Discussion

The data presented confirm the magnitude of intrauterine growth retardation in developing countries. As summarized in Table 4, we estimate that at least 13.7 million babies in developing countries are already malnourished at birth (IUGR-LBW) every year, representing 11% (ranging from 1.9% to 20.9%) of all newborns in these countries. This rate is considerably higher than that estimated for developed countries, which is approximately 2%. Overall, the incidence of IUGR-LBW is about 6 times higher in developing than in developed countries (Villar et al, 1994).

The estimates for IUGR-LBW should be viewed as a conservative estimation of the magnitude of fetal growth retardation; the actual incidence of IUGR could be considerably higher. For example, if the rate of infants below the 10th percentile of the birth-weight-for-gestational-age reference curve is considered, 23.8%, or approximately 30 million newborns per year, would be affected (Table 4). There are nevertheless some healthy infants with birth weights below the 10th percentile, who represent the lower tail of a fetal growth distribution. However, in most developing countries a large proportion of newborns suffers from some degree of IUGR, as illustrated by the overall downward shift of the birth weight distribution. Unfortunately, a methodology to disentangle these two groups is not available.

Figure 3. Difference of observed and estimated IUGR-LBW rates plotted against the mean of the two rates using 17 data sets from developing countries.

Figure 4. Incidence of IUGR-LBW in developing countries, 1985-1995.

The destination employed and the presentation of material on this map do not imply the expression of any opinion whatsoever on the part of the World Health Organization concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted lines represent approximate border lines for which there may not yet be full agreement.

Table 3. Estimated incidence rate of LBW and IUGR-LBW, and expected number of affected newborns in a year

	Incidence LBW		Total incidence IUGR-LBW
United Nations regions and subregions	% (< 2500g)	Total numbers (thousand)	% (< 2500g; ³ 37 weeks)	Total numbers (thousand)
AFRICA	NAb	NAb	NAb	NAb
Eastern Africa	NAb	NAb	NAb	NAb
Middle Africa	21.3	792	14.9	554
Northern Africa	NAb	NAb	NAb	NAb
Southern Africa	NAb	NAb	NAb	NAb
Western Africa	17.2	1628	11.4	1001
ASIA	18.0d	14911d	12.3d	10147d
Eastern Asia	5.8d	1339d	1.9d	463d
South-central Asia	28.3	11833	20.9	8739
South-eastern Asia	10.3	1308	5.6	711
Western Asia	8.3	431	4.5	234
LATIN AMERICA AND THE CARIBBEAN	11.5	1370	6.5	779
Caribbean	11.7	84	6.7	48
Central America	12.3	440	7.2	258
South America	11.1	846	6.2	473
OCEANIA	15.0e	28.2e	9.8e	18.4e
Melanesia	15.4	28	9.9	18
Micronesia	NAb	NAb	NAb	NAb
Polynesia	4.0	0.2	0.2	0.4
DEVELOPING COUNTRIES	16.4	20423	11.0	13699
DEVELOPED COUNTRIESa	6.2	890	NAc	NAc
WORLD TOTAL	15.3	21313	NAc	NAc

a Includes Europe, North America, Australia, New Zealand and Japan.
^b Not applicable because coverage of live births < 80%.
^c Not applicable because developed status.
^d Excludes Japan.
^e Excludes Australia and New Zealand.

Table 4. Summary estimates of impaired fetal growth in developing countries

Indicator	Source	Rate (%)	Total number newborns affected per year¹
IUGR-LBW (< 2500g; ³ 37 wks gestation)	Live births weighted average using LBW rates from WHO data bank (WHO, 1992) and regression model (Villar et al, 1994)	11.0 (1.9-20.9)²	13,699,000
LBW (< 2500g; all gestational ages)	Live births weighted average using LBW rates from WHO data bank	16.4 (5.8-28.3)	20,423,000
IUGR (< 10th percentile; all gestational ages)	From WHO Collaborative Study on Maternal Anthropometry and Pregnancy Outcomes (WHO, 1995b)	23.8 (9.4-54.2)	29,639,000

¹ Total live births for 1995 are based on the UN World Population Prospects (UN, 1995).
² Range.

