Summary of Findings: Reducing Fetal Deaths in Developing Countries

  • Approximately 4 million fetal deaths occur each year, 98 percent of them in developing countries. These are rough estimates, as fetal deaths are infrequently acknowledged or recorded in developing countries.

  • Because intrapartum fetal deaths are more easily prevented, as fetal mortality rates decline, an increasingly higher proportion of fetal mortality occurs in the antepartum period.

  • Known risk factors for fetal deaths include demographic and social correlates such as advanced maternal age; chronic maternal conditions such as anemia and sickle cell disease; maternal infections such as syphilis, HIV, and malaria; inadequate maternal nutrition; and maternal complications (both antepartum and intrapartum). Many of these factors could be addressed in antenatal care, as well as through comprehensive family planning and health education measures described in previous chapters.

  • Surveillance and analysis of fetal mortality will enable developing countries to adapt and implement interventions to reduce fetal deaths as part of an overall effort to improve birth outcomes.



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Improving Birth Outcomes: Meeting the Challenge in the Developing World Summary of Findings: Reducing Fetal Deaths in Developing Countries Approximately 4 million fetal deaths occur each year, 98 percent of them in developing countries. These are rough estimates, as fetal deaths are infrequently acknowledged or recorded in developing countries. Because intrapartum fetal deaths are more easily prevented, as fetal mortality rates decline, an increasingly higher proportion of fetal mortality occurs in the antepartum period. Known risk factors for fetal deaths include demographic and social correlates such as advanced maternal age; chronic maternal conditions such as anemia and sickle cell disease; maternal infections such as syphilis, HIV, and malaria; inadequate maternal nutrition; and maternal complications (both antepartum and intrapartum). Many of these factors could be addressed in antenatal care, as well as through comprehensive family planning and health education measures described in previous chapters. Surveillance and analysis of fetal mortality will enable developing countries to adapt and implement interventions to reduce fetal deaths as part of an overall effort to improve birth outcomes.

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Improving Birth Outcomes: Meeting the Challenge in the Developing World 4 Reducing Fetal Mortality The major causes of embryonic and fetal death vary over the course of gestation. Fetal deaths that occur late in gestation (after 28 weeks) and involve a potentially viable fetus are amenable to prevention. This chapter therefore focuses on factors that strongly influence late fetal survival, such as maternal health and the management of labor and delivery, and reviews promising interventions to reduce late fetal deaths in developing countries. Many of the interventions described in the previous chapter are also effective in reducing fetal mortality. An estimated 4 million late fetal deaths1 occur each year, 98 percent of them in developing countries (Save the Children, 2001; World Health Organization, 1996). Despite the magnitude of this public health problem, it has attracted little attention, and information on these deaths is limited. Late fetal deaths are not included in estimations of the global burden of disease, and are not therefore recognized by decisionmakers for their important role in that burden. A substantial proportion of fetal deaths do not have an identified cause. Fetal autopsy, discussed at the end of this chapter, is sometimes useful for this purpose, but is not available in most developing country settings. Reported fetal mortality rates vary widely, but generally parallel neonatal and maternal mortality. Table 4-1 summarizes fetal death rates reported from several studies in developing countries. Data on fetal death in 1   For this statistic, late fetal deaths are those that occur after 22 (not 28) weeks of gestation.

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Improving Birth Outcomes: Meeting the Challenge in the Developing World TABLE 4-1 Fetal Deaths from Developing Country Studies Study Population Fetal Death Rate % Antepartum Deaths % Perinatal Deaths % Births in Hospitals Number of Fetal Deaths in Study (H or P) Reference Latin America/Caribbean   Pelotas, Brazil (1982) 16.5   49.0 99 122 (P) Barros et al., 1987 Curaçao (1984–1985) 17.8 58.6 52.0 99 116 (P) Wildschut et al., 1989 Jamaica (1986) 24.3 77.8 57.6 84 255 (P) Ashley et al., 1994a Asia   Quezon City, Philippines (1980–1982) (<1000g) 10.3   51.9 24 42 (Ref H) Baja-Panlilio et al., 1986 Jiangsu, China (1980–1981) 13.1 58.0 53.5   1140 (H) Li et al., 1982 Vila, Fiji (1992) (≥500g) 15.9 43.0 46.0 80 23 (Ref H) Maouris, 1997 Colombo, Sri Lanka (1993) 17.7 86.1 65.0   223 (H) Lucas and Ediriweera, 1996 Nepal (1989–1990) 26.4 31.2 55.2   395 (H+C) Geetha et al., 1995 Matlab, Bangladesh (1986) 38.3   49.3 5 2,213 (P) Fauveau et al., 1990

