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Neonatal mortality of low-birth-weight infantsin BangladeshSohely Yasmin,1 David Osrin,2 Elizabeth Paul,3 & Anthony Costello4 Objective To ascertain the role of low birth weight (LBW) in neonatal mortality in a periurban setting inBangladesh.
Methods LBW neonates were recruited prospectively and followed up at one month of age. The cohort ofneonates were recruited after delivery in a hospital in Dhaka, Bangladesh, and 776 were successfully followed upeither at home or, in the event of early death, in hospital.
Findings The neonatal mortality rate (NMR) for these infants was 133 per 1000 live births (95% confidenceinterval: 110–159). The corresponding NMRs (and confidence intervals) for early and late neonates were 112 (91–136) and 21 (12–33) per thousand live births, respectively. The NMR for infants born after fewer than 32 weeks ofgestation was 769 (563–910); and was 780 (640–885) for infants whose birth weights were under 1500g. Eighty-four per cent of neonatal deaths occurred in the first seven days; half within 48 hours. Preterm delivery wasimplicated in three-quarters of neonatal deaths, but was associated with only one-third of LBW neonates.
Conclusion Policy-relevant findings were: that LBW approximately doubles the NMR in a periurban setting inBangladesh; that neonatal mortality tends to occur early; and that preterm delivery is the most importantcontributor to the NMR. The group of infants most likely to benefit from improvements in low-cost essential care forthe newborn accounted for almost 61% of neonatal mortalities in the cohort.
Keywords Infant mortality; Infant, Low birth weight; Prospective studies; Cohort studies; Bangladesh (source: MeSH ).
Mots cle´s Mortalite´ nourrisson; Nourrison faible poids naissance; Etude prospective; Etude cohorte; Bangladesh(source: INSERM ).
Palabras clave Mortalidad infantil; Recie´n nacido de bajo peso; Estudios prospectivos; Estudios de cohortes;Bangladesh (fuente: BIREME ).
Bulletin of the World Health Organization, 2001, 79: 608–614.
Voir page 613 le re´sume´ en franc¸ais. En la pa´gina 613 figura un resumen en espan˜ol.
per thousand live births (6). However, the NMRs candiffer by rural, urban and other locations (2, 7), even Perinatal and neonatal mortality are increasingly within large demographic surveys (8).
important public health issues in many developing Low birth weight (LBW) is defined as a birth countries, as postneonatal mortality rates fall (1). In weight of less than 2500 g and is a well-documented Bangladesh, for example, the infant mortality rate risk factor for neonatal mortality (9, 10). In appears to have fallen this century from over Bangladesh, for example, the LBW prevalence 200 deaths per thousand live births to approximately varies between 23% and 60% (11–13) and this has 80 deaths per thousand live births (2–4). By contrast, presumptive effects on stillbirth and neonatal death neonatal deaths now account for about two-thirds of rates. Despite the apparent importance of LBW as the 8 million infant deaths that occur globally each an indicator, there have been few prospective year (5), and the neonatal mortality rate (NMR) in studies of outcome for LBW infants in developing Bangladesh was recently estimated to be 65 deaths countries, largely because of the difficulties inherentin community-based data collection. The definition 1 Associate Professor, Department of Community Medicine, Dhaka of LBW also fails to distinguish between LBW neonates who are premature and those who are 2 Honorary Research Fellow in International Child Health, Centre for merely small for their gestational age. As a result, International Child Health, Institute of Child Health, London, England.
there is a lack of information about infant mortality 3 SeniorLecturerinMedicalStatistics,RoyalLondonandSt Bartholomew’s in the first four weeks of life, and this has hindered the development of appropriate neonatal interven- Professor of International Child Health, Centre for International tions. In this paper we report the findings of a Child Health, Institute of Child Health, 30 Guilford Street, LondonWC1N 1EH (email: a.costello@ich.ucl.ac.uk). Correspondence should prospective cohort study of LBW infants in Dhaka, Bangladesh, and have modelled the effects of Bulletin of the World Health Organization, 2001, 79 (7) Mortality of low-birth-weight infants in Bangladesh informed consent for participation was obtainedfrom each mother before data collection.
