowitz et al. (1982a)

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FERTI~TY AND MATERNAL MORTALS 9 inherent in delivery itself. Most of the studies concerning maternal mortality report parity-specific mortality; a few report rates by gravidity.4 All the population-based studies indicate and results from hospital studies generally confine that the flat birth and births of high order are strong risk factors for maternal mortality (Table 2~. These studies indicate a I- or U-shaped risk with parity: high during the first pregnancy, lowest during the second or third, and high again by the fifth pregnancy. A similar pattern is found for gravidity, with an even stronger relative risk for first pregnancies relative to later-order pregnancies than is observed for first births. Corroboration for the higher risk of first deliveries comes from the population- based morbidity study carried out in West Jerusalem, where the obstetric inter- vention rate was calculated by parity (Harlap etal., 1971~. Obstetric interventions included any specialist intervention at any stage of labor, including surgical or medical inductions of labor, forceps or vacuum deliveries, breech deliveries, cesarean sections, and other major third-stage interventions; while probably an overestimate, this measurement does indicate potential mortality in the absence of medical care. Both the parity-specific rates and the ratios (adjusted for age, ethnicity, and hospital) indicate about a 70 percent higher risk for first than for second births (Table 3~. Except for very high parity births (10+), this study does not confirm the excess risk of multiparty. This is surprising in light of the very clear enhanced risk of malpresentation for multiparous women noted by, for example, Faundes et al. (1974~: 3.4 breech presentations per 1,000 women of parity 0, 10.1 for panties 1 and 2, 14.4 for parities 3 and 4, 17.5 for parities 5 and 6, and 19.0 for parity 7+. A review of a series of 50,057 deliveries, including 5,785 to grand multiparous (parity 7+) women in Haifa, Israel (Fuchs et al., 1985), yielded a rate of malpre- sentation of 11.9 per 1,000 for the grand multiparous women in contrast to a rate of 3.3 per 1,000 for women of lower parity. A study from the Sudan (Aziz, 1980) comparing 2,049 primiparous, 3,679 multiparous, and 3,130 grand multiparous (5+) women found slightly higher rates of abnormal presentation for grand multiparas (14 percent compared to 9 percent for multiparas and 9.5 percent for primiparas). This same study found more toxemia among primiparas than other women (10.8 percent vs. 7.8 percent for multiparas and 8.5 percent for grand multiparas), more anemia among grand multiparas (7.4 percent) than other women (4.5 percent), and a clear increase in the risk of antepartum hemorrhage with parity (primiparas 1.3 percent, multiparas 1.9 percent, grand multiparas 4.5 percent). Al-Sayegh and Hathout (1974) in Kuwait obtained similar results for antepartum hemorrhage (0.1 percent for women of parities 1 to 5, 1.2 percent for parities 6 and 7, and 4.2 percent for parity 8+), but they observed lower rates of abnormal presentation-only 5.1 percent for 4Parity is the number of previous live births; gravidity is the number of previous pregnancies. formation about parity is probably more accurate than that about gravidity.

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TO SUSA}VZIMICK] TABLE 2 Mortality Per 1,000 live Births by Parity and Gravidity Prior to Current Pregnancy Gravidity Tangaila Jamalpuri MatlabC Matlab~ Addis AbabaC Jamaica' Gambia8 Parity G P P G P G P P P P 0 5.5 3.8 33.8 12.7 9.9 9.7 9.5 13.3 0.8 28.6 1 4.3 3.7 4.2 2.4 2.8 4.1 3.8 8.1 0.6 11.9 2 3.4 4.2 2.6 2.3 3.1 3.1 3.2 0.8 3 3.8 5.7 7.6 2.4 4.8 3.1 3.4 0.8 4 7.7 2.3 4.7 4.3 4.9 5.2 5.4 0.9 5 9.1 9.1 14.2 6.0 5.9 3.4 3.7 3.0 1.3 45.5 6 14.9 6.8 5.2 5.9 4.9 7 10.8 14.9 7.4 7.2 6.9 6.8 8 6.5 7.3 8.3 10.4 9+ 6.6 7.8 8.2 Total 5.7 5.7 6.2 5.7 5.7 5.5 5.5 4.9 1.1 22.3 Note: Close examination of the population-based studies indicates some confusion about the definitions of parity and gravidity. Chen et al. (1975) label groups of women by their status prior to the current pregnancy and report, as might be expected, fewer deaths and live births among women who had never had a pregnancy than among those who had never had a live birth (but who might have had a prior pregnancy). Alauddin (1987) also reports both parity-specific and gravidity-speciD~c ratios, but labels women with no previous live births panty O and those with no previous pregnancies gravidity 1. In addition, there seems to be a classification problem, as the reported ratios indicate 10 deaths among women who had no prior pregnancy but only 7 among those with no prior live birth. Walker et al. (1985) have classified women as to parity by considering the number of prior pregnan- cies lasting at least 28 weeks but not necessarily terminating in a live birth, including the current pregnancy. Thus all women who have never had a prior live birth are considered parity 1; in general, even after co'~c;ction for this difference, the panties of women in the Jamaica study will be slightly inflated relative to reported parities of women in the other studies. This study also includes deaths that occurred up to a year after delivery. In the population-based study from Ethiopia (Kwast et al., 1986), a note to the parity 0 rate indicates that it has been calculated per 1,000 nulliparous women. As the parity 1 through 5+ live births add up to the total number of live births in the study, it seems likely that the parity classification includes the current pregnancy, with deaths to women with no prior live birth being categorized as parity O if they did not survive to deliver and parity 1 if they delivered. This rate has been recalculated. Rates reported by Greenwood et al. (1987) are calculated over all pregnancies, as parity-specific numbers of live births are not available. Sources: aAlauddin (1987), bKhan et al. (1985), CChen et al. (1985), Koenig et al. (1988), CKwast et al. (1986),~aLker et al. (1985), and "Greenwood et al. (1987).