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Improving Birth Outcomes: Meeting the Challenge in the Developing World Africa   Libya (1984) 11.5 62.5 43.5   189 (H) Kishan et al., 1988 Gweru, Zimbabwe (1984–1986) 14.9 53.9 48.5   340 (H/MC) De Muylder, 1989 Dar es Salaam, Tanzania (1981) 25.2 59.6 65.5   171 (H) Kazimoto, 1982 Farafenni Area, Gambia (1982–1983) 34.9   46.9 4 23 (P) Greenwood, et al., 1987 Kaduna, Nigeria (1990) 42.8 76.2 63.9   48 (H)* Künzel et al., 1996 Bulowayo, Zimbabwe (1990) 42.9 44.8 55.1   466 (H) Aiken, 1992 Maputo, Mozambique (1982–1991) 44.3 83.0 57.3 15 5,958 (H) Bugalho et al., 1989 Lomé, Togo (1990) 67.0 43.4 86.2   73 (H)* Künzel et al., 1996 Bamako, Mali (1990) 97.7 30.8 84.9   146 (H)* Künzel et al., 1996 P refers to population data, H to hospital data, Ref H to referral hospital data, C to community data, and MC to maternity center data. * Estimated from data in the table. SOURCE: Dr. Affette McCaw-Binns, UWI (Mona).

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Improving Birth Outcomes: Meeting the Challenge in the Developing World developing countries may overestimate fetal mortality in hospitals with many referrals or underestimate it if they serve a higher income segment of the population, because such studies are usually based on hospital data only (Saksena and Srivastava, 1980; Gadow et al., 1991; Conde-Agudelo et al., 2000). Many of the studies in Table 4-1 include estimates of fetal death as a component of perinatal mortality, which includes fetal deaths occurring between 22 or 28 weeks’ gestation (depending on the source) and birth, as well as neonatal deaths that occur during the first week of life. For infants who die shortly after birth, distinguishing between late fetal and early neonatal deaths can be difficult. These diagnoses depend on the skill and experience of clinical staff, who may differ in their application of the broad definitions of fetal and neonatal death (Golding, 1991). In order to recognize the true magnitude of both neonatal and fetal mortality, each outcome and its attendant risk factors need to be measured as accurately as possible. This report addresses fetal mortality separately from neonatal mortality so that the distinctions between them can be clarified and causes of mortality addressed according to their priority. Surveillance of fetal mortality, along with other pregnancy and birth outcomes, is discussed in Chapter 5. FACTORS CONTRIBUTING TO LATE FETAL DEATHS In settings where most women give birth without skilled assistance, fetal mortality is high, and the proportion of fetal deaths that occur during labor and delivery is high (Conde-Agudelo et al., 2000). These are intrapartum fetal deaths (IPFDs) or so-called fresh stillbirths. Such deaths can often be prevented by skilled management of labor and delivery as described in Chapters 2 and 3. However, skilled care is generally not available for home deliveries. As health care services are improved and fetal deaths during labor and delivery are reduced, antepartum fetal deaths (APFDs), which occur before the onset of labor, account for an increasing proportion of late fetal deaths (Kiely et al., 1985); thus in developed countries, only about 10 to 15 percent of late fetal deaths occur in the intrapartum period (Ogunyemi et al., 1998, Kiely et al., 1985). Since intrapartum fetal deaths predominate in most developing countries, their causes and prevention receive particular emphasis in this chapter. Low-cost measures to significantly reduce risk factors for APFDs are also discussed. Intrapartum Fetal Deaths Intrapartum fetal deaths (IPFDs) generally result from maternal conditions or obstetric complications, and frequently involve suboptimal management of labor and delivery (Sheiner et al., 2000; Kiely et al., 1985;

