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Departments of Pediatrics and of Epidemiology & Biostatistics, McGill University Faculty of Medicine, Montreal, Quebec, Canada
2 To whom correspondence should be addressed. E-Mail: michael.kramer{at}mcgill.ca.
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ABSTRACT |
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 TOP ABSTRACT LITERATURE CITED |
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KEY WORDS: • infant mortality • stillbirth • low birth weight • preterm birth • intrauterine growth restriction
In most developed countries, pregnancies are planned, complications are few and outcomes are generally favorable for both mother and infant. Adverse outcomes are far more frequent in the developing world. The most severe adverse outcome of pregnancy is the death of the mother or her offspring. Maternal death has become an extremely rare event in the developed world, with many countries reporting maternal mortality ratios of 5–10 per 100,000 live births. In the least developed countries, the ratios are 100 times higher (1, 2). Disparities in infant deaths are not quite as wide but remain substantial, ranging from 4–5 to >100 per 1000 live births (3, 4). Wide disparities probably also exist in the rate of late fetal deaths (stillbirths), although fetal deaths in developing countries are grossly underreported (5, 6). Even if both the mother and infant survive, pregnancy complications or problems at delivery or during the neonatal period can lead to severe maternal or infant morbidity (7– 11).
Despite the recognized importance of mortality and severe morbidity as measures of adverse pregnancy outcome, much of the published research in the area of adverse pregnancy outcomes, especially those outcomes related to maternal nutrition, are based on proxy outcomes for mortality and severe morbidity. The most commonly studied of these proxies have been low birth weight (LBW) 3, including its constituents, preterm birth and intrauterine growth restriction (IUGR) and congenital anomalies.
Low birth weight is defined by the World Health Organization (WHO) as a birth weight <2500 g. Birth weight, however, is determined by two processes: duration of gestation and rate of fetal growth (12). Thus, infants can have a birth weight <2500 g either because they are born early (preterm birth) or are born small for gestational age (SGA), a proxy for IUGR. WHO defines preterm birth as delivery before 37 completed weeks of gestation and SGA as a birth weight below the 10th percentile for gestational age based on the sex-specific reference by Williams et al. (13). Some SGA infants are merely constitutionally small rather than nutritionally growth restricted; conversely, some IUGR infants who would otherwise be constitutionally large do not meet the standard criteria for SGA. Moreover, newborn infants may be growth-restricted or preterm without having LBW (14). For example, the WHO cutoff for SGA for males at 40 wk is 2944 g whereas the median birth weight for males at 35 wk is 2562 g (13).
One of the reasons that LBW continues to be reported and studied by epidemiologists and public health practitioners is that it can be measured with excellent validity and precision. Measuring preterm birth or IUGR requires a valid estimate of gestational age, which is often difficult in developing countries because of late and infrequent access to prenatal care, inadequate documentation of the date of the last menstrual period and unavailability of early ultrasound examination.
Despite widespread recognition of the importance of LBW in developing countries, reliable data on its magnitude and distribution remain limited. de Onis et al. (15) recently compiled information on birth outcomes around the world, from which they estimated that 20.5 million LBW infants were born in 1995 and that 16% of all newborns in developing countries were LBW. Table 1 is taken from data reported in the WHO Collaborative Study of maternal anthropometry and pregnancy outcomes (16), the United Nations Children's Fund's The State of the World's Children 2003 (4), and the March of Dimes' PeriStats (17). In countries where the prevalence of LBW is very high, most LBW infants are growth restricted rather than preterm (15, 18). As seen in Table 1, the prevalence of IUGR varies widely among developing countries: 30–55% of infants born in South Central Asia versus 15–25% in Africa and 10–20% in Latin America. Caution is again advised in interpreting the values in Table 1 because of the absence of universal birth registration and the poor gestational age data in many developing countries.
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Methodological issues
Fetal growth trajectories. Various body proportionality indices have been used to relate different dimensions of fetal growth, particularly among growth-restricted infants. The most commonly used of these is Rohrer's ponderal index, a measure of birth weight relative to birth length, which is defined as 100 times the birth weight in grams divided by the birth length in centimeters cubed. The ponderal index is often then used to subdivide IUGR infants into those who are proportionate (also called symmetric or stunted) and disproportionate (asymmetric or wasted) (40, 41). Many investigators have assumed that differences in proportionality at birth reflect differences in timing of intrauterine growth restriction on the basis of highly diagrammatic fetal growth velocity curves published by Tanner (42), which suggested deceleration in length growth in the second trimester. In fact, studies based on serial ultrasound measurements (43) or prostaglandin-induced pregnancy terminations (44– 46) clearly demonstrate that crown-to-heel length, biparietal diameter and head circumference increase linearly throughout the second trimester. Moreover, proportionality among IUGR infants is strongly confounded by the severity of the growth restriction (i.e., disproportionate IUGR infants tend to be more severely growth restricted than their proportionate counterparts) (47, 48).