Criteria for including an infant in the study Bangladesh has a population of 126 million and a growth rate of 2.0%. Per capita income is US$ 370 The infant had completed more than 28 weeks of per annum. The literacy rate is 63% for men and 48% gestation, and had a birth weight less than 2500 g.
for women. The average household size is 5.6 people The family residence was within 80 km of the and 16% of households do not own land (3). Up to study site and the household location was 90% of women in Bangladesh marry by 18 years of age and most conceive in their teens (14). Health care The mother gave verbal consent to inclusion.
for mothers and children is minimal: community-based support during pregnancy is available from Neonates who did not meet all of the above inclusion family welfare assistants, but the responsibilities of criteria, or who suffered a significant congenital the assistants are often unfeasibly broad. For anomaly, were excluded from the study. Both example, they bear the burden of referring the stillbirths and livebirths were recorded, but only the estimated 600 000 high-risk pregnancies in visitors to latter are reported here. Data were collected by a team of four paediatric medical officers and one clerical assistant. Their one-month induction period com- maternity service at Mitford Hospital, a government- prised a week of discussion, planning and ques- run centre which hosts about 4000 deliveries per year.
tionnaire design; a week of anthropometric and Although services are free in principle, attendance clinical assessment training; a week of clinical involves both explicit and implicit costs (15). The practice; and a week of questionnaire pretesting, hospital is adjacent to the Buriganga river in the old part of Dhaka and draws clients from urban, Infant anthopometric data were recorded at the suburban and rural areas. Seventy-five per cent of time of birth. Birth weight was measured with infants service users are classified as living in poverty. The undressed on a portable Soehnle 831 000 scale, with high uptake of services at the hospital is probably an accuracy to within 10 g. Birth length was measured explained by the low cost of the services and by the with a portable, non-stretch/shrink-toughened difficulties of delivering home services in the nearby plastic roll-up mat with an accuracy of 0.5 cm congested slums. After presentation at the hospital, (Rollametre). The circumference of the head, mid- the majority of births take place within two days. The upper arm and chest were measured using a plastic subsequent hospital stay is usually six hours, unless tape with an accuracy of 1 mm. Gestational age was the mother or infant experiences problems. It is assessed clinically by the method of Dubowitz, as recommended that mothers stay in hospital for adapted by Capurro (18). Maternal postdelivery 10 days after caesarean section, or for as long as weight was measured with women lightly clothed infants require specialized care. Specialized care is on a Soehnle 7209 scale with a weight range of provided in a neonatal unit in the form of incubator 0–130 kg and accuracy to within 200 g. Height was care, antimicrobials and nasogastric or intravenous measured with a wall-hung plastic injection-moulded hydration. Hospital records suggest an LBW pre- scale with an accuracy of 1 mm (Minimeter 183).
valence of 30%, and there is usually more than one Questionnaires were administered within a few hours of birth and covered areas that included past obstetrichistory, history of the present pregnancy and socio- The cohort of infants was recruited at the time of LBW was defined as a birth weight of less than birth in the hospital and consisted solely of LBW 2500 g, regardless of gestational age. Preterm delivery infants, who were to be followed up at home. The implied a gestation at birth of less than 37 completed objective was to quantify mortality in this high-risk weeks, while term was defined as a gestational age of population over the course of the first month of 37–42 completed weeks. NMR was defined as the extrauterine life. Ethical approval for the study was number of deaths in the first 28 days after birth per obtained from the Bangladesh Medical Research thousand live births. Early NMR (ENMR) refers to deaths on days 0–6; late NMR (LNMR) to deaths on Infants were enrolled consecutively between May 1994 and September 1995. Enrolment ran for If an infant died before discharge from the six days per week, excepting religious holidays hospital, an immediate verbal autopsy was sought and (15 days) and strikes (10 days). The theoretical the diagnosis confirmed with attending doctors.
sample size required to yield 90 deaths (for risk Death at home was assessed after a period of 28 days factor analysis) was projected from population by the principal investigator, who recorded the age at estimates of NMR (16, 17) at a power of 80% and death and conducted a verbal autopsy by parental a two-sided alpha of 0.05. During the enrolment interview. The verbal autopsy method used a format period, every birth in the maternity unit was developed by a WHO advisory team and allowed for attended by a member of the study team. Verbal 15 causes of death, including a category for unknown Bulletin of the World Health Organization, 2001, 79 (7) causes (19). For ethical reasons, infants received 345 women weighed less than 45 kg (37%). Mean medical treatment if the investigators felt that it was height was 150 cm (SD = 4.7 cm) and the 10th centile was 145 cm. Some 731 women (78%) had blood Data from seven questionnaires were entered haemoglobin levels below 11 g/dl and were into loose-leaf paper files that were collected and considered to be anaemic on this basis. Twenty- reviewed weekly, and compiled in an electronic three per cent of the mothers received no antenatal database by the principal investigator. Data cleaning care, 374 (48%) were primiparous, and 23 (3%) had and analysis were performed within STATA (Inter- delivered their fifth child or higher. Maternal age cooled STATA 5.0 for Macintosh, Stata Corporation, ranged from 14 to 45 years (interquartile range: USA). Baseline characteristics were analysed with 20–26 years; median: 22 years). Many of the women two-sample comparison of means, one-way ANOVA did not know their age, and clustering in the data and analogous nonparametric tests. Mortality rates distribution around multiples of five may result from were computed arithmetically and confidence inter- vals estimated using binomial methods.