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FERRY AND MATERNAL MORTAR ~ ~ women of parity 8 or more. Their case series is, however, quite a bit smaller, including 2,060 women of parities 1 to 5, 494 of parities 6 and 7, and 446 of parity 8+. In a 1958-1960 multicenter study in the United States, Israel and Blazar (1965) reported a much higher rate of essential hypertension among grand multiparas (7+) (without controlling either for age or race), higher rates of uterine rupture and posq?ar~m hemorrhage, and significantly higher rates of placenta previa and placental absorption, but no difference in maternal mortality, presumably because of adequate hospital care. Interaction Between Age and Gravidity/Parity Most information about complication or mortality is couched in terms of either age or parity: women are at greatest risk at young and old ages and at low and high panties. Because age and parity are strongly associated, it is not clear if the age-specif~c and panty-specific patterns reflect the same basic age-driven risk, if they have independent effects, or if they act in combination. Contraception provides the means of affecting timing of fertility and thus increases the impor- tance of knowing whether there is an interaction between age and parity in their effects on morbidity and mortality associated with fertility. Four of the population-based studies provide information about maternal mor- tality by age and panty. The simple I- or U-shaped relationship between panty TABLE 3 Obstetric Interventions by Parity in Jerusalem Parity . Intervention Rate/1,000 - Rat~o 2 3 4 5 - 7-9 10+ AB 244 138 145 116 107 103 125 159 146 84 89 81 71 73 84 100 Note: Ratio is adjusted for age, ethnic group, and hospital Overall maternal mortality ratio in this population was 0.03 per 1,000 births. Source: Harlap et al. (1971).

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FERTILITY AND MATERNAL MORTALS 37 TABLE 19 Case-fatality Rates per 100 Hospitalized Patients With Hepatitis Female Place Year Male Nonpregnant Pregnant Reference India 1949 7.8 27.3 50.5 Wahi and Arora (1953) Saudi Arabia 53~3 4.5 11.9 46.3 Gelpi (1978) Libya 1975 .5 1.6 13.0 Christie et al. (1976) Bombay 65 66 - 25.6 53.8 D'Ctozand Balani (1968) South Iran 55-70 - 18.0 44.0 Borhanmesh et al. (1973) South Imn 67-70 - - 26.0 " Algiers 1956 - - 61.1 Haemmerli (1966) India 1956 - - 44.8 " Haifa 1959 - - 30.0 " Athens 1962 - - 25.9 " Jerusalem 1947 - - 18.5 " Cordoba 1957 - - 16.3 " Ghana 62~3 - - 13.3 Morrow et al. (1968) Haifa 5~57 _ _ 9.2 Peretzet al. (1959) (for males, 30.9 per 100,000; for females, 34.8), but pregnant women had higher case-fatality rates and a higher risk of serious disease. Haemmerli (1966) raised the question of genetic susceptibility, noting the predominance of high case-fatality rates in the circum-Mediterranean area; this seems unlikely given the additional case series reports from India, Ghana, and Ethiopia (Wahi and Arora, 1953; Morrow et al., 1968; Kwast and Stevens, 1987) as well as the high proportional mortality from hepatitis reported in some of the hospital maternal mortality series (D 'Cruz and Balani, 1968b; Shah et al., 1971; Konar et al., 1980; Barford and Parkes, 1977; Ojo and Savage, 1974~. The generally higher case-fatality rate for nonpregnant women than for men has been attributed to the lower nutritional status of women, but no evidence has been offered to support this. Tuberculosis Whether women with untreated tuberculosis are at higher risk of maternal mortality is unclear. Although this was the prevailing opinion in Europe and North America beginning in the late 19th century through the 1940s and currently prevails in many high-mortality countries today, it is possible that pregnant women with tuberculosis really die at no greater rate than nonpregnant women with tuberculosis. No study from a high-mortality country that addresses this question has been identified. However, a careful review by Hedvall (of European

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3 ~ SUSAN ZIMICK] studies) in 1953 showed about as many that demonstrate no adverse effect or even a favorable effect of pregnancy on tuberculosis as those that show a negative effect. In Hedvall's (1953) own prospective study of pregnant women with pulmonary tuberculosis, 9 percent improved during pregnancy and 7 percent worsened. Women who are adequately treated probably have no higher risk. In a com- panson of pregnant and nonpregnant tubercular women, with both groups having similar severity of disease and being treated similarly for active tuberculosis, Flanagan and Hensler (1959) showed no difference in disease progression. Malaru: During an epidemic of malaria in Ceylon the case fatality rate was twice as high among pregnant (13.1 percent) as among nonpregnant (6.5 percent) women (Wickramasuriya, cited in McGregor, 