Stillbirth. A number of important methodological issues arise with respect to stillbirth. As previously mentioned, stillbirths are grossly underregistered in developing countries (5, 6). However, even in developed countries, wide differences exist concerning the gestational age at which stillbirth registration is legally required and in the classification of stillbirths versus live births despite universal adoption of the WHO International Classification of Diseases definition of a live birth (49).
Total stillbirth rates are generally reported as the number of stillbirths beyond a certain gestational age or birth weight (typically 20 or 22 wk and 500 g, respectively) divided by the number of total births (live births plus stillbirths) that meet the same gestational age or birth weight criteria. Many epidemiologists and public health practitioners, however, have stratified the overall stillbirth rate by gestational age or birth weight. This is clearly inappropriate because the denominator (the number of stillbirths and live births at a given gestational age or birth weight) are only a subgroup of all fetuses at risk, and the resulting proportion (rate) is conditional on birth at that gestational age or birth weight. This type of inappropriate measure of stillbirth risk leads to the completely mistaken notion that stillbirth risk decreases as gestation advances. In fact, when the risk of stillbirth is expressed appropriately as a proportion of all ongoing pregnancies, the risk rises as term approaches and is highest in the postterm period (50, 51).
Measurement issues. Our ability to measure micronutrient intake is a problem because of imprecision in the measurement of dietary intake and variation in intake over time, particularly as gestation advances (52, 53). Micronutrient status is also affected by variations in metabolism and excretion, and blood levels of many micronutrients may vary as a result of physiological dilution caused by the plasma volume expansion that is a normal physiological manifestation of pregnancy (54). Blood levels are also subject to other environmental and physiological influences. For example, zinc concentrations fall (55) and ferritin concentrations rise (56) in response to infection.
Causal inference. In isolating the effect of one or more micronutrients on pregnancy outcome, an important methodological issue to consider is the strong correlation among micronutrients and between micronutrients and macronutrients. This creates a large potential for confounding by other micronutrients and by overall energy intake and leads to major inferential problems for causality (12).
Confounding is also a major issue with respect to socioeconomic status and the above-noted hemodynamic changes. Women with low micro- and macronutrient intakes are often those of lower education and income, which are associated with many adverse behavioral and psychosocial factors that can cause adverse pregnancy outcomes, such as cigarette smoking, drug use, sexual practices and stress (57). Plasma volume expansion can lower micronutrient levels and thus negatively confound the true effects of micronutrient deficiency (54). These issues of confounding underline the importance of randomized trials of individual micronutrients or combinations of micronutrients in establishing causal effects and in evaluating interventions to prevent adverse pregnancy outcomes.
Temporal trends
Temporal trends in adverse pregnancy outcomes have provided a mixture of both good news and bad. The good news is that infant mortality has fallen in many parts of the world. It is essential to point out that this decrease in infant mortality has occurred on a background of little or no success in preventing LBW. Rather, infant mortality has been reduced at all birth weights, including infants of normal birth weight (58– 60). In some developing countries with reliable national or regional birth registration, preterm birth appears to be on the rise (61, 62), as has been reported from most developed countries (63– 65). The temporal increase in preterm birth is primarily due to an increase in obstetric intervention, which is often motivated by a desire to reduce the risk of stillbirth and of maternal mortality and severe morbidity (66). In developed countries a rise in multiple births (attributable to hormonal treatments and assisted reproduction technologies for infertility) has also been an important cause of the trend toward increasing preterm birth (67).
Some developed countries, including Canada, the United States and Norway have reported a temporal increase in fetal growth and particularly in the size of infants born at term (68– 70). No consistent increase has been seen in the size of preterm infants.
Several developed countries have reported a fall in stillbirth rates (63). Neural tube defects have recently been falling in developed countries, particularly those that have promoted preconceptional folic acid supplementation and (probably even more importantly) food fortification with folic acid (71, 72). Data from China suggest that folic acid supplementation is a feasible public health objective in developing countries as well (73). A recent report from Canada has shown, for the first time, that prevention and termination of pregnancies with congenital anomalies has had a perceptible effect on overall infant mortality (74). The prospects are excellent that this trend will continue in the future and it is hoped that it will spread to developing countries as well.
