Animal Source Foods to Improve Micronutrient Nutrition
and Human Function in Developing Countries
The Effect of Micronutrient Deﬁciencies on Child Growth: A Review ofResults from Community-Based Supplementation Trials1
Juan A. Rivera,2 Christine Hotz, Teresa Gonza´lez-Cossı´o, Lynnette Neufeld andArmando Garcı´a-Guerra
Centro de Investigacio´n en Nutricio´n y Salud, Instituto Nacional de Salud Pu´blica, Cuernavaca, Morelos, Me´xico
Several micronutrients are required for adequate growth among children. However, it has been unclear
as to which nutrient deﬁciencies contribute most often to growth faltering in populations at risk for poor nutrition andpoor growth. Therefore, evidence from community-based, randomized, placebo-controlled, micronutrient supple-mentation trials was reviewed to determine which micronutrient deﬁciencies have been found to be causal to growthfaltering. Although correction of growth-limiting nutrient deﬁciencies may be achieved through provision ofpharmacological nutrient supplements, it also was of interest to review evidence for the use of animal source food
supplements to improved growth among children in at-risk populations. There is strong evidence for the contributionof zinc deﬁciency to growth faltering among children; even mild to moderate zinc deﬁciency may affect growth.
Vitamin A and iron deﬁciencies also have been demonstrated to cause growth faltering, however only when thedeﬁciency state of these nutrients is severe. Several controlled, community-based intervention trials that haveincluded animal source foods, either together with additional micronutrient supplements or with other supplementalfood sources, have demonstrated positive growth responses among children. Three trials that used an animal source
food alone (skim milk powder) also resulted in a positive growth response. However, the geographic scope of thelatter three trials was limited, and it remains unclear to what extent supplemental animal source foods alone andwhich types of animal source foods can be used to improve growth among children in at-risk populations.
KEY WORDS: Micronutrients animal source foods growth supplements
Growth retardation is highly prevalent in developing
about half of the world’s population is at risk of inadequate
countries (1) and is associated with several adverse outcomes
throughout life (2). Inadequate intakes of dietary energy and
Attained height is the result of the interaction between
protein and frequent infections are well-known causes of
genetic endowment and both macro- and micronutrient
growth retardation (3–5). However, the role of specific mi-
availability during the growth period. Longitudinal growth
cronutrient deficiencies in the etiology of growth retardation
occurs through a process of cell proliferation, the addition of new
has gained attention more recently (6–8). Micronutrient de-
cells to the growth plate of the bone and hypertrophy, resulting
ficiencies are highly prevalent in low-income countries, and
in the expansion of the growth plate (11). Although the control
the most probable causes are low content in the diet and poor
of bone growth in its different phases is not entirely understood,
bioavailability. More than half of preschool children are
the key roles of growth hormone (GH)3 and insulin-like growth
anemic, and an estimated 75 million and 140 million preschool
factor I (IGF-I) have been identified. IGF-I receptors are found
children have clinical and subclinical vitamin A deficiencies,
predominantly in proliferating bone chondrocytes (11), and
respectively (9). Less information is available on the prevalence
IGF-I itself stimulates synthesis of collagen and proteoglycans.
of zinc deficiency, although it has been estimated recently that
These physiological functions explain the role of IGF-I in lineargrowth. Furthermore, GH itself and its effect on IGF-I synthesisexert a direct effect on growth.
1 Presented at the conference ‘‘Animal Source Foods and Nutrition in
Nutrition plays a key role in the control of linear growth
held in Washington, D.C. June 24–26, 2002. The
through a variety of mechanisms. Evidence from animal
conference was organized by the International Nutrition Program, UC Davis and
models indicates that energy and protein restriction reduces
was sponsored by Global Livestock-CRSP, UC Davis through USAID grant
IGF-I plasma concentration, which returns to normal after
number PCE-G-00-98-00036-00. The supplement publication was supported byFood and Agriculture Organization, Land O’Lakes Inc., Heifer International, PondDynamics and Aquaculture-CRSP. The proceedings of this conference arepublished as a supplement to The Journal of Nutrition. Guest editors for this
3 Abbreviations used: GH, growth hormone; IGF-I, insulin-like growth factor I;
supplement publication were Montague Demment and Lindsay Allen.
HAZ, height-for-age Z-score; WAZ, weight-for-age Z-score; WHZ, weight-for-
2 To whom correspondence should be addressed. E-mail: [email protected]
height Z-score; RDA, Recommended Daily Allowance.
0022-3166/03 $3.00 Ó
2003 American Society for Nutritional Sciences.
MICRONUTRIENTS, ANIMAL SOURCE FOODS AND GROWTH
replenishment. The impact of reduced protein intake appears
or weaned, or whose intake of complementary foods was low
to be larger than that observed with energy restriction (12).