1986~. This pattern of enhanced risk of mortality from P. falciparllm during pregnancy is probably generalizable to areas of unstable (epidemic) transmission (Brabin, 19839. In hyperendemic areas where immunity to the parasite is high because of repeat exposure, pregnancy does not seem to have the same amplifying effect. However, a number of studies have shown that in these stable-transmission areas malaria parasitemia is more frequent and heavier during pregnancy, and particularly during the first and to a lesser extent during the second pregnancy (McGregor et al., 1983; McGregor, 19869. One direct consequence of this for maternal health is an increased probability of anemia (Gilles et al., 1969; McGregor, 1986; Brabin, 1983~. CONCLUSION The basic pattern observed for the relationship between fertility and maternal mortality is that risk of mortality is highest for first pregnancies and for fifth and subsequent ones. This pattern exists whatever the overall level of maternal mortality. Extremes of age, lack of medical care, poverty, and some infectious disease cofactors increase the risk. Thus, the lowest age-parity-specific risk in Jamaica is only half to a third as large as that in Bangladesh or Indonesia. These conditions also increase the relative risk of first and high-order pregnancies: the risk of first pregnancies relative to middle pregnancies is higher in Asia and Africa than in Jamaica. As conditions improve, the U-shaped curve of risk with parity is not only lower but also flatter. Given this pattern the potential for fertility reduction alone affecting maternal mortality is limited. The possible mechanisms through which fertility reduction can occur are contraception and provision of safe induced abortions. For first births use of contraception or safe abortion could reduce risk of mortality either through allowing postponement of the first birth until after age 20 or through averting unwanted birds. Even if contraception is available, use by teenagers

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FERTILITY AND MATE~~ MORTEM 39 may not be high, so provision of safe abortion is probably the most effective way to reduce mortality associated with unwanted first pregnancies. However, in many countries there are severe constraints to providing either contraceptives or abortions to young unmarried women, who are the most likely to have unwanted first pregnancies. The potential is greater for reducing mortality associated with unwanted higher- parity births. Family planning programs typically affect fertility mainly through reducing the number of high-parity births. Thus, except in sub-Saharan Africa, substitution of safe for unsafe abortions and contraception for abortion could substantially reduce maternal mortality 20 percent to 25 percent of all maternal deaths in some park of Asia are associated with abortion. However, this effect will be limited by the effectiveness of programs to convince women to use contraception. As for the middle parities, there is as yet insufficient evidence about whether the length of the interval between births has any effect on risk of maternal mortality. It is likely that maternal mortality ratios the risk of death per pregnancy- will increase, at least in the short term, in some areas as family size decreases. This paradoxical effect arises because of the way family planning programs typically affect fertility. First, as the number of high-parity births decreases, high- risk first births form a larger proportion of all births. Second, there is strong evidence for a population of at least two segments, one of which is in contact with the official health system, gets prenatal care, and has risks that are well below those of the other segment. It is likely that women who elect to contracept to postpone early childbearing, to end childbearing early, or to increase intervals between births will initially be those at lower risk of maternal mortality. Thus, reducing the high-parity fertility of these women may exclude those who have higher intrinsic risks. It is important to remember, however, that even when the risk per bird increases, the absolute number of deaths to women will probably decrease. Examination of the causal patterns of mortality suggests some alternative routes to reduce-maternal mortality. For all causes whatever is measured by "antenatal care" is important. The Zaria data show that it is not simply physical access to a hospital, though that is clearly important. It would be helpful to know for those living close to a hospital if having been to an antenatal clinic reduced the interval between development of a complication during home delivery and going to the hospital. It is unfortunate that the population-based studies have not paid more attention to antenatal care and hospital attendance for complications as factors in mortality. it.