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Improving Birth Outcomes: Meeting the Challenge in the Developing World Stewart et al., 1998; Escoffery et al., 1994). Early recognition and treatment of risk factors can prevent certain fetal deaths. However, the majority of fetal deaths occur in pregnancies considered to be low risk. Diabetes mellitus The offspring of women with diabetes tend to be large for gestational age, and therefore at increased risk for intrapartum injury and asphyxia (Gunton et al., 2000; Garner, 1995). Even with improved glycemic control, the fetus is large in 8 to 43 percent of such pregnancies. Smoking among mothers with diabetes increases the risk for fetal mortality (Gunton et al., 2000). Complications for women with diabetes include maternal infections (more common than among healthy women), pre-eclampsia, and diabetic nephropathy (which carries a high risk of hypertension as well), all of which increase the risk of adverse outcomes. Avoiding adverse fetal outcomes requires early dietary advice, an insulin regimen, and consistent monitoring of glucose and maintenance of an optimal level (Garner 1995). Infections The risk for IPFD is much higher for pregnancies among women infected with syphilis than in uninfected women (Schulz et al., 1987). Obstetric complications Intrapartum hemorrhage. Premature separation of the placenta (abruptio placentae) causes hemorrhage. The separation varies in size from small to complete and the risk of fetal death increases with the degree of placental separation (Ananth et al., 1999). Hypertensive disease (which includes chronic hypertension, pre-eclampsia, and eclampsia) may be exacerbated by pregnancy or arise for the first time during pregnancy. Hypertensive disease was found to be a major risk factor in analyses of about 15,000 late fetal deaths in Latin America (Conde-Agudelo et al., 2000), almost 600 late fetal deaths in Jamaica (Greenwood et al., 1994), and 93 late fetal deaths in Ghana (Wiredu and Tettey, 1998). In a study in Mozambique, the fetal death rate for 1,275 women with hypertensive disease of pregnancy was 5.7 percent compared with 2.3 percent for the more than 43,000 women without hypertensive disease (Merz et al., 1992). In a study in Shanghai, China, 8,852 of 158,790 pregnancies involved hypertensive disease; 44 percent were classified as moderate or severe, and the adverse outcomes included 48 antepartum fetal deaths and 12 late fetal deaths (Huang, 2001). Prolonged or obstructed labor. This is one of the most common pre-

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Improving Birth Outcomes: Meeting the Challenge in the Developing World ventable causes of fetal mortality. It may involve prolonged first or second stage of labor, cephalopelvic disproportion, uterine rupture, or malpresentation. In Zimbabwe, major causes of perinatal mortality were found to include prolonged first- and/or second-stage labor, uterine rupture, and a retained second twin (Aiken, 1992). Although improvements in antenatal, intrapartum, and neonatal care have the potential to reduce perinatal mortality, further study into specific preventive measures is necessary. Fetal malpresentation, such as breech or transverse lie, has also been associated with increased risk for fetal death in studies in both developing (Conde-Agudelo et al., 2000; Kapoor et al., 1994; Aiken, 1992; Kusiako et al., 2000) and developed (Sheiner et al., 2000) countries. Multiple pregnancy. Studies of more than 7,000 births in southern Brazil and more than 9,500 births in Jamaica have reported a two- to fourfold higher risk of fetal mortality in multiple pregnancies compared with singleton pregnancies (Barros et al., 1987; McCaw-Binns, 2000). Cord complications including prolapse, cord around the neck, knots, or other entanglement also contribute to intrapartum fetal death (Sheiner et al., 2000). Asphyxia Asphyxia is an important cause of fetal death. Asphyxia can be broadly defined as progressive hypoxaemia and hypercapnia with a significant metabolic acidaemia (Low, 1997; Bax and Nelson, 1993). In the early 1990s, the Jamaican Perinatal Mortality Survey found intrapartum asphyxia to be the cause of 23 percent of fetal deaths in which the fetus weighed at least 2,500 g (Escoffery et al., 1994). The rate of asphyxia is higher in Ghana (56 percent) (Wiredu and Tettey, 1998). Growth-restricted fetuses appear to have a lower tolerance for intrapartum asphyxia (Tuthill et al., 1999). Birth injury Birth injury includes preventable and unavoidable mechanical or hypoxic-ischemic injuries suffered by the neonate during labor and delivery. These may include trauma to the head (most significant is intracranial hemorrhage); trauma to internal organs (such as the liver or spleen); injury to the spinal cord or peripheral nerves (most common is brachial plexus injury and most devastating is cord transection); and fractures (to the clavicles and extremities). The predisposing factors include macrosomia (particulaly for diabetic mothers), cephalopelvic disproportion, dystocia, prolonged or obstructed labor, breech presentation, and prematurity. Although injury may occur despite skilled care at delivery, some injuries are