(28). These cross-sectional studies suggest that relatively small
The association between nutritional status and the IGF-I
increases in the intake of animal source foods may reduce the
system also has been observed in humans: IGF-I is reduced
prevalence of growth stunting in populations at risk. However,
during acute protein deficiency (kwashiorkor) and protein-
as these cross-sectional studies cannot confirm a direct impact
energy malnutrition in children (12). Some micronutrients also
of animal source food intake on growth, it will be necessary to
affect the IGF-I system. For example, it is well documented that
consider results from experimental studies using animal source
zinc deficiency in rats causes not only growth retardation but
also a decrease in both IGF-I plasma concentration and GH
The objectives of this review are as follows: 1) to summarize
receptors, which return to normal after zinc repletion (13).
evidence in the literature regarding the effects of common
Additionally, through its influence on the GH/IGF-I system,
micronutrient deficiencies on child growth derived from
zinc deficiency has been observed to affect bone metabolism
community-based, randomized controlled supplementation
(14). The role of zinc in growth also may be explained in part
trials using either single or multiple micronutrients; and 2) to
through its participation in DNA synthesis (15).
summarize evidence of the effects of interventions that in-
Studies on rats also have shown similar decreases in plasma
cluded animal source foods in the prevention of growth re-
IGF-I concentrations with depletion of potassium, magnesium
tardation in community-based intervention trials.
or thiamine, which return to normal after repletion of thesenutrients (12). Copper also is involved in growth through itsrole in cross-linking collagen fibers, and manganese deficiency
is associated with skeletal abnormalities, including retardedgrowth, which may be mediated through defects in pro-
We conducted a literature review using the PubMed electronic
system. No language restriction was imposed on the search, and
teoglycan physiology in the growth plate (11). Vitamin D and
articles published after 1989 were identified. Relevant studies Downloaded from
calcium deficiencies also affect bone development, as ma-
published before 1989 were identified through bibliographies of the
nifested through the condition known as rickets (16).
obtained published articles. For the micronutrient studies, only
Vitamin A was first identified as the growth-promoting
randomized, placebo-controlled supplementation trials were included.
factor ‘‘A.’’ Studies in the 1920s–1930s demonstrated arrested
The food-based intervention trials had to have included a concurrently
growth, especially of weight in rats, after acute vitamin A
enrolled control group. Only studies conducted for a minimum of 8 wk
depletion (17–20). However, even today effects of vitamin A
were accepted, as we consider this the minimum necessary to observe jn.nutrition.org
on linear growth, bone formation and body composition in
an impact of supplementation on growth.
animals are less clear (21). Judisch et al. (22) found that anemicchildren were small for their age and that their growth ratesaccelerated when treated with iron. Since then, however,
evidence for the effect of iron deficiency on growth has been
Randomized trials of the effect of micronutrient
Deficiencies of some micronutrients, such as iron, magne-
sium and zinc, result in anorexia (15,23). Therefore, these
Single micronutrients. Community-based, randomized con-
nutrient deficiencies also may contribute to growth retarda-
trolled supplementation trials were identified for zinc, iron and
tion indirectly by reducing the intake of other growth-
vitamin A. The findings from these studies are described in de-
limiting factors, such as energy and protein. Also, several
tail below, and a summary of the results is presented in Table 1.
micronutrients, including zinc, iron and vitamin A, are
Zinc. A meta-analysis of the effects of zinc supplementation
associated with immune function and risk of morbidity, which
on the growth of prepubertal children was published recently
in turn affect growth (4). Therefore, micronutrient deficiencies
(8); therefore, the results of this analysis are summarized here.
may have an indirect effect on growth by increasing the
The studies in this analysis included the following: 1) ran-
prevalence or severity of morbidity and anorexia.
domized, placebo-controlled intervention trials in which the
Several approaches may be taken to improve the intake of
supplemented and controlled groups were enrolled con-
growth-limiting nutrients, including administration of micro-
currently; 2) children ,12 y of age or specifically stated to be
nutrient supplements, fortification of food with micronutrients
prepubertal throughout the period of intervention; 3) no pre-
or improved dietary intake. In populations where dietary quality
mature infants; 4) subjects free of chronic diseases (e.g.,
is poor, it is likely that several micronutrient deficiencies co-
marasmus and cystic fibrosis); 5) zinc as the only component of
occur (24–26), in which case growth may be affected by more
the supplement that differed between treatment groups;
than one growth-limiting nutrient. Therefore, interventions
6) supplementation that was provided for at least 8 wk; and
designed to increase the intake of several common growth-
7) information on the body weight and/or height that was
limiting nutrients may be more effective in preventing growth
collected during the period of supplementation and reported in
retardation than those that increase the intake of only one
sufficient detail. A total of 33 studies were considered to be
problem nutrient. In general, animal source foods contain
acceptable, where 13 of the studies were conducted in Latin
higher concentrations of several micronutrients that may be
America/Caribbean, 8 in Asia, 8 in North America/Europe and
limiting to growth (e.g., calcium, zinc, iron and certain amino
4 in Africa. There were positive effect sizes for 25 out of 33
acids), and micronutrients in animal source foods also tend to
studies that measured height and 25 out of 32 studies that
be more readily available than micronutrients from plant foods.