The birth weights of the cohort infants were at the lower end of a normal distribution and weretherefore nonparametrically distributed. The lowest values observed were approximately 500 g; but 92%of the infants weighed 1500 g or more, and 69% weighed 2000 g or more. Birth lengths ranged from The outcomes for cohort infants during this study are 25 cm to 54.5 cm (interquartile range 42.8– summarized in Fig. 1. Of 937 liveborn infants 46.5 cm), head circumferences from 18 cm to enrolled, outcome data were available for 776, 39.5 cm (interquartile range 23–37 cm), and chest representing a loss to follow-up of 17%. Selected circumferences from 16–36.6 cm (interquartile socioeconomic and demographic findings for the cohort families are presented in Table 1. The monthly Gestational age at birth and birth weight were income of most cohort families was under 3000 taka available for 931 infants, allowing the generation of (US$ 66), although 53% of the fathers were in regular categorical variables for preterm and term delivery employment as skilled manual workers (predomi- and for birth weight band (Table 2). Predictably, preterm birth contributes disproportionately to the Most of the mothers were Muslim (77%) and lower birth weight bands: 94% of infants with birth about one-third had received no formal schooling, weights less than 1500 g were preterm, compared one-half had been educated at primary level, and 13% with only 25% of infants with birth weights between had progressed to secondary school. Twenty-seven 2000 and 2499 g. The relative importance of each per cent of them had married in their teens. Maternal birth weight band is also presented in the table: postdelivery weight was normally distributed about a over 70% of LBW infants fell into the 2000– mean of 47 kg (standard deviation (SD) = 6.1 kg); Bulletin of the World Health Organization, 2001, 79 (7) Mortality of low-birth-weight infants in Bangladesh Table 1. Socioeconomic and demographic characteristics of cohort The contribution of birth weight and gestational bands to overall mortality is summarized in Table 3.
There were 103 neonatal deaths, of which 43 oc- curred within 48 hours of birth, and 87 within the first six days; 81 of the deaths occurred in hospital, 22 at home. Verbal autopsy implicated birth asphyxia (as encephalopathy) in 34% of the cases, and infection (as either generalized sepsis or pneumonia) in 9% of neonatal deaths. In 45% of the cases, no cause otherthan LBW or preterm delivery could be identified.
Kaplan–Meier survival plots for bands of birth weight and gestation are shown in Fig. 2, which underscore the impressions that infant mortality varies with birth weight and gestation period, and thatthe greatest risk of infant death occurs early in the Over one-third of all infant deaths occurred in the very low-birth-weight (VLBW, below 1500 g) group (38% of deaths, Table 3), despite the low prevalence of VLBW infants (7% of all LBW, Table 2). Similarly, preterm births are implicated in 75% of neonatal deaths (Table 3), but account for only 39% of LBW infants in the cohort (Table 2).
Thirty-nine per cent of deaths occurred in infants who weighed less than 1500 g at birth, were born at less than 32 weeks gestation, or both; conversely, 61% of neonatal deaths occurred in infants with birth weights 1500–2499 g and gestation periods of The data show that the overall NMR was 133, the ENMR was 112 and the LNMR 21 per thousand live births (Table 4). Predictably, the NMRs forcertain groups were much higher: 78% (NMR = 780per thousand live births) of very low-birth-weightinfants (VLBW, below 1500 g) died in the neonatal Table 2. Contributions of term and preterm deliveries to birthweight bands period, whereas only 5% of neonates with birthweights 2000–2499 g died in the same period. Also, preterm infants were five times as likely to die as term infants (risk ratio: 4.78; 95% confidence interval3.14–7.27); indeed, infants born at fewer than 32 weeks of gestation had a NMR comparable to that of VLBW infants (77% died in the neonatal It may not be possible to generalize the conclusions been at higher risk of dying if born in the community.