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Improving Birth Outcomes: Meeting the Challenge in the Developing World the result of inadequate medical knowledge or suboptimal care during labor and delivery. More specific diagnoses can assist efforts to prevent avoidable birth injuries. Escoffery and coworkers (1994) found evidence of birth trauma in 22 percent of the IPFDs they examined in Jamaica. In a study in Ghana, birth trauma was found to be responsible for a little more than 5 percent of fetal deaths (Wiredu and Tettey, 1998). Economic factors To the extent that low family income limits access to quality health care services, it is a risk factor for IPFD. Family income has been negatively correlated with fetal mortality in India (Saksena and Srivastava, 1980) and Brazil (Barros et al., 1987), with women from the poorest families having a fetal death rate two to four times higher than women from the wealthiest families. A similar relative risk of late fetal death was determined for rural women (who tend to have lower socioeconomic status) compared with urban women in Nepal (Jahn et al., 2000). The risk for late fetal death was significantly higher among wives of unskilled laborers (such as subsistence farmers) in Papua New Guinea (Amoa et al., 1998). In a large study of over 850,000 hospital births in 11 Latin American countries, the late fetal death rate was almost twice as high in free hospitals that serve mainly low-income women as in hospitals requiring payment for services (Gadow et al., 1991). This difference may in part reflect a lower quality of care provided to patients who do not pay for services. Antepartum Fetal Deaths The risk factors reported for APFDs include maternal conditions, obstetric complications, and advanced maternal age. Some studies, described below, also indicate that inadequate antenatal care, smoking, high parity, and low socioeconomic status increase the risk for APFD. Hypertensive disease of pregnancy Hypertensive disease was found to be a major risk factor for APFD. In Sri Lanka, hypertensive disease was associated with 32 percent of antepartum deaths, the majority of which occurred after 31 weeks of gestation (Lucas and Ediriweera, 1996). Hypertension may result in uteroplacental insufficiency, abruptio placentae, or placental infarction—all risk factors for late fetal death.

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Improving Birth Outcomes: Meeting the Challenge in the Developing World Antepartum hemorrhage This was shown to be one of the most important risk factors for fetal death in studies in Latin America (Conde-Agudelo et al., 2000), Jamaica (Greenwood et al., 1994), and Ghana (Wiredu and Tettey, 1998). Diabetes mellitus It is well known that maternal diabetes mellitus increases the risk of intrauterine fetal death (Garner, 1995; Casson, 1997; Hawthorne et al., 1994; Mondestin, 2002; Platt et al., 2002). Although the exact cause of fetal death is unknown, uteroplacental insufficiency, vascular disease, and hypertension associated with diabetes increase risk of death. In addition, congenital malformations in diabetic pregnancies also contribute to increased risk of late fetal death. Several studies have shown that diabetes in pregnancy is associated with hyptertension (Cundy et al., 2002) or with hypertensive disorder of pregnancy (Sibai et al., 2000). Maternal hypertension associated with diabetes may result in fetal compromise earlier in gestation and is particularly worrisome (Lagrew et al., 1993). Early recognition of diabetes mellitus in pregnancy and control of maternal glucose levels can reduce fetal mortality and other complications in affected pregnancies (Langer and Conway, 2000). Sickle cell disease This inherited disorder occurs worldwide with the highest incidence in malaria-endemic areas of Africa. Sickle cell disease is associated with an increased risk of fetal mortality, presumably due to placental infarcts (Mahomed, 2003). This risk can be substantially reduced with appropriate antenatal care and management of labor and delivery (Sun et al., 2001; Smith et al., 1996); however, this level of care is not generally available in the countries where sickle cell disease is most prevalent. Infections Fetal mortality is associated with a variety of maternal infections including sexually transmitted diseases, bacterial infections of the genitourinary tract, and rubella2 (Goldenberg et al., 1997; Gibbs, 2002). Syphilis, like rubella, Toxoplasma, and cytomegalovirus, can cause 2   Rubella is discussed in the companion report, Reducing the Impact of Birth Defects: Meeting the Challenge in the Developing World (Institute of Medicine, 2003).