Despite this evidence of progress, important gaps remain in our knowledge base:
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FOOTNOTES |
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3 Abbreviations used: BMI, body mass index; IUGR, intrauterine growth restriction; LBW, low birth weight; SGA, small for gestational age; WHO, World Health Organization.
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LITERATURE CITED |
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TOPABSTRACTLITERATURE CITED |
|---|
1. Rosenfield, A. & Maine, D., (1985) Maternal mortality—a neglected tragedy Where is the M in MCH? Lancet. 2: 83–85.[Medline]
2. AbouZhar, C. & Wardlaw, T. (2001) Maternal mortality at the end decade: what signs of progress? Bull. WHO. 79: 561–573.[Medline]
3. Save the Children. (2001) State of the World's Newborns. Available: http://www.savethechildren.org/mothers/newborns. Accessed October 7, 2002.
4. United Nations Children's Fund. The State of the World's Children 2003. Available at http://www.unicef.org. Accessed January 8, 2003.
5. Lumbiganon, P., Panamonta, M., Laopaiboon, M., Pothinam, S. & Patithat, N. (1990) Why are Thai official perinatal and infant mortality rates so low? Int. J. Epidemiol. 19: 997–1000.
6. McCaw-Binns, A. M., Fox, K., Foster-WIlliams, K. E. Ashley, D. E., & Irons, B. (1996) Registration of births, stillbirths and infant deaths in Jamaica. Int. J. Epidemiol. 25: 807–813.
7. Stones, W., Lim, W., Al-Assawi, F., & Kelly, M. (1991) An investigation of maternal morbidity with identification of life-threatening "near miss" episodes. Health Trends. 23: 13–15.[Medline]
8. Bouvier-Colle, M-H, Salanave, B., Ancel, P-Y, Varnoux, N., Fernandez, H., Papiernik, E., Bréart, G., and the regional teams for the survey: Benhamou, D., Boutroy, P., Caillier, E., Dumoulin, M., Fournet, P., Elhassani, M., Puech, F., & Poutot, C. (1996) Obstetric patients treated in intensive care unts and maternal mortality. Eur. J. Obstet. Gynecol. Reprod. Biol. 65: 121–125.[Medline]
9. Tinker, A. (2000) Women's health: the unfinished agenda. Int. J. Gynaecol. Obstet. 70: 149–158.[Medline]
10. McCormick, M. (1985) The contribution of low birth weight to infant mortality and childhood morbidity. N. Engl. J. Med. 312: 82–90.[Abstract]
11. Page, J. M., Schneeweiss, S., Whyte, H. E. A. & Harvey, P. (1993) Ocular sequelae in premature infants. Pediatrics 92: 787–790.
12. Kramer, M. S. (1987) Determinants of low birth weight: methodological assessment and meta-analysis. Bull. World Health Organ. 65: 663–737.[Medline]
13. Williams, R. L., Creasy, R. K., Cunningham, G. C., Hawes, W. E., Norris, F. D. & Tashiro, M. (1982) Fetal growth and perinatal viability in California. Obstet. Gynecol. 59: 624–632.[Medline]
14. Kramer, M. S. & Victora, C. G. (2001) Low birth weight and perinatal mortality. In: Nutrition and Health in Developing Countries (Semba, R. D. & Bloem, M. W., eds.), pp. 57–69. Humana Press, Totowa, NJ.
15. de Onis, M., Blossner, M. & Villar, J. (1998) Levels and patterns of intrauterine growth restriction in developing countries. Eur. J. Clin. Nutr. 52 (Suppl. 1), S5–S15.
16. World Health Organization. (1995) Maternal anthropometry and pregnancy outcomes. WHO Collaborative Study. Bull. World Health Organ 73: 1–68.
17. March of Dimes. Perinatal Profiles: Statistics for Monitoring State Maternal and Infant Health. Available at http://www.modimes.org. Accessed January 8, 2003.
18. Villar, J. & Belizan, J. M. (1982) The relative contribution of prematurity and fetal growth retardation to low birth weight in developing and developed societies. Am. J. Obstet. Gynecol. 143: 793–798.[Medline]
19. Kramer, M. S. (1990) Birth weight and infant mortality: perceptions and pitfalls. Paediatr. Perinat. Epidemiol. 4: 381–390.[Medline]
20. Zhu, B.-P., Rolfs, R. T., Nangle, B. E. & Horan, J. M. (1999) Effect of the interval between pregnancies on perinatal outcomes. N. Engl. J. Med. 340: 589–594.
