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Harvard Institute for International Development, Cambridge, MA, USA; 2Department of Epidemiology and Nutrition Harvard School of
Public Health, Boston, MA, USA; and 3Ministry of Health, Khartoum, Sudan
Objective: The aim of the study was to examine the relationships between nutritional status and diarrhoea and
respiratory infections.
Design: Prospective cohort study within the framework of a randomized double-blind placebo-controlled
intervention trial.
Setting: In rural communities in the Khartoum and Gezira regions, in Northern Sudan.
Subjects: 28,753 Sudanese pre-school children between 6 months and 6 y old.
Methods: Relative risks of subsequent diarrhoea and respiratory infections in relation to nutritional status
measured by anthropometry (Z-scores of height-for-age (H=A), weight-for-height (W=H), and weight-for-age
(W=A), which reect stunting, wasting and underweight, respectively) were estimated using odds ratios from
logistic regression adjusting for various covariates.
Results: H=A, W=H and W=A were signicantly and inversely associated with subsequent diarrhoea and febrile
diarrhoea (P for trend < 0.001) with risks being 2.00 times higher (95% condence interval, CI (1.64, 2.43))
among children with W=A Z-scores below 74 Z, and 1.75 times higher (95% CI (1.56, 1.96)) among those with
a W=A Z-score between 74 and 73 Z compared with children having a W=A Z-score 1. Age, gender, region
of residence and seasonality modied these associations. Also, febrile cough was inversely associated with W=A
and W=H (P < 0.03), with risks ranging from 1.41 times higher (95% CI (1.02, 1.97)) to 1.21 times higher (95%
CI (1.04, 1.41)) in the group of underweight children with W=A Z-scores below 74 and between 72 and 71 Z,
all compared with normally nourished children ( 71 Z).
Conclusions: The reduction of severe but also mild and moderate undernutrition is necessary through nutrition,
health and socio-economic improvement in order to prevent morbidity.
Sponsorship: This study was carried out under cooperative agreement no. DAN-00450G-SS-6067 of the Ofce
of Nutrition, US Agency for International Development, Washington DC, and the Harvard Institute for
International Development.
Descriptors: nutritional status; anthropometry; diarrhoea; respiratory infections; socio-economic factors
European Journal of Clinical Nutrition (2000) 54, 463472
Introduction
Diarrhoea and respiratory infections are leading causes of
child deaths, and the majority of these occur in developing
countries (Tulloch & Richards, 1993). Undernutrition is
known to adversely affect specic and non-specic defence
mechanisms resulting in increased susceptibility to infections. This, in turn, can cause further deterioration in
nutritional status through reduced food intake, malabsorption, mobilization of body stores, increased losses and other
systemic reactions that can affect linear and ponderal
growth (Scrimshaw, 1992). Scrimshaw (1992), Santos
(1994), and Rivera and Martorell (1988) have comprehensively reviewed evidence of the synergistic relationship
between undernutrition and infection. Community-based
studies investigating associations between nutritional
*Correspondence: WW Fawzi, Department of Nutrition, Harvard School
of Public Health, 665 Huntington Avenue, Boston, MA 02115, USA.
Guarantors: P Nestel, MG Herrera and WW Fawzi.
Contributors: JK contributed to the design of this analysis, prepared the
drafts of the paper and did the statistical analysis. P Nestel designed and
implemented the eld study, MH and with WF initiated the study, and
provided advice in data analysis and commented on the manuscript. A ElA contributed to the implementation of the study in the eld.
Received 27 September 1999; revised 19 December 1999; accepted
13 January 2000
status and morbidity from diarrhoea and respiratory infections have reported inconsistent results. A study from
Nigeria showed that moderate and severe undernutrition
were associated with both the incidence and duration of
diarrhoeal disease (Tomkins, 1981), while three other
studies observed positive associations between undernutrition and the incidence of diarrhoea only (Sepulveda et al,
1988; El-Samani et al, 1988; Lindtjrn et al, 1993). Yet
another three studies found positive associations between
severe and moderate undernutrition and the duration or
percentage of annual time with diarrhoeal illness, but not
the incidence of disease (Trowbridge et al, 1981; Black
et al, 1984; Bairagi et al, 1987). In two studies, no
associations were observed between nutritional status and
the incidence or duration of diarrhocal disease (Chen et al,
1981; Mathur et al, 1985).