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Improving Birth Outcomes: Meeting the Challenge in the Developing World transplacental infection of the fetus. Although a rapid serological test allows on-site diagnosis so that a highly effective treatment of penicillin can be initiated immediately, there continues to be a high level of infectious maternal syphilis in several countries (Hira et al., 1990). The prevalence of syphilis among women attending antenatal clinics is 4 to 16 percent in several countries of Africa and the Caribbean (Hira et al., 1990; Schulz et al., 1987; Prabhakar et al., 1991; McDermott et al., 1993). Untreated syphilis has been shown in several studies to increase the risk of fetal death (de Aquino, 1998; Osman et al., 2001; Schulz et al., 1987; McDermott et al., 1993). In Malawi, a longitudinal population-based study found a population-attributable risk (PAR) for syphilis of 26 percent among mothers who had experienced a fetal death. For antepartum fetal deaths, the PAR was 38 percent for syphilis (McDermott et al., 1993). Syphilis was the attributed cause of 10 percent of late fetal deaths in a case-control study of 315 consecutive late fetal deaths in Papua New Guinea (Amoa et al., 1998). Other bacterial infections—symptomatic or asymptomatic—are an important risk for late fetal death (Maleckiene et al., 2000). Various reproductive tract infections have been associated with preterm spontaneous labor (Brocklehurst et al., 2002) and rupture of membranes, which can result in fetal death. Infection of normally sterile sites like amniotic fluid, interior of the placenta, and fetal blood can be life threatening (Maleckiene et al., 2000). Chorioamnionitis or amniotic fluid infection has been identified as an important cause of fetal death in several studies in developing (Naeye et al., 1977; Ross et al., 1982, Moyo et al., 1996; Folgosa et al., 1997; Matthews et al., 2001) and industrialized (Tolockiene et al., 2001) countries. HIV. A systematic review of maternal HIV infection and perinatal outcomes (Brocklehurst and French, 1998) suggests a weak association in developing country studies when there is an attempt to control for confounding. Studies to date have not provided good data on the disease stage of women or their immune function. Viral hepatitis. Viral hepatitis is a common cause of liver disease during pregnancy and is a cause of fetal death (Michielsen and Van Damme, 1999). Obstetric complications Placental abruption, oligohydramnios, and umbilical cord complications have been identified as important risks for APFD in hospital-based, retrospective studies in developed countries (Sheiner et al., 2000; Oron et al., 2001; de Aquino et al., 1998; Ananth et al., 1999). The risk of late fetal death rises steeply when more than half the placenta becomes separated. Hypertensive disease of pregnancy, tobacco use, and drug use are all risk factors for placental abruption (Ananth et al., 1999).

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Improving Birth Outcomes: Meeting the Challenge in the Developing World Multiple pregnancy. In Jamaica, antepartum fetal deaths were found to occur about twice as frequently among twins as among singletons (Ashley et al., 1994b). Prolonged pregnancy is defined as a pregnancy that lasts 42 weeks or more. Developed country studies have shown that prolonged pregnancy increases the risk of fetal death (Hollis, 2002). This risk is increased for growth restricted fetuses; growth restriction itself is an independent risk factor (Divon et al., 1998). In terms of numbers of fetal deaths, however, many more fetuses die between 37 and 42 weeks than after 42 weeks. In low-resource settings, the date of conception is frequently not known, which limits the ability to understand the role of prolonged pregnancy in these populations. Congenital malformations3 These have been found to account for 6 percent of fetal deaths in Jamaica (Ashley et al., 1994a) and almost 8 percent in Zimbabwe (Aiken, 1992). As fetal mortality due to more preventable causes decreases, the proportion of fetal deaths associated with malformations increases (De Galan-Roosen et al., 1998). Maternal age and parity Several studies show an increase in fetal deaths with advanced maternal age (Fretts et al., 1995; Huang, 2000; Andersen et al., 2000; Seoud et al., 2002; Sheiner et al., 2000; Amoa et al., 1998; Khandait et al., 2000). Data from India (Saksena and Srivastava, 1980), Brazil (Barros et al., 1987), and Mexico (Bobadilla-Fernandez, 1986) indicate that fetal death rates are lowest among teen mothers and rise with maternal age. Risk ratios vary from 2 to 4 in the oldest versus the youngest age groups. Other studies have found a U-shaped relationship between maternal age and fetal mortality, with the youngest and oldest mothers faring worst (de Aquino et al., 1998; Andersen et al., 2000; Onadeko et al., 1996; Stanley and Straton, 1981; Murphy et al., 1987; Ahlenius and Thomassen, 1999). Multivariate analyses indicate that the high fetal death rates sometimes observed among teenage mothers may result from social and behavioral influences, rather than a specific biological effect of young maternal age although biological factors can have an influence in very young mothers (Bacci et al., 1993; Hardy et al., 1987; La Guardia et al., 1989). The relationship between maternal parity and fetal mortality is unclear. It is often difficult to separate the effects of 3   Discussed in the companion report, Reducing the Impact of Birth Defects: Meeting the Challenge in the Developing World (Institute of Medicine, 2003).