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40 SUSAN ZIMICKI APPENDIX CONTENTS OF CAUSAL CATEGORIES The abortion category includes all abortion-associated deaths, whether in- duced or spontaneous, because' many studies either do not mention whether abortion was induced or indicate that it was determined indirectly. Hemorrhage includes all deaths attributed to hemorrhage, antepartum hemorrhage, placenta previa, placental abruption, postpartum hemorrhage, and retained placenta that were categorized by the author as hemorrhage rather than sepsis. A few deaths attributed to hemorrhage and ruptured uterus were classified under difficult labor, along with deaths attributed to ruptured uterus (whether or not there was a previous scar) and obstructed labor, including deaths due to disproportion and malpresentation. The sepsis category includes deaths attributed to puerperal tetanus and septicemia. If the author classified a death as due to cesarean section, anesthesia, sepsis, or hemorrhage connected with cesarean section or to anesthe- sia, the death was classified as operative, even if it was highly probable that the section was performed for obstruction or abruption. It is clear that the categories of hemorrhage, difficult labor, sepsis, and operative overlap, in that many deaths could almost as easily be put in one category as in another. Hypertensive disease includes deaths due to toxemia and eclampsia. Under romboembolism are grouped deaths ascribed to pulmonary, amniotic fluid, and air embolisms as well as those due to cerebrovascular hemorrhage. This last category probably includes a number of deaths with toxemia as an underlying cause. The cardiovascular category includes mainly deaths attributed to congenital heart disease (mitral stenosis) and rheumatic heart disease or simply to cardiovas- cular disease. It is not clear how frequently cardiac failure due to anemia is classified as cardiovascular. The gastrointestinal infectious category includes amebiasis, typhoid, and cholera deaths. All deaths attributed to hepatitis, infec- tious hepatitis, or hepatic coma when it is clear that there was an epidemic (either because the author says so or because the proportion of deaths so indicates) were attributed to hepatitis. Isolated hepatic or jaundice deaths that were not called infectious hepatitis are classified as "other indirect." The "other infectious" category includes mainly incidental deaths: anthrax (from Iran), smallpox, men- ingiiis, tuberculosis, malaria, and pneumonia. Suicide, murder, and one motor vehicle death make up the "violent death" category. The~"other" category includes deaths due to epilepsy and various cancers, most of which seem to be incidental. REFERENCES Adadevoh, K. B., and D. Akinla 1970 Postabortal and postpartum tetanus. Journal of Obstetrics and Gynecology of the British Commonwealth 70:1019-1023.

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FERTIJ~TY AND MATERNAL MORTALITY 41 Adetoro, O. O. 1987 Matemal mortality-a twelve-year study at the University of Ilonn teaching hospital (UTAH), Ilonn, Nigena. International Journal of Gynaecology and Obstetrics 25:93-98. 1989 A 15-year study of illegally induced abortion mortality at Ilonn, Nigena. Interna tional Journal of Gynaecology and Obstetrics 29:65-72. Aggarwal, V.P., and J.K.G. Mati 1980 Review of abortions at Kenyatta National Hospital, Nairobi. East African Medical Journal 57:13~143. Aitken, I. W., and B. Wells 1986 Maternal height and cephalopelvic disproportion in Sierra Leone. Tropical Doctor 16:132-134. Alauddin, M. 1987 Maternalmortalityinrural Bangladesh: The TangailDistnct. Studies in Family Planning 17(1):13-21. Al-Sayogh, K. N., and H. M. Hathout 1974 A mappraisal of grand multiparty. International Journal of Gynaecology and Obstetrics 12(5):159-165. Adcutu, A. A. 1978 A clinical study of maternal age and parturition In 2791 Tanzanian priTniparae. International Journal of Gynaecology and Obstetrics 16(1):20-23. Armon, P. J. 1977 Rupture of the uterus in Malawi and Tanzania. East African Medical Journal 54(9):462~71. 1979 Maternal deaths in the Kilimanjaro region of Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 73(3):284-288. Aziz, F. A. 1980 Pregnancy and labor of grand multiparous Sudanese women. International Journal of Gynaecology and Obstetrics 18(2):140146. Barford, D. A., and J. R. Parices 1977 Maternal mortality a survey of 1 18 maternal deaths and the avoidable factors involved. South African Medical Journal 51(4):101-105. Bhaia, J. C. 1985 Maternal Mortality in Anantapur District, India: Preliminary Findings of a Study. WHO FHE/PMM/85.9.16. WHO Intel~egional Meeting on Prevention of Maternal Mortality, Geneva, November 11-15. Billewicz, W. Z., and I. A. McGregor 1981 'Ihe demography of 2 West African (Gambian) villages 1951-1975. Journal of Biosocial Science 13:21~240. Blank, A., and W. Freedman 1969 Sickle cell trait and pregnancy. Clinical Obstetrics and Gynecology 12:123-133. Boenna, J. T. 1987 Maternal Mortality in Sub-Saharan Africa: Levels, Causes and Interventions. Presented at the IUSSP Seminar on Monality and Society in Sub-Saharan Africa, October 19-23, Yaounde, Cameroon. Borazjani, G., H. Javey, H. E. Sadgadi, and K. Daneshbod 1978 Maternal mortality in South Iran: A seven-year survey. International Journal of Gynaecology and Obstetrics 16:65~69. Borhanmanesh, F., P. Haghighi, K. Hekmat, K. Rezaizadeh, and A. G. Ghavami 1973 Viral hepatitis during pregnancy. Gastroenterology 64:30~312.