measured body weight. The overall effect size (expressed in
Indeed, results from observational studies conducted in Mexico
standard deviation units) in height was 0.350 (CI ¼ 0.189,
and Peru have suggested that intake of animal source foods is
0.511; p , 0.0001) and weight was 0.309 (CI ¼ 0.178, 0.439;
associated positively with growth. In Mexico, a higher con-
p , 0.0001). The growth responses were greater in children
sumption of animal products between 18 and 30 mo of age was
with low initial weight-for-age Z-scores and in those aged $6
associated with greater weight and length at 30 mo (27). In
mo with initial low height-for-age Z-scores.
Peru, intake of animal source foods was associated with greater
Results of one zinc supplementation trial conducted in West
growth among infants who were either breastfed less frequently
Java, Indonesia met the criteria described above and was
Randomized, placebo-controlled, single-micronutrient supplementation trials and effects on child growth
WAZ, and children $ 6 mo of age with , ÿ2 HAZ
No difference in HAZ, WAZ, WHZ, prevalence
Effect size for HAZ not signiﬁcant (p = 0.09)
No difference in plasma IGF-I concentration
Signiﬁcantly greater rate of weight gain
showing greatest increase in hemoglobin(p 0.05)
Weight, height and arm circumference increased
signiﬁcantly in the anemic group after iron
Morbidity scores signiﬁcantly lower in anemicchildren after iron treatment
No growth effect among nonanemic children
Change in height and HAZ signiﬁcantly greater
Change in WHZ signiﬁcantly greater incontrol group
WAZ were signiﬁcantly greater after iron
(severe anemiaand heavy hookwormexcluded)
Total food (g) and energy intake signiﬁcantlyincreased after iron treatment—anorexia mayhave partly caused poor growth in untreatedchildren
Changes in weight, weight-for-height, arm
circumference and skinfolds were signiﬁcantly
indicators did not improve signiﬁcantly afteriron treatment
Multiple-micronutrient deﬁciencies were noted inthe children (see Rivera et al., 2001)
No signiﬁcant differences in changes in weight,
height or arm circumference observed after irontreatment, nor among those initially stuntedor anemic
Hemoglobin increased signiﬁcantly afteriron treatment
Parallel study with albendazole treatment also didnot improve growth
No difference in HAZ, WAZ, WHZ or knee-heel
The rate of weight gain was signiﬁcantly greater
No signiﬁcant differences in length gain or armcircumference
No signiﬁcant differences in weight or height
Vitamin A, 10 mg ofcholecalciferol and50 mg of Vitamin C)
Signiﬁcant decline in hemoglobin observedin controls but not in those treated with iron
Vitamin A supplementation unlikely to improve
the growth of young children who have only mild
Signiﬁcant height and weight increases observed
only in nonbreastfed children and those with low
Signiﬁcantly greater weight observed only in girls
Linear growth increased signiﬁcantly among
children of low socioeconomic status or with HIV
Risk of stunting was signiﬁcantly reduced amongchildren with poor water supply, those who wereexclusively breastfed 4–6 mo and those who hadpersistent diarrhea
Signiﬁcantly greater increases in weight and arm
circumference increments in children with initially
1 Initial status refers to nutritional status (biochemical or anthropometric) or physiological status (presence of infections) of the subjects at baseline, where this information was provided or relevant.
Where no information is provided, this indicates that subjects were not selected on the basis of their initial status.
published after the meta-analysis was completed (29). No
one analyzed the subgroup of anemic infants separately. The
differences were found among the groups in height-for-age,
three that selected only anemic subjects all demonstrated
weight-for-age or weight-for-height Z-scores (HAZ, WAZ and
positive effects on growth. Two of five studies that did not
WHZ, respectively) and in plasma IGF-I concentrations in
select for iron status but noted a high (>50%) prevalence of
a subsample. The effect size for length was estimated by us to be
anemia showed a growth response after iron supplementation.