21. Shults, R. A., Arndt, V., Olshan, A. F., Martin, C. F. & Royce, R. A. (1999) Effects of short interpregnancy intervals on small-for-gestational age and preterm births. Epidemiology 10: 250–254.[Medline]
22. Erickson, J. D. & Bjerkedal, T. (1978) Interpregnancy interval: association with birth weight, stillbirth, and neonatal death. J. Epidemiol. Community Health 32: 124–130.
23. Klebanoff, M. A. (1999) The interval between pregnancies and the outcome of subsequent births. N. Engl. J. Med. 340: 643–644.
24. Institute of Medicine. (1985) Preventing Low Birthweight. National Academy Press, Washington, D. C.
25. Kramer, M. S., Demissie, K., Yang, H., Platt, R. W., Sauvé, R. & Liston, R. (2000) for the Fetal and Infant Health Study Group of the Canadian Perinatal Surveillance System. The contribution of mild and moderate preterm birth to infant mortality. JAMA 284: 843–849.
26. Stewart, A. L., Rifkin, L., Amess, P. N., Kirkbride, V., Townsend, J. P., Miller, D. H., Lewis, S. W., Kingsley, D. P., Moseley, I. F., Foster, O. & Murray, R. M. (1999) Brain structure and neurocognitive and behavioural function in adolescents who were born very preterm. Lancet 353: 1653–1657.[Medline]
27. Hack, M., Wilson-Costello, D., Friedman, H., Taylor, G. H., Schluchter, M. & Fanaroff, A. A. (2000) Neurodevelopment and predictors of outcomes of children with birth weights of less than 1000 g: 1992–1995. Arch. Pediatr. Adolesc. Med. 154: 725–731.
28. Conde-Agudelo, A., Belizan, J. M. & Diaz-Rossello, J. L. (2000) Epidemiology of fetal death in Latin America. Acta Obstet. Gynecol. Scand. 79: 371–378.[Medline]
29. Huang, D. Y., Usher, R. H., Kramer, M. S., Yang, H., Morin, L. & Fretts, R. C. (2000) Determinants of unexplained antepartum fetal deaths. Obstet. Gynecol. 95: 215–221.[Medline]
30. Froen, J. F., Arnestad, M., Frey, K., Vege, A., Saugstad, O. D. & Stray-Pedersen, B. (2001) Risk factors for sudden intrauterine unexplained death: epidemiologic characteristics of singleton cases in Oslo, Norway, 1986–1995. Am. J. Obstet. Gynecol. 184: 694–702.[Medline]
31. Kramer, M. S., Olivier, M., McLean, E. H., WIllis, D. M. & Usher, R. H. (1990) The impact of intrauterine growth retardation and body proportionality on fetal and neonatal outcome. Pediatrics. 85: 707–713.
32. Albertsson-Wikland, K. & Karlberg, J. (1994) Natural growth in children born small for gestational age with and without catch-up growth. Acta Paediatr. 399: 64–70.
33. Strauss, R. S. (2000) Adult functional outcome of those born small for gestational age. JAMA 283: 625–632.
34. Goldenberg, R. L., Hoffman, H. J. & Cliver, S. P. (1998) Neurodevelopmental outcome of small-for-gestational-age infants. Eur. J. Clin. Nutr. 52 (Suppl. 1), S54–S58.
35. Hack, M. (1998) Effects of intrauterine growth retardation on mental performance and behavior, outcomes during adolescence and adulthood. Eur. J. Clin. Nutr. 52 (Suppl. 1), S65–S71.
36. Larroque, B., Bertrais, S., Czernichow, P. & Léger, J. (2001) School difficulties in 20-year olds who were born small for gestational age at term in a regional cohort study. Pediatrics 108: 111–115.