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42 SUSAN ZIMICK] Brabin, B. J. 1983 An analysis of malaria in pregnancy in Africa. Bulletin of the World Health Organization 61(6):1005-1016. Caffrey, K. T. 1979 Matemal mortalit~a continuing challenge in tropical practice a report Iran Nigena. East African Medical Journal 56:27~277. Chattopadhyay, S. K., B. S. Sengupta, C. Chattopadhyay, ~ Zaidi, and H. Showail 1986 Maternal mortality in Riyadh, Saudi Arabia. British Journal of Obstetrics and Gynecology 90:809-814. Chaturachinda, K., S. Tangtrakul, S. Pongthai, W. Phuapradit, A. Phanusopone, V. Benchakan, and J. J. Clinton Abortion: an epidemiologic study at Ramathibodi Hospital, Bangkok. Studies in Family Planning 12(6n) 2s7-262. Chen, L. C., M. C. Gesche, S. Ahmed, A. I. Chowdhury, and W. H. Mosley 1975 Matemal mortality in Bangladesh. Studies in Family Planning 5:33~341. Chi, I.-C., T. Agoestina, and J. Harbin 1981 Matemal mortality at twelve teaching hospitals in Indonesia An epidemiologic analysis. International Journal of Gynaecology and Obstetrics 19:259-266. Christie, A. B., A. A. Allam, M. K. Aref, I. H. E1 Muntasser, and M. El-Nageh 1976 Pregnancy hepatitis in Libya. The L;ancet (October 16):827-829. Committee on Matemal and Child Care of the Council of Medical Services 1964 A Guide for Maternal Death Studies. American Medical Association, Chicago. Daneshbod, K., G. R. Borasjani, H. Sagadi, and M. M. Hamidzadeh 1970 Survey of maternal deaths in South Iran: Analysis of 96 autopsies. Journal of Obstetrics and Gynecology of the British Commonwealth 77(12):1103-1108. Dawn, C. S., N. Gupta, and D. L. Poddar 1972 Avoidable factors in maternal deaths. Journal of the Indian Medical Association 59(3): 101-104. D'C~uz, I. A., and S. G. Balarn 1968 Infectious hepatitis and pregnancy. Obstetrics and Gynecology 31:449-455. D'Cruz, I. A., J. M. Fonseca, and V. T. Parmar 1968 Medical causes of maternal mortality. Journal of the Association of Physicians in India 16(7):417~24. Eastman, N. J. 1944 We effect of the interval between births on maternal and fetal outlook. American Journal of Obstetrics and Gynecology 47(4):445-466. Efiong, E. I., and M. O. Banjoko 1975 The obstetric performance of Nigerian pnmigravidae aged 16 and under. British Journal of Obstetrics and Gynecology 82(3):22~233. Egwuatu, V. E. 1986 Childbearing among the Igbos of Nigeria. International Journal of Gynaecology and Obstetrics 24: 103-109. Ekwompu, C. C. 1980 Infection as a possible trigger factor in the genesis of eclampsia. Tropical Doctor 10:17~178. 1981 E1 Dareer, A. 1983 Complications of female circumcision in the Sudan. Tropical Doctor 13:131-133. Elkins, T., E. Onwuka, T. Stowall, M. Hagood, and D. Osborn 1985 Utenne rupture in Nigeria. Journal of Reproductive Medicine 30(3):195-199.