Few community-based prospective studies have examined the relationship between nutritional status and acute
respiratory infections. Signicant positive associations
have been observed between stunting and wasting and the
incidence (Tupasi et al, 1988, 1990; Ballard et al, 1995;
Smith et al, 1991) or duration of respiratory infections
(James, 1972). Such associations were not found in a study
in Southern Ethiopia (Lindtjrn et al, 1993). Some of the
inconsistencies in the results may have been due to the
464
signicantly and inversely with breast-feeding, the availability of water in the house and household wealth. Gender
was only signicantly associated with W=A and W=H, and
maternal literacy signicantly and inversely with H=A and
W=A only. The prevalence of stunting and of wasting was
signicantly higher among children from poorer households, among those living in households that did not have
piped water, as well as among breast-fed children (Table 1).
Breast-feeding was protective against wasting and stunting
among the under 2-y-old children with 42% higher risk of
stunting (95% CI (33%, 51%) comparing non-breast-fed
children with those being breast-fed).
An inverse relationship between diarrhoea and febrile
diarrhoea and nutritional status was observed, and because
the associations went in a similar direction and were only
slightly more pronounced for febrile diarrhoea than for
diarrhoea alone, the two categories were collapsed into one,
namely diarrhocal disease. Results from the multivariate
logistic regression analyses for diarrhoeal disease in relation to nutritional status, after adjusting for covariates, are
presented in Table 2.
Very severely stunted children were 1.50 times (95% CI
(1.33, 1.69)) more likely to have had subsequent diarrhoeal
disease than children whose H=A Z-score was 71 Z or
above, after adjusting for age and gender (Table 2, I, model
a). The multivariate association after adjustments for socioeconomic variables, morbidity at the beginning of the
respective round, dietary variables and season was stronger
with 69% higher risk of subsequent disease (95% CI (49%,
92%), Table 2, I, model b). Including W=H as a continuous
variable in the models did not improve the predictive power
(Table 2, I, model c), although the association was statistically signicant (P < 0.001).
Mild and moderate and severe wasting increased the risk
of subsequent diarrhoeal disease by 9% (95% CI (2%,
17%)) and 34% (95% CI (21%, 48%), respectively), even
465
Table 1 Stunting and wasting by age, gender, socioeconomic variables and breast-feeding at baseline
Age (months)
6 11
12 23
24 35
36 47
48
Gender
Boys
Girls
Literacy
Yes
No
Water
Yes
No
Wealth
Well
Average
Poor
Very poor
Breast-feeding
Yes
No
No. of childrena
Stuntingb
1396
4367
4499
4409
8607
13.4
32.4
28.6
27.1
25.3
11624
11653
P-valueb
Wastingb
P-valueb
P < 0.01
1.0
6.02
7.08
7.26
6.02
7.17)
8.41)
8.58)
7.12)
6.8
10.4
5.8
4.4
5.8
P < 0.01
1.0
1.56
0.83
0.63
0.68
26.6
26.2
P 0.10
1.0
0.97 (0.92, 1.03)
7.0
6.1
P < 0.01
1.0
0.82 (0.76, 0.89)
11357
11207
23.0
28.7
P < 0.01
1.0
1.10 (1.03, 1.19)
5.1
0.7
P < 0.01
1.0
1.09 (0.99, 1.22)
10116
13161
23.3
29.2
P < 0.01
1.0
1.19 (1.11, 1.27)
5.3
7.6
P < 0.01
1.0
1.22 (1.11, 1.35)
2322
11556
7241
2142
19.9
24.2
29.9
33.0
P < 0.01
1.0
1.28 (1.16, 1.41)
1.64 (1.47, 1.83)
1.81 (1.57, 2.08)
3.2
6.2
7.6
10.0
P < 0.01
1.0
1.79 (1.50, 2.14)
1.91 (1.59, 2.31)
2.38 (1.93, 2.94)
4129
19149
31.2
25.2
P < 0.01
1.0
1.42 (1.33, 1.51)
9.0
6.1
P < 0.01
1.0
1.31 (1.16, 1.48)
(5.09,
(5.96,
(6.14,
(5.09,
(1.31,
(0.68,
(0.52,
(0.56,
1.85)
1.01)
0.78)
0.83)
466
Very severe
<74 Z
433
7.5
Severe
74 to 73 Z
681
6.4
Moderate
73 to 72 Z
Mild
72 to 71 Z
1 Z
1239
6.0
1329
5.2
1047
4.5
1.0
1.0
1.0
566
7.2
1878
5.5
2211
8.9
1.0
1.0
1.0
1614
5.8
1536
4.9
733
4.4
1.0
1.0
Trend b
P < 0.001
20
10.4
54
8.6
P < 0.001
153
10.1
698
8.1
P < 0.001
Multivariate models included nutritional status: height-for-age (H=A), weight-for-height (W=H) and weight-for-age (W=H) respectively (four indicator
variables, reference: Z-score of 71 Z or above), age (0 11, 12 23, 24 35, 36 47 and 48 months), gender, and variables assessing socioeconomic
status (SES), that is piped water in the house, latrine in the house, maternal literacy (all yes=no), household wealth (ordinal with four levels) as well as
region of residence (four indicator variables) and variables accounting for vitamin A intake: capsule (vitamin A=placebo), dietary vitamin A intake (ordinal
in quintiles) as well as morbidity in the previous round (three indicator variables), season (ve indicator variables) and H=A and W=H Z-score (continuous)
as further specied in the text.
b
P-values of tests for trend from logistic regression models adjusting for the specied covariates and using nutritional status as continuous variable.