37. Paz, I., Laor, A., Gale, R., Harlap, S., Stevenson, D. K. & Seidman, D. S. (2001) Term infants with fetal growth restriction are not at increased risk for low intelligence scores at age 17 years. J. Pediatr. 138: 87–91.[Medline]
38. Barker, D. J. P. (1998) Mothers, Babies and Health in Later Life. Churchill Livingstone, Edinburgh.
39. Leon, D. A. (1998) Fetal growth and adult disease. Eur. J. Clin. Nutr. 52 (Suppl. 1), S72–S82.
40. Rosso, P. & Winick, M. (1974) Intrauterine growth retardation: a new systematic approach based on the clinical and biochemical characteristics of this condition. J. Perinat. Med. 2: 147–160.[Medline]
41. Miller, H. C. & Merritt, T. A. (1979) Fetal Growth in Humans. Year Book Medical, Chicago.
42. Tanner, J. M. (1979) Foetus Into Man: Physical Growth From Conception To Maturity. Harvard University Press, Cambridge, MA.
43. Campbell, S. & Newman, G. B. (1971) Growth of the fetal biparietal diameter during normal pregnancy. Trop. J. Obstetr. Gyn. Br. Commwlth. 78: 513–519.
44. Birkbeck, J. A., Billewicz, W. Z. & Thomson, A. M. (1975) Human foetal measurements between 50 to 150 days gestation, in relation to crown-heel length. Ann. Hum. Biol. 1: 173–178.
45. Birkbeck, J. A., Billewicz, W. Z. & Thomson, A. M. (1975) Fetal growth from 50 to 150 days gestation. Ann. Hum. Biol. 2: 319–326.[Medline]
46. Kaul, S. S., Bahn, A. & Chopra, S. R. K. (1986) Fetal growth from 12 to 26 weeks of gestation. Ann. Hum. Biol. 13: 563–570.[Medline]
47. Kramer, M. S., McLean, F., Olivier, M., Willis, D. M. & Usher, R. H. (1989) Body proportionality and head and length "sparing" in growth-retarded neonates: a critical reapparaisal. Pediatrics 84: 717–723.
48. Horta, B. L. (2001) Determinants of catch-up growth in small-for-gestational-age infants. PhD thesis, Dept. of Epidemiology & Biostatistics, McGill University, Montreal, Canada.
49. Kramer, M. S., Platt, R. W., Yang, H., Haglund, B., Cnattingius, S. & Bergsjo, P. (2002) Registration artifacts in international comparisons of infant mortality. Paediatr. Perinat. Epidemiol. 16: 16–22.[Medline]
50. Yudkin, P. L., Wood, L. & Redman, C. W. G. (1987) Risk of unexplained stillbirth at different gestational ages. Lancet i: 1192–1194.
51. Kramer, M. S., Liu, S., Luo, Z., Yuan, H., Platt, R. W. & Joseph, K. S. (2002) For the Fetal and Infant Health Study Group of the Canadian Perinatal Surveillance System. Analysis of perinatal mortality and its components: time for a Change? Am. J. Epidemiol. 156: 493–497.
52. Medlin, C. & Skinner, J. D. (1988) Individual dietary intake methodology: a 50–year review of progress. J. Am. Diet. Assoc. 88: 1250–1257.[Medline]
53. Institute of Medicine. (1990) Nutrition During Pregnancy. National Academy Press, Washington, D. C.
54. Food and Nutrition Board. (1978) Laboratory Indices of Nutritional Status in Pregnancy. National Academy Press, Washington, D. C.
55. Brown, K. H. (1998) Effect of infections on plasma zinc concentration and implications for zinc status assessment in low-income countries. Am. J. Clin. Nutr. 68: 425S–429S.[Abstract]
56. Eskeland, B., Baerheim, A., Ulvik, R. & Hunskaar, S. (2002) Influence of mild infections on iron status parameters in women of reproductive age. Scand. J. Prim. Health Care 20: 50–56.[Medline]
57. Kramer, M. S., Séguin, L., Lydon, J. & Goulet, L. (2000) Socio-economic disparities in pregnancy outcome: why do the poor fare so poorly? Paediatr. Perinat. Epidemiol. 14: 194–210.[Medline]
58. Lee, K. S., Kim, B. I., Khoshnood, B., Hsieh, H. L., Chen, T. J., Herschel, M. & Mittendorf, R. (1995) Outcome of very low birth weight infants in industrialized countries: 1947–1987. Am. J. Epidemiol. 141: 1188–1193.
59. Kalter, H., Na, Y. & O'Campo, P. (1998) Decrease in infant mortality in New York city after 1989. Am. J. Public Health 88: 816–820.