0.09 and was not significant. The authors concluded that there
On the other hand, none of the four trials that selected only
must have been additional underlying factors, including other
nonanemic children showed an effect on growth. We con-
nutritional deficiencies, that impaired the growth of these
cluded that there is substantial evidence indicating that iron
children. Nonetheless, the general conclusions of the meta-
supplementation of anemic infants or young children has effects
analysis remain valid, as the authors indicated that .500
on growth. Although the mechanisms by which anemia causes
studies with no effect of zinc supplementation on growth would
growth retardation are not clear, it may result from reduced oxi-
be required to invalidate their findings (8).
dation reactions that occur when the functional iron compar-
Iron. Twelve iron supplementation trials were identified,
tment is depleted, from increased morbidity or from decreased
which provided sufficient information to determine whether
appetite. Discrepancies in results in some of the trials cond-
there was a statistically significant difference in growth response.
ucted in communities with a high prevalence of anemia may be
These studies included children between 2 mo and 13.5 y of age,
due to the presence of concurrent deficiencies of other growth-
receiving 10–80 mg of iron/d for at least 2 mo and up to 1 y.
limiting nutrients. Available evidence suggests that iron suppl-
These studies were conducted in Asia (n ¼ 5), Africa (n ¼ 4)
ementation has no effect on the growth of nonanemic children.
and Latin America (n ¼ 2). Three of these studies selected
Vitamin A. Ramakrishnan and Martorell (39) conducted
children who were anemic (30–32). All three studies showed
a literature review of vitamin A supplementation trials that
that provision of iron supplements to the anemic infants or
measured impact on growth. They reported on nine random-
young children resulted in improved growth. The two studies
ized, double-blind trials (40–48), seven of which were placebo-
that measured length or height demonstrated greater linear
controlled. The trials were conducted in India (n¼3),
growth (31,32), whereas the third study that did not measure
Indonesia (n¼2), China, Tanzania, Ghana and Nepal. Seven
length showed significantly greater weight gain (30). It also was
of the trials provided high vitamin A doses every 4 or 6 mo, and
noted in the Indonesian study (31) that a decrease in morbidity
two of them provided daily amounts that were close to the
was observed among the anemic children who received iron.
recommended daily allowance (RDA). All trials were con-
Four studies enrolled children from communities that were
ducted among children ,3 y of age in populations with
not selected based on their iron status, but baseline mea-
evidence of vitamin A deficiency and high risk of growth
surements indicated that at least 50% of the children were
retardation. The follow-up period (;1 y) would have been
anemic (23,33,34,35). One group of Kenyan schoolchildren
sufficient to find impacts on growth. Most of these trials found
demonstrated significant gains in height and weight, as well as
that vitamin A reduced mortality; however, eight of the nine
increased food intake, after 14 wk of treatment with iron (23).
studies did not find any effects on length or weight. The two
Another study, also conducted among Kenyan schoolchildren,
studies that reported effects on growth, one in length (40) and
resulted in increased weight, weight-for-height, arm circum-
one in weight (46), were the only ones that did not have
ference and skinfolds, but no increase in height was
observed after 7 mo of intermittent iron supplementation
Since the publication of the review, results of four additional
(33). A study conducted in Benin among preschool children
vitamin A supplementation trials meeting the requirements for
showed no change in height or weight, although hemoglobin
inclusion in this review were published from Indonesia (49),
concentration was noted to increase significantly after treat-
Sudan (50), Tanzania (51) and Zaire (52). These studies were
ment (35). Treatment for intestinal helminthes with alben-
community-based, high-dose vitamin A supplementation trials
dazole also had no effect on growth in the latter study;
that followed children under 6 y of age for 1–2 y. Two of these
therefore, it is possible that some other growth-limiting
studies examined the effects of supplementation on growth
nutrient was severely deficient in this group. Rosado et al.
according to initial serum retinol concentrations in the children
(34) also reported no effect of iron treatment on growth
(49,52). Children with severe vitamin A deficiency (serum
among preschoolers in Mexico. However, it was noted that
retinol ,0.35 mmol/L) demonstrated improved growth among
several multiple-micronutrient deficiencies were present,
those who received the vitamin A supplement compared to
including zinc, vitamin A and vitamin B-12. One further
control children with severe vitamin A deficiency. The third
study conducted in Indonesia did not measure baseline
study (50) observed the impact of vitamin A supplementation
prevalence of anemia, but after 6 mo of iron treatment, 66%
on weight gain only in girls 1–3 y of age but not in the other age
of infants in the placebo group were anemic compared to 28%
groups (6 mo–1 y and 3–6 y) or in boys, but results were not
in the group that received iron (29). No effect on growth
analyzed according to baseline serum retinol concentrations.
was observed in the iron-supplemented group nor were any
The study conducted in Tanzania (51) was the only study
differences in IGF-1 concentrations found. Zinc supplemen-
prospectively designed to evaluate factors that modify the effect
tation in the same study also did not improve growth. The
of vitamin A supplementation on growth. Children hospitalized
authors concluded that there must have been other underlying
with pneumonia were admitted to the study and received either
growth-limiting deficiencies present.
repeated high-dose vitamin A treatment over 8 mo or a placebo.