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FERTILITY AND MATERNAL MORTALITY 43 Faundes, A., B. Fanjul, G. Henriquez, G. More, and C. Tognola 1974 ~luencia de la edad y de la pandad sobre algunos parametros de morbilidad mamma y sobre la morbimortalidad fetal. Revista Chilena de Obstetrica y Ginecologia 37(1):6-14. Faveau, V., M. A. Koenig, J. Chakraborty, and A. I. Chowdhury. 1988 Causes of maternal mortality in rural Bangladesh 1976-1985. Bulletin of the World Health Organization 66(5):643-652. Flanagan, P., and N. M. Hensler 1959 Ihe course of active tb complicated by pregnancy. Journal of the American Medical Association 170:783. Flavier, J. M., and C. H. C. Chen 1980 Induced abortion in rural villages of Cavite, the Philippines: knowledge, attitudes and practice. Studies in Family Planning 1 1(2):65-71. Fortney, J. A. 1987 File importance of family planning in reducing maternal mortality. Studies in Fanuly Planning 18(2):109 1 14. Fonney, J. A., I. Susanti, S. Gadalla, S. Saleh, P. J. Feldblum, and M. Potts 1985 MatemalMortalityinIndonesiasnd Egypt. WHO FHE/PMM/85.9.13. WHO temational Meeting on Prevention of Maternal Mortality, Geneva, November 1 1-15. Fo~tney, J. A., I. Susanti, S. Gadalla, S. Saleh, P. J. Feldblum, and M. Pous 1988 Maternal Mortality in Indonesia and Egypt. International Journal of Gynaecology and Obstetrics 26:21-32. Frost, O. 1980 Municipal community obstetricians in a developing country. Tropical Doctor 10:179-183. Fuchs, K., B.-A. Peretz, R. Marcovici, E. Paldi, and I. Timor-Tritish 1985 Ihe "grand multipara" Is it a problem? A review of 5785 cases. International Journal of Gynaecology and Obstetrics 23:321-325. Gelpi, A. P. 197 ~Viral hepatitis complicating pregnancy: mortality trends in 1979 Saudi Arabia. International Journal of Gynaecology and Obstetrics 17(1):73-77. Gilles, H. M., J. B. Lawson, M. Sibelas, A. Voller, and N. Allan 1969 Malaria, anaemia and pregnancy. Annals of Tropical Medicine and Parasitology 63:245-263. Golan, A., O. Sandbank, and O. Rubin 1980 Graham, W., and P. Airey. 1987 Measuring maternal mortality: sense and sensitivity. lIealth Policy and Planning 2(4):323-333. Greenwood, A. M., B. M. Greenwood, A. K. Bradley, K. Williams, P. C. Shenton, S. Tulloch, P. Byass, and F. S. J. Oldfield 1987 A prospective survey of the outcome of pregnancy in a rural area in the Gambia. Bulletin of the World Health Organization 65(5):635-643. Rupture of the pregnant uterus. Obstetrics and Gynecology 56(5):549-554. Groen, G. P. 1974 Utenne rupture in rural Nigena: review of 144 cases. Obstetrics and Gynecology 44:682~87. Haemmerli, U.P. 1966 Jaundice during pregnancy. ActaMedicaScandinavika 179(Suppl.444):1-111. Hadap, S., R. Kaufman, R. Rhymes, A. M. Davies, V. V. Sterk, and P. Weiskopf 1971 Pattems of obstetric intervention in a total population: a report from the Jerusalem perinatal study. Israel Journal of Medical Science 7(10):1115-1127.

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44 SUSAN ZIMICKI Harnson, K. A. 1976 Harrison, K. A., and L A. Rossiter 1985 Childbearing, health and social priorities: a survey of 22,774 consecutive hospital births in Zaria, Northern Nigeria. Chapter 5: Matemal modality. British Journal of Obstetrics and Gynecology 92(Suppl.5):3-13. Sickle cell disease in pregnancy. Tropical Doctor 6(4):74-80. Hayfield, V. J. 1980 Maternal mortality In Nigeria compared with earlier international expenence. International Journal of Gynaecology and Obstetrics 18:70-75. Hay, D. M., and J. J. Boyd 1973 A study of the obstetric performance of the adolescent Jamaican prunigravida. American Journal of Obstetrics and Gynecology 116(1):34-38. Hedvall, E. 1953 Pregnancy and tuberculosis. Accra Medica Scandinavika 286(Suppl. 147):1-101. Islam, S. 1982 Case studies of indigenous abortion practitioners in rural Bangladesh. Studies in Family Planning 13(3):86-93. Israel, S. L., and A. S. Blazar 1965 Obstetric behavior of the grand multipara. American Journal of Obstetrics and Gynecology 91(3):326-332. Janowitz, B., D. L. Covington, J. E. Higgins, L. F. Morena, M. S. Nakamura, J. A. Nunez, and M. M. Letelier 1982a Cesarean delivery in selected Latin American hospitals. Public Health 96:191-201. Janowitz, B., M. S. Nakamura, F. E. Lins, M. L. Brown, and D. Clopton 1982b Cesarean section in Brazil. Social Science and Medicine 16:19-25. Janowitz, B., J. Lewis, N. Burton, and P. Lamptey, eds. 1984 Reproductive Health in Africa: Issues and Options. Research Triangle Parl`, N.C.: Family Health Intemational. Khan, A.R., S.F. Begum, D. Covington, B. Janowitz, S. James, and M. Potts 1984 Risks and costs of illegally induced abortion in Bangladesh. Journal of Biosocial Science 16(1):89-98. Khan, A. R., F. A. Jahan, and S. F. Begum 1986a Matemal mortality in rural Bangladesh: the Jamalpur District. Studies in Family Planning 17(1):7-12. Khan, A. R., R. W. Rochat, F. A. Jahan, and S. F. Begwn 1986b Induced abortion in a rural area of Bangladesh. Studies in Family Planning 17(2):95-99. Koenig, M. A., V. Faveau, A. I. Chowdhury, J. Chakraborty, and M. A. Khan. 1988 Matemal mortality in Matlab, Bangladesh 197~85. Studies in Family Planning 19(2):69-80. Konar, M., K. Sikdar, S. Basak, and D. Lahim 1980 Matemal mortality (ten years' survey in Eden hospital). Journal of the Indian Medical Association 75(3):45-51. Kwast, B. E., and J. A. Stevens 1987 Viral hepatitis as a major cause of maternal mortality in Addis Ababa, Ethiopia. International Journal of Gynaecology and Obstetrics 25:99-106. Kwast, B. E., R. W. Rochat, and W. Kidane-Manam 1986 Maternal mortality in Addis Ababa, Ethiopia. Studies in Family Planning 17(6):288-301. Lamb,W.H.,C.Lamb,F.A.Foord,andR.G.Whitchead 1984 Changes in maternal and child mortality rates in three isolated Gambian villages over 10 years. The Lance' (October 20):912-914.