of this study because the cohort was recruited from a Loss to follow-up is also likely to be biased towards hospital, where service users tend to come from social groups at higher risk of mortality, so that late groups with higher socioeconomic status and lower neonatal deaths may be overrepresented in the drop- exposure to risk. However, our sample population out group. Thus, even though our ENMR figures for was poor by any standards, and the maternal birth weight and gestational bands are consistent with demographic and anthropometric features in the earlier results (22), we advise caution when using our cohort were similar to others described in Bangladesh data since the balance of biases may underestimate (20, 21), although this may reflect the high level of the ENMR and LNMR in the general population.
ambient risk factors in a population homogeneous Support for this idea comes from the observation that for deprivation. Alternatively, referral for hospital LBW prevalence is 30% in Mitford hospital, 10% delivery may select for the more at risk; and the fact lower than the national estimate. There may also be a that the majority of infant deaths occurred in hospital systematic downward bias in the assessment of raises the question of whether the infants would have gestational age, since we relied, of necessity, on the Bulletin of the World Health Organization, 2001, 79 (7) method of Capurro (18). The group of preterm Table 3. Neonatal mortality by birth weight and gestation period neonates would thus be overascribed, since infantswith intrauterine growth retardation (IUGR) may achieve lower scores on such profiles.
Our findings show that several factors influ- ence the NMR, which need to be addressed if neonatal survival is to be improved. The most obvious factor is LBW. The cohort consisted entirely of LBW infants, and the NMR was 133 deaths per thousand live births, roughly double the figures forunselected South Asian populations, which range from 50 to 97 deaths per thousand live births (11, 17, 23, 24). The next most striking finding is that 84%(95% confidence interval: 76–91%) of cohort deathsoccurred in the first week of extrauterine life, halfwithin the first 48 hours. This is generally consistentwith previous findings from Bangladesh indicatingthat 21% of neonates die within the first three days(25); comparable results have been reported forBrazil (26). By contrast, a study in the Gambia (NMR= 39 deaths per thousand livebirths) suggested thatearly and late neonatal deaths were roughly equal (27),although early deaths may have been underreported.
The data also show that VLBW is strongly associatedwith high mortality. VLBW infants made up only 7%of the LBW total, but accounted for a third of infantdeaths and had a mortality rate of 780 per thousandlive births. Like VLBW, lower gestational age at birthalso carries a high mortality risk (769 per thousandlive births at less than 32 weeks). More interesting,perhaps, is that 75% of all deaths occurred in preterminfants, even though they constituted only a third ofall LBW infants.
The majority of LBW infants in developing countries are small-for-dates rather than preterm(28), and the high prevalence of LBW can beexplained mainly on the basis of IUGR. For thisreason, IUGR has become a focus for potentialinterventions, two assumptions being that: (i) intra- Table 4. Neonatal, early neonatal and late neonatal mortality uterine growth may be more tractable to interven- rates, by birth weight and gestation period tions than preterm labour (although the degree oftractability remains questionable and there are over- laps in etiology between the two areas); and (ii) its numerical dominance in the etiology of LBW means that interventions to reduce IUGR will pay dividends in terms of outcome (29). This second assumption may be valid in the context of later morbidity, sinceIUGR may have effects on childhood growth, cognitive development and subsequent diseases in adulthood (30, 31). However, our study suggests that IUGR should not be emphasized alone, if neonatal mortality is to be reduced. Previous work suggests that preterm infants have a perinatal mortality rate Neonatal mortality rates are expressed as deaths per thousand live births. CI: 95% binomial 13 times higher than that of term infants of comparable birth weight, and twice that of infants with IUGR (32). This conclusion is supported by the ENMR = early neonatal mortality rates.
results presented in this study, showing that 75% ofall deaths in the LBW group were accounted for by LNMR = late neonatal mortality rates.
Sixty-one per cent of cohort deaths occurred to infants whose birth weights were 1500 g or more and Bulletin of the World Health Organization, 2001, 79 (7) Mortality of low-birth-weight infants in Bangladesh whose gestation periods were 32 weeks or more. This cessation of programmatic interventions and advo- is a group where an emphasis on essential newborn cacy aimed at improving women’s health, nutrition care may have large effects (33). It has been suggested over the life cycle and gender equity. Instead, that two-thirds of all first-week deaths can be programmatic agendas should include both the prevented by simple practices (22, 34, 35), and an prevention of preterm delivery and the prevention emphasis on the care of infants at high risk of dying and reduction of IUGR. We also advocate an may pay greater dividends in the short term than emphasis on essential care of the newborn infant at attempts to prevent the birth of LBW infants. Given community level, since the short-term effects of this the difficulties inherent in preventing IUGR and preterm delivery, there is a strong case for shifting thefocus of current discourse towards community-based care of the newborn. We do not propose a Conflicts of interest: none declared.