There also were four iron supplementation trials that
No overall effect of the treatment was observed in these
selected only children who were nonanemic (31,36–38).
children. However, treatment had a significant positive effect
None of these studies demonstrated an effect of iron on
on the linear growth in subgroups of children of low socio-
growth. In fact, the study conducted in Indonesia demonstrated
economic status and in children with HIV infection. Among
a significantly lower rate of weight gain among children who
those who received vitamin A treatment, risk of stunting after
received iron compared to controls (36).
1 y was significantly lower among children with poor water sup-
In summary, 11 trials that reported information necessary to
ply, and in those who were exclusively breastfed for 4–6 mo
judge the effect of iron supplementation on growth were
(but not ,4 mo). Finally, treatment attenuated the negative ef-
reviewed. Four selected anemic infants or young children and
fect of persistent diarrhea on stunting.
MICRONUTRIENTS, ANIMAL SOURCE FOODS AND GROWTH
Based on these clinical trials, we conclude that vitamin A
receive either the fortified or the nonfortified beverage, where
supplementation is unlikely to improve the growth of young
seven servings (100 kcal) of the beverage were provided 5 d/wk.
children who are only mildly to moderately vitamin A deficient.
The fortified beverage contained varying proportions of RDA
On the other hand, severe vitamin A deficiency does appear to
for four minerals and eight vitamins. This treatment was
cause growth retardation, which may be alleviated after vitamin
provided for 8 wk, and change in weight, but not height, was
A supplementation. Effects of vitamin A deficiency on growth
included as a growth outcome. The children receiving the
may be mediated through morbidity, as suggested by the results
fortified beverage gained significantly more weight than those
of the study in Tanzania, where stunting vitamin A deficiency
receiving the unfortified beverage. The trial conducted in
appeared to contribute to stunting among children with serious
Tanzania reported various outcomes of a similarly designed trial
infections such as HIV or persistent diarrhea. The interaction
in a series of abstracts (56,57,58). The fortified or nonfortified
of breastfeeding with the effect of supplemental vitamin A on
beverages contained 30–120% of the RDA for three minerals
growth is equivocal. The results from Tanzania suggest that
and seven vitamins and were provided on school days for
additional vitamin A enhanced the protective effects of
a period of 6 mo. High prevalences of anemia and severe
breastfeeding against stunting, whereas the Indonesian study
vitamin A deficiency were reported at baseline in this pop-
suggested that nonbreastfed children benefited more from
ulation (56). Children who received the fortified beverage had
supplemental vitamin A in terms of growth.
significantly greater weight and height increments over the
Other single micronutrients. We did not find randomized
study period (58) and a reduced risk of stunting (57) compared
supplementation trials with other micronutrients. There is
to children who received the nonfortified beverage.
a theoretical basis to consider potassium, manganese, thiamin
Another study worth noting is one conducted among low-
and copper as other micronutrients besides zinc, vitamin A and
income, Chinese schoolchildren aged 6–9 y (59), which looked
iron as being growth-limiting nutrients in populations. However
at the effects of daily supplementation with zinc (20 mg) versus
it is possible that these nutrients are more often consumed in
multiple micronutrients (half of the RDA for seven minerals Downloaded from
adequate quantities and/or that there is a lack of information
and 10 vitamins and one-quarter of the RDA for folate) with
available on the occurrence of these deficiencies in populations.
and without zinc for 10 wk. A placebo group was not included,
Multiple micronutrients. To date, limited information is
iron was not included in the multiple-micronutrient treatment
available on the effects of multiple-micronutrient supplemen-
and only knee height was reported as a growth outcome. The
tation on growth. For the purpose of this review, multiple-
differences in knee height among groups were reported to be
micronutrient supplements were considered to be those that
statistically significant (p , 0.01), and the largest growth incre- jn.nutrition.org
contained at least iron, zinc and a form of vitamin A. Five
ments occurred in the zinc 1 micronutrients groups, followed
placebo-controlled trials of supplementation with multiple
by the group of micronutrients alone and finally, the group of
micronutrients were identified and are summarized in Table
zinc alone. These results suggest that micronutrients other than
2. Two of these studies were published in peer-reviewed
zinc were limiting bone growth in the study population.