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FERTILITY AND MATERNAL MORTALITY 45 Lamptey, P. R., B. Janowitz, J. B. Smith, and C. Klufio 1985 Abortion experience among obstetrics patients at Korle-Bu hospital, Accra, Ghana. Journal of Biosocial Science 17(2)(Apol):195-203. Leedam, E. 1985 Traditional birth attendants. International Journal of Gynaecology and Obstetrics 23:249-274. Iindpaintner, L. S., N. Jahan, A. P. Satterthwaite, and S. Zimicki 1982 Maternity-related mortality in Matlab Dana, Bangladesh. Intemational Center for Dniarrhoeal Disease Research, Bangladesh. mimeo. Mahler, H. 1987 The safe motherhood initiative: a csi!~1 to action. The L~zneet (March 21):668-670. Malone, M. I. 1980 The quality of care in an ante-natal clinic in Kenya. East African Medical Journal 57:86-96. Mashini, I., A. Mmueh, and H. Hadi 1984 Maternal mortality in the American University of Beirut Medical Center (AUBMC) 1971-1982. International Journal of Gynaecology and Obstetrics 22:275-279. McFee, J. 1973 Anenua: a high-risk complication of pregnancy. Clinical Obstetrics and Gynecol ogy 16:153-171. McGregor, I. A. 1986 Malaria in Pregnancy; With Consideration of Some Factors Which Influence Remedial Strategies. Presented at Annual Consultative Meeting of Combatting Childhood Communicable Disease Project, Brazzaville, Congo, March. McGregor, I. A., M. E. Wilson, and W. Z. Billewicz 1983 Malaria infection of the placenta in the Gambia, West Africa; its incidence and relationship to stillbirth, birthweight and placental weight. Transactions of the Royal Society of Tropical Medicine and Hygiene 77(2):232-244. Megafu, U. 1985 Factors influencing maternal survival in ruptured uterus. International Journal of Gynaecology and Obstetrics 23:475~80. Melrose, E. B. 1984 Matemal deaths at King Edward vm Hospital Durban: a review of 258 consecutive cases. South African Medical Journal 65:161-165. Mhango, C., R. Roc hat, and A. Arkutu 1986 ReproduetiLve mortality In Lusaka Zambia 1982-1983. Studies in Family Planning 1~7(5):243-257. Mokgdcong, E. T., and M. Marivate 1976 Treatment of the ruptured uterus. South African Medical Journal 50:1621-1624. Morrow, R. H., Jr., H. F. Smetana, F. T. Sai, and J. H. Edgeomb 1968 Unusual features of viral hepatitis in Accra, Ghana. Annals of Internal Medicine 68:125~1264. Mtimavalye, L. A. R., D. Lisasi, and W. K. Ntuyabaliwe 1980 Matemal mortality in Dar es Salaam Tanzania 197~1977. East African Medical Journal 57:1 1 1-1 18. Mutambirwa, J. 1985 Pregnancy, childbirth, mother and child care among the indigenous people of Zimbabwe. International Journal of Gynaecology and Obstetrics 2;3:27~285. Nasah, B. T., and P. Drouin 1978 Review of 70 cases of ruptured uterus in Cameroon. Tropical Doctor 8(3):127-131. Ngoica, W. M., and J. K. G. Mati 1980 Obstetric aspects of adolescent pregnancy. East African Medical Journal 57:12~130.

