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Am J Clin Nutr 2004;80:193– 8. Printed in USA. © 2004 American Society for Clinical Nutrition 193
194 CAULFIELD ET AL
TABLE 1
Prospective cohort studies with information on weight-for-age z score and survival or death by cause
mo mo
Sudan Fawzi et al (6) 6–72 6 365 985 1123 592
Senegal Garenne et al (7) 0–59 6 1663 2186 2035 1249
Guinea-Bissau Andersen (8) 0–59 6–12 1155 4366 7341 2731
Ghana WHO/CHD (9) 0–12 12 46 183 506 1410
Nepal West et al (10, 11) 0–72 12 1030 2082 2002 892
Bangladesh Arifeen et al (12) 0–11 3 79 250 475 478
Pakistan Khan et al (13), Jalil et al (14) 0–60 120 253 687 1241 1341
India WHO/CHD (9) 0–12 12 172 639 1259 1295
Indonesia Sutrisna et al (15) 0–60 18 207 240 797 4856
Philippines Ricci and Becker (16) 0–59 3 800 3144 4834 5115
Ҁ3.00 SDs, and 쏝Ҁ3.00 SDs were estimated. In a healthy pop- diarrhea and pneumonia; however, exposure to infectious dis-
ulation, we would expect only 13.6%, 2.1%, and 0.1% of children eases such as malaria and measles depends on the ecology of the
to be classified into each of these categories, respectively. study setting and health care utilization (ie, measles vaccination
TABLE 2
Relative risk (95% CI) of mortality overall and by cause associated with low weight-for-age estimated from weighted random effects regression analysis
Diarrhea 12.50 (7.19, 21.73) 5.39 (3.73, 7.79) 2.32 (1.93, 2.79) 1.0
Pneumonia 8.09 (4.36, 15.01) 4.03 (2.67, 6.08) 2.01 (1.63, 2.47) 1.0
Malaria 9.49 (3.25, 27.66) 4.48 (2.20, 9.15) 2.12 (1.48, 3.02) 1.0
Measles 5.22 (2.29, 11.88) 3.01 (1.74, 5.21) 1.73 (1.32, 2.28) 1.0
All causes 8.72 (5.55, 13.72) 4.24 (3.13, 5.53) 2.06 (1.77, 2.39) 1.0
1
Calculated at Ҁ3.5, Ҁ2.5, and Ҁ1.5 compared with 0.5 SD weight-for-age from weighted random effects models. A significant test for trend is evidenced
by a statistically significant (P 쏝 0.05) coefficient for weight-for-age in each model.
196 CAULFIELD ET AL
TABLE 3
Mean z score and percentage of children in each weight-for-age category in each World Health Organization (WHO) region1
Prevalence
WHO region2 Mean z score 쏝Ҁ3 SDs 쏜Ҁ3 to 쏝Ҁ2 SDs 쏜Ҁ2 to 쏝Ҁ1 SDs 쏜Ҁ1 SDs
%
Africa D Ҁ1.54 7.1 25.1 38.3 29.5
Africa E Ҁ1.5 6.8 24.2 38.3 30.7
The Americas A 0 0.1 2.1 13.6 84.2
The Americas B Ҁ0.35 0.5 4.5 20.8 74.2
The Americas D Ҁ0.84 1.6 10.8 31.3 56.3
Eastern Mediterranean B Ҁ0.6 0.8 7.3 26.3 65.6
Eastern Mediterranean D Ҁ1.33 4.7 20.4 37.8 37.1
Europe A 0 0.1 2.1 13.6 84.2
Europe B Ҁ0.57 0.7 6.9 25.7 66.7
Europe C Ҁ0.05 0.2 2.4 14.5 82.9
Southeast Asia B Ҁ1.35 5.0 20.8 37.9 36.3
Southeast Asia D Ҁ1.9 13.4 32.5 35.8 18.3
Western Pacific Region A Ҁ0.22 0.3 3.5 18.0 78.2
Western Pacific Region B Ҁ1.0 2.3 13.6 34.1 50.0
1
Expected percentages of children in each weight-for-age category in a healthy population are those reported here for The Americas A and Europe A.