journals, two were published abstracts and another was
In summary, of the five trials examined, four demonstrated
submitted recently to a journal for peer review. The studies
a positive growth response to multiple-micronutrient supple-
were conducted in Botswana, Tanzania, Guatemala, Mexico
mentation. The positive growth response found in the two
and Vietnam. The studies in Botswana and Tanzania were
studies conducted among infants and preschool children was
conducted among schoolchildren, whereas the others included
significant only among certain subgroups of children (i.e. those
infants and preschoolers aged between 6 and 30 mo.
under 12 mo of age in Mexico and those initially stunted in
The three studies conducted among infants and preschool
Vietnam). The effect size for change in linear growth in the
children varied somewhat in design. The study in Mexico (26)
subgroups for which positive responses were found in these
supplemented 8- to 14-mo-old children daily for 1 y with a fla-
studies (Mexico, 0.29; Vietnam, daily 0.48, weekly 0.37) was
vored beverage containing 1–1.5 times the RDA of six minerals
in the range of that found in the meta-analysis of zinc
and 13 vitamins. This population of children was reported to
supplementation for initially stunted children. The abstract
have multiple-micronutrient deficiencies. Supplemented in-
reported from Guatemala did not report specifically on effects
fants initially aged ,12 mo had significantly greater length gains
among possible vulnerable subgroups of children, but suggested
than the placebo group, with a difference of 0.29 length-for-age
that these factors were controlled for in the analysis.
Z-score at the end of supplementation, whereas no effects were
It is not possible to determine which micronutrients in these
observed in children aged $ 12 mo at baseline. The study in
studies were limiting to growth, and clearly, this would depend
Vietnam (53) supplemented children 6–24 mo of age for 3 mo
on the existence and severity of various micronutrient de-
with either of the following: 1) daily supplements with 8 mg of
ficiencies. Based on the results of the meta-analysis of zinc
iron, 5 mg of zinc, 333 mg of retinol and 20 mg of vitamin C,
supplementation on growth, it is clear that zinc is a common
5 d/wk; 2) weekly supplements with 20 mg of iron, 17 mg of zinc,
growth-limiting nutrient. The conclusions of the single-
1700 mg of retinol and 20 mg of vitamin C; or 3) a placebo.
micronutrient trials confirm that zinc deficiency and severe
Positive impacts on HAZ were documented both in the daily
iron and vitamin A deficiencies are causal to growth retarda-
(10.48, p , 0.001) and weekly (10.37, p , 0.001) groups, but
tion. However, the study conducted among schoolchildren in
only in infants who were stunted at baseline. Limited infor-
China (59) and others (60) suggest that zinc alone was not the
mation is as yet available for the study conducted in Guatemala
primary growth-limiting nutrient. It is possible that micro-
(54). The supplements provided either whey protein concen-
nutrient deficiencies other than zinc, iron and vitamin A also
trate or bovine serum concentrate, both with or without
cause growth faltering as the latter studies did not select for
multiple micronutrients (composition not reported), for ;7 mo.
anemia or severe vitamin A deficiency.
There were no differences in length or weight between the pro-
Supplementation and/or nutrition education trials
tein-supplemented groups and the groups containing micronu-
including foods of animal origin and their influence
The two African trials provided schoolchildren with
beverages with or without multiple-micronutrient mixtures.
Perhaps the main question to be asked by the review in this
In the study in Botswana (55), schools were randomized to
section is whether animal source foods can be used to provide
Randomized, placebo-controlled, single-micronutrient supplementation trials and effects on child growth
Weight and weight-for-age Z-scores increased
signiﬁcantly after supplementation with the multiple
micronutrient–containing beverage (effect size forweight-for-age Z-score = 0.36)
Mean change in weight was 0.8 kg greater (p , 0.001)
and mean change in height was 0.7 cm greater
(p , 0.001) in the group that received micronutrients
Stunting was signiﬁcantly reduced (odds ratio 0.52)
No difference among groups in changes in length,
Impact of supplementation on length-for-age in infants
,12 mo of age at recruitment (effect size = 0.30;p , 0.05)
Effect size on children $12 mo of age: 0.10 (N.S.)
No signiﬁcant differences in growth among groups
Among those stunted at baseline, HAZ increased
signiﬁcantly after daily (effect size 0.48) and
MICRONUTRIENTS, ANIMAL SOURCE FOODS AND GROWTH
additional micronutrients sufficient to prevent or limit growth
Breastfed infants received one of the following porridges:
faltering in children living in high-risk environments. Very few
a cereal-legume blend (Weanimix), Weanimix 1 vitamins and
studies have been designed to answer this question directly.