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46 SUSAN ZIMICKI Odur~tan, S. O., and V. B. Odulami 1975 Maternal mortality in western Nigeria. Tropical and Geographic Medicine 27:313-316. Ojo, O. A., and V. Y. Savage 1974 A ten-year review of maternal mortality rates in the University College Hospital, Ibadan, Nigeria. American Journal of Obstetrics and Gynecology 118:517-522. Okojie, S. E. 1976 Induced illegal abortions in Benin City, Nigena. International Journal of Gynaecol ogy and Obstetrics 14(6):517-521. Olukoya, A. A. 1987 Pregnancy termination: results of a community-based study in Lagos, Nigeria. International Journal of Gynaecology and Obstetrics 25:41~6. Omran, A. R., C. C. Standley, J. E. Asar, M. Began, V. Guzman, V. Nahapetian, and K. A. Pisharoti, eds. 1981a Family Formation Patterns and Health. Geneva, Switzerland: World Health Organization. Omran, A. R., C. C. Standley, G. Ochoa, A. Gil, H. Hamman, F. El-Sherbini, B. Raza, and F. El- Bhoustani, eds. 1981b Further Studies on Family Formation and llealth. Geneva, Switzerland: World Health Organization. Peretz, A., E. Paldi, S. Brandstacdter, and D. Barzilai 1959 Infectious hepatitis in pregnancy. Obstetrics and Gynecology 14:435041. Pison, Gilles 1989 Institut National d'Etudes Demographiques, Pans, France. Personal communication. Puffer, R. P., and G. W. Griffith 1967 Patterns of Urban Mortality. Washington, D.C.: Pan-American Health Organiza tion. Rao,K. B. 1975 Matemal mortality in a teaching hospital in southern India. Obstetrics and Gynecology 46:397~00. Raymundo, C. 1987 Risks of Motherhood Among Urban Poor. University of the Philippines, Manila. October. Mimeo. Rendle-Short, C. W. 1960 Rupture of the gravid uterus in Uganda. American Journal of Obstetrics and Gynecology 79(6):111~1120. Rochat, R. W., S. Jabeen, M. Rosenberg, A. R. Mcasham, A. R. Khan, M. Obaidullah, and P. Gould 1981 Maternal and abortion-related deaths in Bangladesh 1978-1979. International Journal of Gynaecology and Obstetrics 19(2):155-164. Rosenfield, A., and D. Maine 1985 Maternalmortality a neglected tragedy: Whereis them in mch? The Lancet (July 13):83-85. Royston, E. 1982 The prevalence of nutritional anemia in women in developing countries a critical review of available information. World }lealth Statistics Quarterly 35(2):52-91. Royston, E., and J. Ferguson 1985 lbe coverage of maternity care: a critical review of available information. World Health Statistics Quarterly 38:267-288. Royston, E., and A. D. Lopez On the assessment of maternal mortality. World lieallh Statistics Quarterly 40:214-224.

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FERTILITY AND MATERNAL MORTALITY 47 Shah, K. P., J. M. D. E. Souza, D. Sawardeker, and R. V. Aphale 1971 Comparative study of maternal mortality in rural community and city teaching institution. Indian Journal of Public Health 15(3):83-91. Tezcan, S., and A. R. Omran 1981 Prevalence and reporting of induced abomc~n in Turkey: two survey techniques. Studies in Family Planning 12(6n) 262-271. Russell, J., and A. Pebley 1984 Me potential impact of changes in fertility on infant, child and maternal mortality. Studies in Family Planning 15(6):256-266. Unuigbe, J. A., A. U. Oronsaye, A. A. E. Orhue. 1988 Abortion-reJated morbidity and mortality in Benin City, Nigeria: 1973-1985. International Journal of Gynaecology and Obstetrics 26:435~39. Vennema, A. 1975 Pennatal mortality and maternal modality at the provincial hospital, Quang Ngai, South Vietnam 1967-1970. Tropical and Geographic Medicine 27:3038. Verzin, J. 1975 Sequelae of female circumcision. Tropical Doctor 5:163-169. Voorhoeve, A. M., A. S. Muller, and H. W'Oigo 1979 Agents affecting health of mother and child in a rural area of Kenya: XVI. The outcome of pregnancy. Tropical and Geographic Medicine 31:607~27. Wahi, P. N., and M. M. Arora 1953 Epidemic hepatitis. New England Journal of Medicine 248:451~54. Walker, G. J., D. E. C. Ashley, A. McCaw, and G. W. Bernard 1985 Matemal Monality in Jamaica: A Confidential Inquiry Into All Maternal Deaths in Jamaica 1981-1983. WHO PHE/PMM/85.9.10. WHO Interregional Meeting on Prevention of Matemal Mortality, Geneva November 11-15. WHO 1987 Hypertensive Disorders of Pregnancy. Technical Repon 758. Geneva, Switzerland: World Health Organization. WHO Intemational Collaborative Study of Hypertensive Disorders of Pregnancy 1988 Geographic variation in the incidence of hypertension in pregnancy. American Journal of Obstetrics and Gynecology 158(1):8~83. WHO Secretariat 1985 Measunng Maternal Monality. WHO FHE/PMM/85.6.2. Interregic~nal Meeting on Prevention of Matemal Mortality, Geneva, November 1 1-15. Winikoff, B., and M. Sullivan 1987 Assessing the role of family planning in reducing maternal mortality. Studies in Family Planning 18(3):128-143.