2
the neonatal period relate more to events during pregnancy, birth, determined through verbal autopsy that uses standard protocols
and the transition to extrauterine life and less to the infectious (23). Several reasons exist why the results for measles and ma-
causes of death studied here. laria deaths should be interpreted with caution. First, a reduced
The studies included here used specific protocols to assess number of studies contributed to these analyses, 6 for measles
both anthropometric status and cause of death. With minimal and 3 for malaria. Second, past studies on the influence of low
training, weight measures are highly accurate and precise; there- weight-for-age on measles mortality yielded equivocal results (24 –
fore, errors in exposure assessment are unlikely to have affected 26). Third, attributing deaths to malaria is problematic, and, as in the
our results. However, it is also true that the estimates of the study in Guinea-Bissau, deaths as a result of malaria were not dis-
weight-for-age distribution for each WHO region were imputed tinguished from deaths as a result of other causes of fever unless
on the basis of the best available information to date; thus, dis- these illnesses had symptoms or signs consistent with other causes
crepancies with present extent of underweight are possible as such as diarrhea or pneumonia. The results for Guinea-Bissau are
new surveys become available. In most cases, cause of death was consistent with those from Senegal, and, although the results from
TABLE 4
Population attributable fraction (PAF) of deaths by cause and World Health Organization (WHO) region
%
Africa D 56.1 64.7 54.6 45.2 57.7
Africa E 55.1 61.7 53.6 44.2 56.7
The Americas A 0.00 0.00 0.00 0.00 0.00
The Americas B 13.2 16.1 12.6 9.3 13.8
The Americas D 32.4 38.1 31.2 24.3 33.7
Eastern Mediterranean B 22.6 27.1 21.7 16.5 23.7
Eastern Mediterranean D 49.7 56.3 48.2 39.2 51.3
Europe A 0.00 0.00 0.00 0.00 0.00
Europe B 21.3 25.5 20.4 15.5 22.3
Europe C 2.2 2.8 2.1 1.5 2.3
Southeast Asia B 50.4 57.1 49.0 39.9 52.0
Southeast Asia D 64.8 71.1 63.4 53.8 66.4
Western Pacific Region A 8.1 10.0 7.7 5.7 8.5
Western Pacific Region B 38.4 44.5 37.1 29.3 39.8
World 52.5 60.7 52.3 44.8 57.3
1
Regions for the Global Burden of Disease project. A indicates very low child mortality and very low adult mortality; B, low child mortality and low adult
mortality; C, low child mortality and high adult mortality; D, high child mortality and high adult mortality; E, high child mortality and very high adult mortality.
UNDERWEIGHT AND CAUSE-SPECIFIC MORTALITY 197
Ghana suggest a different pattern of relation between underweight result that a large proportion of child deaths as a result of malaria
and mortality risk, the number of deaths as a result of malaria is quite could be prevented by child nutrition interventions is notewor-
small (n ҃ 8). Further studies would need to be included to refine thy. With current programmatic efforts, rates of undernutrition
these estimates. among children are declining in most countries at 1% per year or
It is important to consider that low weight-for-age is com- less (36). We and others argue that this amount of progress is
monly associated with deficiencies of micronutrients (27). For unacceptable (37, 38). Strategies to more effectively reduce child
example, zinc deficiency contributes to poor growth in young undernutrition by using experiences gained from successful nu-
children (28). The association of low weight-for-age with these trition programmers (39) are urgently needed.
deficiencies could mean that some of the risk attributed to un-
We thank the researchers who provided us with original data anthropo-
derweight should be attributable to specific micronutrient defi- metric status and cause-specific mortality.
ciencies; however, these other deficiencies also occur in children LC, MdO, MB, and RB contributed to the conceptualization, data analysis,
who are not underweight. Moreover, zinc supplementation in and writing of the manuscript. None of the authors have any financial or
populations that have a moderately high prevalence of zinc de- personal interest in any company or organization sponsoring the research.
ficiency has had similar effects on reducing infectious disease
morbidity in children who were classified to be undernourished
or not (29), and vitamin A supplementation reduces mortality in REFERENCES
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