minerals, Weanimix 1 fish powder or koko (a traditionally used
Several studies have used interventions that included increased
fermented maize porridge) 1 fish powder. No differences were
intake of animal source foods. However, the intervention
observed in length or weight among the four intervention
designs varied greatly and most included components other
groups. However, LAZ and WAZ among all of the sup-
than provision of animal source foods, such as additional
plemented infants (pooled) were greater than among those in
micronutrients or nutrition education, to improve young child
the cross-sectional study group. It is possible that all of the
feeding practices. The studies included in this review are
supplemental food types tested were equally sufficient to in-
randomized intervention trials with a concurrently enrolled
crease the intake of growth-limiting nutrients. However, the
control group and they lasted at least 8 wk.
authors also suggested that the provision of the hygienically
Food supplements containing animal source foods plus
prepared supplemental foods in vacuum flasks may have
additional micronutrients. Two studies were identified that
reduced exposure to diarrheal pathogens and that more prompt
provided food supplements plus additional micronutrients
use of clinic facilities may have been encouraged indirectly due
in the intervention (2,61). One study was conducted in
to frequent morbidity monitoring during the intervention. It
Guatemala, where four villages received either a skim milk–
was not possible to assess the contribution of decreased
based, high-protein, high-energy supplement (atole) or a no-
morbidity rates to the apparently improved growth among the
protein, low-energy supplement (fresco), where both sup-
plements contained additional micronutrients (2,62). The
The three controlled trials described above produced posi-
supplements were distributed in a central location in each
tive effects on growth, and two of the studies (61,63) suggested
village and were available on demand to all members of the
that the growth impact was at least partially mediated through
community. Intake of the supplements was registered daily for
attenuation of the negative effects of diarrheal morbidity on Downloaded from
all children under 7 y of age. Supplementation with atole
growth. The main difference between these studies and those
resulted in 2.45 6 0.10 cm greater length at 3 y of age than in
that provided micronutrient supplements alone is that these
the group receiving fresco. In Colombia, women in their first
trials also included supplementary energy and protein, which
trimester of pregnancy living in an urban area were selected
also may be limiting to growth and may contribute to improved
from low income families in which 50% of the children under 5 y
catch-up during convalescence. As both food supplements and
of age in the family had a weight-for-age that was .85% of the
micronutrients were provided simultaneously in the interven- jn.nutrition.org
Colombian standards (61). Mothers were followed through
tion, it is not possible to ascertain whether the nutritious food
pregnancy and infants resulting from that pregnancy were
supplement alone could produce similar benefits without the
followed for 3 y. The families were randomly assigned to receive
provision of additional micronutrients.
either no supplement or food supplements consisting of dry
Nutrition education interventions that included increased
skim milk, enriched bread and vegetable oil, plus iron and
intake of animal source foods. Two studies conducted nutri-
vitamin A supplementation for the enrolled children. At 3 mo,
tion education interventions that included a component to
a difference in weight of 197 g in favor of the supplemented
increase the intake of animal source foods. A year-long in-
group and at 6 mo a difference in length of 0.9 cm were
tervention was conducted in China that assessed the impact
documented. By 36 mo, the supplemented group had a mean
of nutrition education and growth monitoring activities on
weight that was 476 g (p , 0.05) higher and a mean length that
growth among children from their first year of life (65). The
was 2.2 cm (p , 0.005) greater than the control group. Among
educational component included specific messages to encour-
unsupplemented children, diarrhea was significantly negatively
age exclusive breastfeeding for 4–6 mo, after which time, hard-
associated with length; however, supplementation completely
boiled egg yolk should be offered to the infant daily. It was
offset the negative effect of diarrheal disease on growth.
reported that more women in the intervention group could cite
Two other studies that provided food supplements con-
important foods to include in the complementary diet and
taining animal source foods plus additional micronutrients were
appropriate patterns of breastfeeding, and more children in the
identified. Although these did not meet the criteria for in-
intervention group received egg yolk daily. Infants in the
clusion in the review, their results are worth mentioning. A
intervention group had significantly better growth in weight
study conducted in a peri-urban area in Guinea-Bissau aimed
and length than the control group. (WAZ: ÿ1.17 vs. ÿ1.93,
to determine the effects of a dietary supplement (millet gruel
p ¼ 0.004; HAZ: ÿ1.32 vs. ÿ1.96, p ¼ 0.002). The increase
with egg, milk powder, banana, margarine and sugar) plus
in intake of egg yolk by young children may have contributed to
micronutrients given to children ,3 y of age with diarrhea
increased intake of growth-limiting nutrients in this population.