467
Table 3 Modication of the relationship between diarrhoeal disease and weight for age (W=A)
Characteristic
Age (months)
48
36 47
24 35
12 23
0 11
Gender
Boys
Girls
Breast-feedingd
Yes
No
Region
1, Abu Dileig
2, Ri Genoub
3, El Jaeli
4, Ri Shamal
5, Gezira
Season
January February
March April
May June
July August
September October
November December
Stratum-specic
Risk of diarrhoeal disease within subgroups of characteristicsc
Morbidity rates risk of morbidity among
Interaction, w2(d.f.),
among all childrena children > 2 SDb
< 73 Z
73 to 72 Z
> 72 Z
P-valuee
41.0
9.7
15.8
24.6
40.6
1.00
1.78
2.77
4.46
6.38
1.30)
1.31)
1.30)
1.46)
1.29)
1.00
1.00
1.00
1.00
1.00
10.6
10.8
1.00
1.00
4.4
3.9
1.00
1.00
11.5
7.6
7.2
7.9
16.5
1.00
0.67
1.02
0.71
1.30
(0.54,
(0.83,
(0.55,
(1.09,
0.84)
1.26)
0.91)
1.57)
1.49
1.70
1.64
1.16
1.75
(1.19,
(1.39,
(1.26,
(0.89,
(1.53,
1.87)
2.08)
2.12)
1.53)
2.01)
1.26
0.96
1.12
1.19
1.24
(1.02,
(0.78,
(0.89,
(0.95,
(1.12,
1.56)
1.19)
1.41)
1.49)
1.38)
1.00
1.00
1.00
1.00
1.00
16.7
16.9
12.5
8.1
6.3
9.7
1.00
1.16
0.60
0.44
0.46
0.57
(1.00,
(0.51,
(0.38,
(0.38,
(0.49,
1.35)
0.71)
0.52)
0.56)
0.67)
1.37
1.78
1.76
1.77
1.49
1.69
(1.10,
(1.38,
(1.47,
(1.40,
(1.18,
(1.01,
1.70)
2.29)
2.12)
2.24)
1.89)
2.00)
1.33
1.23
1.35
1.17
0.92
1.02
(1.13,
(1.01,
(1.14,
(0.93,
(0.71,
(0.85,
1.56)
1.48)
1.58)
1.46)
1.86)
1.23)
1.00
1.00
1.00
1.00
1.00
1.00
(1.54,
(2.43,
(3.89,
(5.12,
2.05)
3.16)
5.12)
7.95)
1.59
1.85
1.58
1.49
1.93
(1.26,
(1.50,
(1.35,
(1.25,
(1.17,
1.98)
2.28)
1.85)
1.76)
3.19)
1.10
1.08
1.20
1.28
1.17
(0.93,
(0.89,
(0.96,
(1.12,
(1.10,
468
Very severe
< 74 Z
Severe
74 to 73 Z
Moderate
73 to 72 Z
Mild
72 to 71 Z
71 Z
118
3.9
202
3.7
418
3.9
468
3.6
360
3.1
1.0
1.0
1.0
9
8.4
19
5.7
183
4.5
648
3.7
725
3.3
1.0
1.0
1.0
48
6.1
206
4.6
537
3.8
558
3.5
235
2.8
1.0
1.0
Trend b
P 0.105
P 0.029
P 0.025
Multivariate models included nutritional status: height-for-age (H=A), weight-for-height (W=H) and weight-for-age (W=A) respectively (four indicator
variables, reference: Z-score of 71 or above), age (0 11, 12 23, 24 35, 36 47 and 48 months), sex and successively variables assessing
socioeconomic status (SES) that is, water piped water in the house, latrine in the house, maternal literacy (all yes=no), household wealth (ordinal with four
levels), region of residence (four indicator variables) and variables accounting for vitamin A intake: periodic large dose supplementation during the study
(vitamin A=placebo) and dietary vitamin A intake (ordinal in quintiles), as well as morbidity in the previous round (three indicator variables), season (ve
indicator variables) and H=A and W=H Z-score (continuous), as further specied in the text.
b
P-values of test for trend from logistic regression models adjusting for the specied covariates and using nutritional status as continuous variable.