60. Joseph, K. S., Kramer, M. S., Allen, A. C., Cyr, M., Fair, M., Ohlsson, A. & Wen, S. W. (2000) Gestational age- and birthweight-specific declines in infant mortality in Canada, 1985–94. For the Fetal and Infant Health Study Group of the Canadian Perinatal Surveillance System. Paediatr. Perinat. Epidemiol. 14: 332–339.[Medline]
61. Silva, A. A. M., Barbieri, M. A., Gomes, U. A. & Bettiol, H. (1998) Trends in low birth weight: a comparison of two birth cohorts separated by a 15-year interval in Ribeirao Preto, Brazil. Bull. World Health Organ. 76: 73–84.[Medline]
62. Barros, F. C., Victora, C. G., Vaughan, J. P., Tomasi, E., Horta, B. L., Cesar, J. A., Menezes, M. B., Halpern, R., Post, C. L. & del Mar Garcia, M. (2001) The epidemiological transition in maternal and child health in a Brazilian city, 1982–93: a comparison of two population-based cohorts. Paediatr. Perinat. Epidemiol. 15: 4–11.[Medline]
63. Joseph, K. S., Kramer, M. S., Marcoux, S., Ohlsson, A., Wen, S. W., Allen, A. & Platt, R. (1998) Determinants of preterm birth rates in Canada from 1981 through 1983 and from 1992 through 1994. N. Engl. J. Med. 339: 1434–1439.
64. Kramer, M. S., Platt, R., Yang, H., Joseph, K. S., Wen, S. W., Morin, L. & Usher, R. H. (1998) Secular trends in preterm birth: a hospital-based cohort study. JAMA 280: 1849–1854.
65. Demissie, K., Rhoads, G. G., Ananth, C. V., Alexander, G. R., Kramer, M. S., Kogan, M. D. & Joseph, K. S. (2001) Trends in preterm birth and neonatal mortality among Blacks and Whites in the United States from 1989 to 1997. Am. J. Epidemiol. 154: 307–315.
66. Joseph, K. S., Demissie, K. & Kramer, M. S. (2002) Obstetric intervention, stillbirth, and preterm birth. Semin. Perinatol. 26: 250–259.[Medline]
67. Blondel, B., Kogan, M. D., Alexander, G. R., Dattani, N., Kramer, M. S., Macfarlane, A. & Wen, S. W. (2002) The impact of the increasing number of multiple births on the rates of preterm birth and low birthweight: an international study. Am. J. Public Health 92: 1323–1330.
68. Ananth, C. V. & Wen, S. W. (2002) Trends in fetal growth among singleton gestations in the United States and Canada, 1985 through 1998. Semin. Perinatol. 26: 260–267.[Medline]
69. Skjaerven, R., Gjessing, H. K. & Bakketeig, L. S. (2000) Birthweight by gestational age in Norway. Acta Obstet. Gynecol. Scand. 79: 440–449.[Medline]
70. Robertson, C. M. T., Svenson, L. W. & Kyle, J. M. (2002) Birth weight by gestational age for Albertan liveborn infants, 1985 through 1998. J. Obstet. Gynaecol. Can. 24: 138–148.[Medline]
71. Liu, S., Joseph, K. S., Wen, S. W., Kramer, M. S., Marcoux, S., Ohlsson, A. & Sauve, R. (2001) Secular trends in congenital anomaly-related fetal and infant mortality in Canada, 1985–1996. Am. J. Med. Genet. 104: 7–13.[Medline]
72. Olney, R. S. & Mulinare, J. (2002) Trends in neural tube defect prevalence, folic acid fortification, and vitamin supplement use. Semin. Perinatol. 26: 277–285.[Medline]
73. Berry, R. J., Li, Z., Erickson, J. D., Li, S., Moore, C. A., Wang, H., Mulinare, J., Zhao, P., Wong, L. Y. & Gindler, J. (1999) Prevention of neural-tube defects with folic acid in China. N. Engl. J. Med. 341: 1485–1490.
74. Liu, S., Joseph, K. S., Kramer, M. S., Allen, A. C., Sauve, R., Rusen, I. D. & Wen, S. W. (2002) Relationship of prenatal diagnosis and pregnancy termination to overall infant mortality in Canada. JAMA 287: 1561–1567.
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M. Merialdi, G. Carroli, J. Villar, E. Abalos, A. M. Gulmezoglu, R. Kulier, and M. de Onis Nutritional Interventions during Pregnancy for the Prevention or Treatment of Impaired Fetal Growth: An Overview of Randomized Controlled Trials J. Nutr., May 1, 2003; 133(5): 1626S - 1631. [Abstract] [Full Text] [PDF]
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