The risk of being born IUGR-LBW is highest in Asia (mainly South-central Asia), followed by Africa (Middle and Western Africa), Oceania (Melanesia), and the Latin American region. However, the number of total live births in each geographical region has the effect of making the geographical distribution even more unequal; nearly 75% of all affected newborns are born in Asia - mainly in South-central Asia-20% in Africa, and about 5% in Latin America. The developing countries of Oceania contribute very little to the absolute number of IUGR-LBW because there were only 187,000 live births reported in this region in 1995.

Major constraints to deriving the above estimates included both the qualitative and quantitative limitations of the available data. Moreover, the assessment of the relative contribution of IUGR to total incidence of LBW is conservative given that we used a regression model that underestimates IUGR-LBW by an average of 1.5% (95% CI: - 2.5 to -0.4). These constraints notwithstanding, we nevertheless consider this to be a valid attempt to quantify the magnitude and geographical distribution of IUGR; not only does it provide an incentive for improving data quality, but it is also a suitable means for identifying those countries where population-wide interventions to prevent and control IUGR are urgently required.

In addition to improving the availability and quality of birth weight data, there is a compelling need for feasible measures to assess gestational age or fetal growth. The World Health Organization has recently recommended that countries implement simplified data collection systems for all deliveries and encourage the systematic collection of population-based data on birth-weight-for-gestational-age (WHO, 1995a). Nevertheless, this recommendation is unlikely to be followed by the majority of the developing countries in the near future given the difficulties inherent in obtaining valid assessments of gestational age. Therefore, at the present time, our estimates of IUGR-LBW represent a good public health approximation for descriptive and epidemiological purposes.

A prevalence of IUGR in excess of 20% has been recommended as the cut-off point for triggering public health action. In the absence of information on gestational age, a prevalence of > 15% of LBW may be used as a proxy cut-off (WHO, 1995a). As shown in Table 4, Figure 4 and Appendix I, many developing countries currently exceed these trigger levels for action and, thus, population-wide interventions are urgently needed in these settings. Unfortunately a systematic review of 126 randomized controlled trials (RCT) evaluating 36 interventions to prevent or treat impaired fetal growth has shown that most of them did not show any significant effect on short-term perinatal outcomes (Gülmezoglu et al, 1997). There were, nevertheless, a few interventions that are likely to be beneficial: smoking cessation, balanced protein/energy supplementation and antimalarial chemoprophylaxis in primi-gravidae. Other interventions such as zinc, folate and magnesium supplementation during gestation merit further research. Appropriate combinations of interventions should also be evaluated since it is more likely that a synergistic approach will reduce a multicausal outcome like IUGR.

In summary, the data presented confirm that intrauterine growth retardation is a major public health problem worldwide. Fetuses who suffer from growth retardation have higher perinatal morbidity and mortality (Williams et al, 1982; Balcazar and Haas, 1991; Villar et al, 1990), and are at an increased risk of sudden infant death syndrome (Øyen et al, 1995). During childhood they are more likely to have poor cognitive development (Paz et al, 1995; Low et al, 1992) and neurologic impairment (Parkinson et al, 1981; Taylor and Howie, 1989; Villar et al, 1984); in adulthood they are at increased risk of cardiovascular disease (Osmond et al, 1993), high blood pressure (Williams et al, 1992), obstructive lung disease (Barker, 1991), diabetes (Hales et al, 1991), high cholesterol concentrations (Barker et al, 1993) and renal damage (Hinchliffe et al, 1992). Moreover, IUGR contributes to closing the intergenerational cycle of poverty, disease and malnutrition. The implications of this vicious cycle are enormous both in terms of human and socioeconomic development of the affected populations. Country-wide interventions aimed at preventing fetal growth retardation are urgently needed. A good start in life will pay off, both in terms of human capital and economic development.

Acknowledgements - We are grateful to Mrs Elisabeth Åhman from the WHO Maternal Health and Safe Motherhood Programme for kindly providing us with the latest version of the WHO Database on Low Birth Weight.