Mortalite´ ne´onatale chez les nourrissons de faible poids de naissance au BangladeshObjectif Evaluer le roˆle du faible poids de naissance vivantes et il e´tait de 780 (640-885) pour 1000 nais- dans la mortalite´ ne´onatale dans un secteur pe´riurbain sances vivantes chez ceux dont le poids de naissance e´tait infe´rieur a` 1500 g. Parmi les de´ce`s ne´onatals, 84 % Me´thodes Des nouveau-ne´s de faible poids de survenaient au cours des 7 premiers jours et la moitie´ naissance ont e´te´ recrute´s de fac¸on prospective et dans les 48 heures suivant la naissance. L’accouchement suivis a` l’aˆge d’un mois. Les nouveau-ne´s de la cohorte pre´mature´ e´tait implique´ dans les trois quarts des de´ce`s ont e´te´ inclus dans l’e´tude apre`s leur naissance dans un ne´onatals, mais n’e´tait associe´ qu’au tiers des insuffi- hoˆpital de Dhaka (Bangladesh) et 776 d’entre eux ont sances ponde´rales a` la naissance.
pu eˆtre suivis a` domicile ou, en cas de de´ce`s pre´coce, a` Conclusion Plusieurs observations sont inte´ressantes du point de vue des politiques de sante´ : le faible poids de Re´sultats Pour ces nourrissons, le taux de mortalite´ naissance double pratiquement le taux de mortalite´ ne´onatale e´tait de 133 pour 1000 naissances vivantes ne´onatale dans un secteur pe´riurbain du Bangladesh ; les (intervalle de confiance a` 95 % : 110-159). Les taux de´ce`s ne´onatals tendent a` eˆtre pre´coces ; l’accouche- correspondants (et leurs intervalles de confiance) pour les ment pre´mature´ est le facteur qui contribue le plus au de´ce`s ne´onatals pre´coces et tardifs e´taient respective- taux de mortalite´ ne´onatale. Le groupe de nourrissons ment de 112 (91-136) et 21 (12-33) pour 1000 nais- qui devrait tirer le plus grand be´ne´fice d’une ame´lioration sances vivantes. Le taux de mortalite´ ne´onatale pour les des soins de base peu couˆteux destine´s aux nouveau-ne´s nourrissons ne´s apre`s moins de 32 semaines de repre´sentait pre`s de 61 % des de´ce`s ne´onatals dans la grossesse e´tait de 769 (563-910) pour 1000 naissances Mortalidad neonatal entre lactantes de bajo peso al nacer en BangladeshObjetivo Determinar la contribucio´n del bajo peso al 1500 g al nacer la tasa fue de 780 (640–885). El 84% nacer (BPN) a la mortalidad neonatal en una zona de las defunciones neonatales se produjeron durante los primeros siete dı´as, y la mitad dentro de las primeras Me´todos Se recluto´ prospectivamente a recie´n nacidos 48 horas. El antecedente de un nacimiento prematuro se con BPN para su posterior seguimiento a la edad de un asociaba a las tres cuartas partes de las defunciones mes. Los neonatos de la cohorte habı´an nacido en un neonatales, pero so´lo a la tercera parte de los recie´n hospital de Dhaka (Bangladesh), y en 776 casos se logro´ seguir su evolucio´n ya fuera en el hogar o, entre los que Conclusio´n Con miras a la elaboracio´n de polı´ticas, fallecieron prematuramente, en el hospital.
revisten intere´s los siguientes datos: el BPN conlleva Resultados La Tasa de Mortalidad Neonatal (TMN) de aproximadamente una duplicacio´n de la TMN en un esos lactantes fue de 133 por 1000 nacidos vivos entorno periurbano de Bangladesh; las defunciones (IC95%: 110–159). Las TMN (e intervalos de confianza) neonatales suelen producirse tempranamente, y el correspondientes a los neonatos precoces y tardı´os nacimiento prematuro es el factor que ma´s contribuye fueron de 112 (91–136) y 21 (12–33) por mil nacidos a la TMN. El grupo de lactantes que ma´s puede vivos, respectivamente. La TMN para los lactantes beneficiarse de una mejora de la atencio´n ba´sica de bajo nacidos con menos de 32 semanas de gestacio´n fue de costo para el recie´n nacido represento´ casi el 61% de la 769 (563–910); y para los lactantes con menos de Bulletin of the World Health Organization, 2001, 79 (7) 1. Costello A. Perinatal health in developing countries. Transactions 20. Rawshan N. Effect of maternal nutrition and socio-economic of the Royal Society for Tropical Medicine and Hygiene, 1993, factors on birth weight of babies in Bangladesh. Bangladesh Medical Research Council Bulletin, 1978, 1: 1–9.