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Improving Birth Outcomes: Meeting the Challenge in the Developing World event: ways to improve nutritional status with local foods; supplementation with iron, folate, and vitamins; maintaining hydration through high fluid intake; prophylaxis against Plasmodium falciparum malaria; and early detection of bacterial infection (Rahimy et al., 2000). Detection and Management of Diabetes. Identification and management of women with pre-gestational diabetes improves pregnancy outcome. Screening for gestational diabetes is appropriate for women at high risk due to a previous large for gestational age infant, previous unexplained fetal death, previous congenital malformation, or obesity. Cesarean section, where safely available, may be needed for large for gestational age infants if there is failure of the normal progression of labor. Recognition of Fetal Deaths Fetal deaths often go unacknowledged or unrecorded in developing countries, which hinders attempts to adapt interventions and set health care priorities to meet local needs. In Jamaica, for example, researchers found that only 13 percent of late fetal deaths and 25 percent of infant deaths had been registered, compared with 94 percent of live births (McCaw-Binns et al., 1996). In Thailand, a comparison of official records with a community-based survey showed that only 55 percent of infant deaths and none of the late fetal deaths recorded in the survey had been officially registered (Lumbiganon et al., 1990). Obtaining accurate measures of both fetal and neonatal mortality will require renewed efforts to record all births and accurately assign deaths as fetal or neonatal. Only when the full magnitude and causes of fetal and neonatal mortality are established can policy makers and health professionals identify and implement appropriate health services. Chapter 5 describes strategies for the surveillance of all pregnancy outcomes; the measures described here represent key steps toward establishing surveillance of fetal death. Autopsy and fetal death audit A well-performed autopsy may be the sole means of establishing diagnoses in fetal deaths, and is likely to contribute information that differs from clinical findings (Bendon, 2001; Magee, 2001; Tennstedt et al., 2001; Meier et al., 1986; Porter and Keeling, 1987). Congenital anomalies may not be grossly apparent and postmortem findings can contribute to genetic counseling of parents on their fetal loss and future pregnancies (Doyle, 2000; Berger, 1978), and to subsequent monitoring of patient care. In addition, examination of the placenta may help elucidate the cause of death (Naeye, 1992). Autopsies are not widely available in developing country settings.

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Improving Birth Outcomes: Meeting the Challenge in the Developing World Classification systems Unlike most systems for classifying perinatal deaths, the Wigglesworth (1980) system does not rely on autopsy data (Hey et al., 1986). This overcomes a difficult challenge for many developing country settings. A modified form of this method, which permits the classification of fetal deaths, can be used to analyze trends in fetal death and identify critical needs (Keeling et al., 1989). For example, studies using this system in Zimbabwe (De Muylder, 1989) and Jamaica (Ashley et al., 1994a) found asphyxia to be a major cause of fetal death, suggesting the need to improve obstetric monitoring and resuscitative procedures (Golding, 1991). RECOMMENDATIONS Recommendations 1, 2, and 4, in the executive summary and chapter 9 have been developed in other chapters. They also address priority interventions for reducing fetal mortality. Surveillance of fetal deaths is even more limited than for neonatal deaths. Until the magnitude of fetal mortality is established, it is likely to remain high. RESEARCH NEEDS As a result of the substantial overlap in the causes of fetal and neonatal mortality, several of the research topics in the previous chapter apply here as well. There are two additional priorities for research: Strategies are needed to determine how to monitor labor and delivery more effectively so as to ensure early recognition of complications in low resource settings. Given the high prevalence of unexplained fetal death in developing countries, autopsy studies in diverse settings could help identify potentially preventable deaths, especially those related to infection. CONCLUSION The most significant risk factors for fetal death also profoundly affect maternal and neonatal health. In most developing countries, IPFD accounts for a high proportion of fetal mortality. Skilled management of labor and delivery, including access to emergency obstetric care (see Chapters 2, 3, and 5), could prevent many of these deaths, in addition to those of mothers and neonates. The decrease in intrapartum fetal mortality in developed countries can be attributed to improved obstetric monitoring and management of labor and delivery (Goldenberg et al., 1987). Reducing APFD