Discussion
Signicant and positive associations were observed
between H=A, W=H and W=A and diarrhoeal disease and
febrile cough. In view of the large study population,
reected in narrow condence intervals, chance is an
unlikely explanation of the results. This study, however,
has some limitations. Despite standardized procedures and
the well-trained staff, measurement and recording errors
could have resulted in misclassication of nutritional status
that would have affected the strengths of associations, but
this was most likely of a non-differential nature with
respect to the outcome.
Misclassication of diarrhoea, cough and fever was
possible because these symptoms are susceptible to misinterpretation. Random misclassication of a binary outcome in effect does not affect the risk estimate in a
prospective study but precision decreases with non-differential under-reporting of cases (Rothman, 1986). Underreporting of illness-related events increases with time after
469
Table 5 Modication of the relationship between cough with fever and weight for age (W=A)
Characteristic
Age (months)
48
36 47
24 35
12 23
0 12
Gender
Boys
Girls
Breast-feedingd
Yes
No
Region
1, Abu Dileig
2, Ri Genoub
3, El Jaeli
4, Ri Shamal
5, Gezira
Season
January February
March April
May June
July August
September October
November December
Morbidity rates
among all childrena
2.9
3.6
4.0
5.2
5.3
1.28
1.38
1.53
1.25
1.0
(1.05,
(1.13,
(1.20,
(0.79,
1.56)
1.42)
1.72)
1.17)
3.32)
1.0
1.0
1.0
1.0
1.0
3.7
3.5
1.0
1.0
6.2
4.4
1.0
1.0
3.3
4.3
2.3
3.8
3.7
1.47
0.92
1.15
1.34
1.0
(1.04,
(0.65,
(0.78,
(1.00,
2.08)
1.30)
1.70)
1.81)
1.17
1.33
1.27
1.31
1.05
(0.79,
(1.01,
(0.77,
(0.92,
(0.79,
1.73)
1.75)
2.11)
1.86)
1.40)
1.23
1.36
0.99
1.13
1.15
(0.87,
(1.05,
(0.65,
(0.83,
(0.95,
1.74)
1.76)
1.53)
1.53)
1.40)
1.0
1.0
1.0
1.0
1.0
2.7
2.9
3.1
4.7
4.8
3.2
1.45
1.73
1.71
2.27
1.52
1.0
(1.07,
(1.30,
(1.32,
(1.72,
(1.15,
1.97)
2.31)
2.20)
2.98)
2.00)
0.95
0.90
0.98
1.47
1.25
1.42
(0.57,
(0.49,
(0.68,
(1.08,
(0.94,
(0.98,
1.61)
1.65)
1.42)
2.00)
1.66)
2.05)
0.95
1.04
0.94
1.59
1.19
1.39
(0.65,
(0.70,
(0.69,
(1.21,
(0.92,
(1.04,
1.37)
1.53)
1.26)
2.10)
1.54)
1.86)
1.0
1.0
1.0
1.0
1.0
1.0
1.56)
1.69)
1.94)
1.98)
1.55
1.17
0.95
1.20
0.65
(1.18,
(0.83,
(0.69,
(0.88,
(0.14,
2.03)
1.66)
1.29)
1.62)
2.90)
1.27
1.07
1.33
0.89
1.78
(1.04,
(0.80,
(1.03,
(0.68,
(0.95,
(Pelletier, et al, 1994); thus, this study may have underestimated true associations.
Child age and gender, socio-economic status, season and
breast-feeding are important confounders of the nutritional
status-mortality relationship (Pelletier, et al, 1994).
El-Samani et al (1988) noted higher incidence rates of
diarrhoea among children who had diarrhoea in the previous child-period, which needs to be taken into account
when looking at the underweight-diarrhoea relationship.
Chowdhury et al (1990) found increased risks of diarrhoea
among moderately and severely stunted and wasted children without diarrhoea in the previous follow-up interval.
In this study diarrhoeal disease was signicantly associated
with previous diarrhoea but not with respiratory symptoms
and neither limiting the analysis to children free of symptoms at baseline nor adjusting for the previous presence of
the specied morbidity changed the risk estimates of the
undernutrition-morbidity relationship markedly.
In this study we adjusted for important confounders like
age, maternal literacy, household wealth, the availability of
piped water and a latrine in the house, region of residence,
periodic vitamin A supplementation during the study,
feeding practice, dietary vitamin A intake, season and
W=H or H=A in the models estimating associations
between morbidity and stunting or wasting, respectively.
Maternal nutrition status and birth weight were not considered potential confounders in this study because their
effects are greatest in the rst 6 months and these data were
not available. Moreover all children enrolled in this study
were older than 6 months. Beyond 6 months of age, linear
and ponderal growth are largely determined by feeding
European Journal of Clinical Nutrition
470
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