2. Faroque A. Infant mortality in Bangladesh: a review of recent 21. Canosa A. Intrauterine growth retardation in India and evidence. Journal of Biological Science, 1991, 23: 327–336.
Bangladesh. Nestle Nutrition Workshop Series, 1989, 18: 3. 1995 Statistical Yearbook of Bangladesh. Dhaka, Bangladesh 22. Shah U, Pratinidhi A, Bhatlawande P. Perinatal mortality 4. The state of the world’s children 1998. Oxford and New York, in rural India: intervention through primary health care. II Neonatal United Nations Children’s Fund, 1998.
mortality. Journal of Epidemiology and Community Health, 1984, 5. Costello AM, Singh ME. Recent developments for neonatal health in developing countries. Seminars in Neonatology, 1999, 23. Nessa S, Arco E, Kabir I. Birth kits for safe motherhood in Bangladesh. World Health Forum, 1992, 13: 66–69.
6. Perinatal mortality: a listing of available information. Geneva, 24. Misra P et al. Perinatal mortality in rural India with special World Health Organization, 1996 (unpublished document reference to high risk pregnancies. Journal of Tropical Pediatrics, 7. Fauveau V et al. Perinatal mortality in Matlab, Bangladesh: a 25. Salway S, Nasim S. Levels, trends and causes of mortality in community-based study. International Journal of Epidemiology, children below 5 years of age in Bangladesh: findings from a national survey. Journal of Diarrhoeal Disease Research, 1994, 8. Demographic and health survey 1993–1994. Dhaka, Bangladesh, Mitra and Associates and Macro International Inc., 1994.
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10. McIntire D et al. Birth weight in relation to morbidity and Annals of Tropical Paediatrics, 1999, 19: 33–43.
mortality among newborn infants. New England Journal of 28. Villar J, Belizan J. The relative contribution of prematurity and fetal growth retardation to low birth weight in developing and 11. Atlas of South Asian women and children. Kathmandu, United developed countries. American Journal of Obstetrics and 12. The progress of nations. New York, United Nations Childrens 29. Villar J et al. A health priority for developing countries: the prevention of chronic fetal malnutrition. Bulletin of the World 13. Nahar N. Recent trends in perinatal health in South Asia: Health Organization, 1986, 64: 847–851.
Bangladesh. In: Costello A, Manandhar D, eds. Improving 30. Barker DJP. Fetal origins of coronary heart disease. British newborn infant health in developing countries. London, Imperial Medical Journal, 1995, 311: 171–174.
31. Lucas A. Role of nutritional programming in determining adult 14. Bangladesh country statistics (2001) (UNICEF website: morbidity. Archives of Disease in Childhood, 1994, 71: 288–290.
32. Barros F et al. Comparison of the causes and consequences of 15. Nahar S, Costello A. The hidden cost of ‘‘free’’ maternity care prematurity and intrauterine growth retardation: a longitudinal in Dhaka, Bangladesh. Health Policy and Planning, 1998, study in southern Brazil. Pediatrics, 1992, 90: 238–244.
33. Costello A, Manandhar D. Current status of newborn care 16. Rahman M et al. Impact of environmental sanitation and in developing countries. In: Costello A, Manandhar D, eds.
crowding on infant mortality in rural Bangladesh. Lancet, 1985, Improving newborn infant health in developing countries. London, 17. Rahman S, Nessa F. Neonatal mortality patterns in rural 34. Ghosh S, Daga S. Comparison of gestational age and weight Bangladesh. Journal of Tropical Pediatrics, 1989, 35: 199–202.
as standards of prematurity. Journal of Pediatrics, 1967, 71: 18. Capurro H et al. A simplified method for diagnosis of gestational age in the newborn infant. The Journal of Pediatrics, 1978, 35. Mavalankar D, Trivedi C, Gray R. Levels and risk factors for perinatal mortality in Ahmedabad, India. Bulletin of the World 19. Bang A et al. Diagnosis of causes of childhood deaths in Health Organization, 1991, 69: 435–442.
developing countries by verbal autopsy: suggested criteria.
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