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Improving Birth Outcomes: Meeting the Challenge in the Developing World involves addressing maternal factors such as advanced age, prior fetal loss, infectious disease, hypertension, obesity, and other health problems through focused antenatal programs, comprehensive family planning, and health education, as described in previous chapters. Continued surveillance and analysis of fetal death, as well as maternal and neonatal mortality and morbidity, will allow communities and countries to adapt interventions to local conditions and set health care priorities. The recommendations and research priorities presented in the next chapter emphasize the need to recognize fetal deaths as part of an overall effort to improve birth outcomes. REFERENCES Aiken CG. 1992. The causes of perinatal mortality in Bulawayo, Zimbabwe. Central African Journal of Medicine 38(7):263–281. Ahlenius I, Thomassen P. 1999. The changing panorama of late fetal death in Sweden between 1984 and 1991. Acta Obstetricia et Gynecologia Scandinavica 78:408–414. Amoa AB, Klufio CA, Moro M, Kariwiga G, Mola G. 1998. A case-control study of stillbirths at the Port Moresby General Hospital. Papua New Guinea Medical Journal 41(3–4):126–136. Ananth CV, Savitz DA, Luther ER. 1996. Maternal cigarette smoking as a risk factor for placental abruption, placenta previa, and uterine bleeding in pregnancy. American Journal of Epidemiology 144(9):881–889. Ananth CV, Berkowitz GS, Savitz DA, Lapinski RH. 1999. Placental abruption and adverse perinatal outcomes. Journal of the American Medical Association 282(17):1646–1651. Andersen A-MN, Wohlfart J, Christens P, Olsen J, Melbye M. 2000. Maternal age and fetal loss: a population-based register linkage study. British Medical Journal 320(7251):1708–1712. Ashley D, McCaw-Binns A, Golding J, Keeling J, Escoffery C, Coard K, Foster-Williams K. 1994a. Perinatal mortality survey in Jamaica: aims and methodology. Paediatric and Perinatal Epidemiology 8(suppl 1):6–16. Ashley D, Samms-Vaughan M, Greenwood R, Golding J. 1994b. The contribution of twins to perinatal mortality in Jamaica. Paediatric and Perinatal Epidemiology 8(suppl 1):158–165. Bacci A, Manhica GM, Machungo F, Bugalho A, Cuttini M. 1993. Outcome of teenage pregnancy in Maputo, Mozambique. International Journal of Gynaecology and Obstetrics 40(1):19–23. Baja-Panlilio H, Cabigas-Resurreccion J, Matanguihan AT, Cadorna JB, Sarmiento B, Villamoran-Baviera E. 1986. Perinatal morbidity and mortality in the Philippines. Asia Oceania Journal of Obstetrics and Gynaecology 12(3):331–339. Barros FC, Victora CG, Vaughan JP, Estanislau HJ. 1987. Perinatal mortality in southern Brazil: a population-based study of 7392 births. Bulletin of the World Health Organization 65(1):95–104. Bax M, Nelson KB. 1993. Birth asphyxia: a statement. Developmental Medicine and Child Neurology 35:1022–1024. Beard JL. 2000. Effectiveness and strategies of iron supplementation during pregnancy. American Journal of Clinical Nutrition 71(suppl):1288–1294. Bendon RW. 2001. Review of some causes of stillbirth. Pediatric and Developmental Pathology 4(6):517–531.

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