(n ¼ 120) versus the children’s typical diet. The supplement
However, it cannot be determined to what extent this, or the
was given during the diarrheal episode and for 1 wk during
other intervention activities, contributed to the greater growth
convalescence (63). Although the intervention was adminis-
tered for a median of only 17 d, the children’s growth response
An intervention conducted in India offered a milk- and
was monitored for a median of 6.6 mo. The treatment group
cereal-based supplement plus nutrition counseling, or visitation
had a weight gain exceeding that of the control group by 61.5 g/
only, for 8 mo among infants recruited at 4 mo of age (66).
wk during the intervention period and by 12.5 g/wk during
Children receiving the supplement had a weight increment
follow-up. Not surprisingly, there was no significant increase in
0.25 kg greater than that of the control group, but no change in
knee-heel height during the intervention period. However, it
length was observed. However, children in the intervention
was significantly greater in the treatment group (7.5 mm/y, p ,
group also had higher rates of diarrhea and were breastfed less
0.0001) after the follow-up. Another study was conducted
frequently than the control children. In this case, the increased
among Ghanaian infants to evaluate the effect of feeding
diarrheal infections may have been caused by use of con-
centrally produced infant cereals of varying nutritional
taminated water needed to dilute the food supplement and
composition on nutritional status (64). Unfortunately, it was
possibly by the displacement of breast milk. This study suggests
not possible to include a concurrently enrolled control group, so
that, in addition to providing increased nutritional intake,
a separate cross-sectional study was used as a comparison.
simultaneous interventions to improve water quality also may
be needed to achieve more effective prevention of morbidity
supplements, with or without additional micronutrients,
reported positive impacts on growth.
Interventions with animal source foods alone. Only four
studies were identified where a single food supplement was
provided to children in the form of milk powder or formulawithout additional micronutrients, three of which were
The essential role for several micronutrients in growth has
conducted in the same population group. Malcolm (67)
been demonstrated clearly by both animal- and clinical-based
reported results of two food-supplementation trials conducted
human trials of supplementation with single micronutrients.
among children in a boarding school in Bundi, New Guinea.
The three micronutrients with the strongest relationship to
The first study compared changes in height, weight and
growth, iron, zinc and vitamin A, are commonly deficient in
skinfold thickness between two classes of children receiving
low-income populations where dietary quality often is poor.
their regular diet of 3 meals daily of taro and sweet potato
The positive impact of community-based supplementation
(tubers) or a skim milk powder supplement providing 25 g of
trials reviewed in this article indeed confirms that iron, zinc and
protein daily for 5 mo. The schoolchildren receiving the
vitamin A are common growth-limiting nutrients. However,
supplement demonstrated significantly greater gains in height
iron and vitamin A appear to be limiting to growth only when
(12.42 cm) and weight (10.73 kg) compared to the control
deficiencies of these nutrients are severe, whereas growth may
class (11.18 cm, p , 0.001 and –0.13 kg, p , 0.01). The
be limited only by mild to moderate deficiency of zinc. This is
second study used a similar design to compare growth response
consistent with the known metabolic and physiologic activity of
of the schoolchildren to supplemental skim milk powder (270
these nutrients: zinc has direct effects on the primary hormonal
kcal/d), margarine (270 kcal/d) or two additional meals of taro
system (IGF-I/GH) that controls growth in the postnatal phase
and sweet potato daily, each provided 5 d/wk for 13 wks. The
when the majority of stunting occurs. On the other hand, iron
skim milk–supplemented group demonstrated the largest
and vitamin A do not appear to influence this system directly,
height and weight increases (12.32 cm, 11.21 kg) relative
but more likely exert their effects on growth when their
to the control group (11.10 cm, 10.50 kg). Only a small
functional stores have been depleted and/or when deficiencies
increase in weight (11.05 kg) occurred in the margarine-
of these nutrients result in increased morbidity, which in turn
supplemented group but skinfolds increased substantially in
contributes to growth faltering. Although single-micronutrient
this group compared to controls. The additional taro and
supplementation trials have been useful to confirm the effects
sweet potato resulted in a small increase in height (11.54 cm)
of specific micronutrients on growth outcomes, programs that
relative to controls. Because the children’s normal diet was
provide supplements of only one nutrient may not be the most
based almost exclusively on tubers with relatively low protein
cost-effective way of preventing growth faltering and associated
content, it was hypothesized that protein was limiting to the
adverse health outcomes because of the co-existence of
growth of these children. These results are consistent with
multiple-micronutrient deficiencies in many populations.
protein, or other growth-limiting nutrients in milk, being
Multiple-micronutrient supplements are expected to be
limiting to the accrual of lean tissues, whereas additional
more efficacious in preventing growth faltering in at-risk pop-
energy provided as fat apparently contributed to fat accumu-
ulations, as all possible growth-limiting micronutrient de-
lation. These results were corroborated by a later trial
ficiencies may be corrected simultaneously. Although the few
conducted in the same area where children receiving a skim
available multiple-micronutrient supplementation trials have
milk powder supplement also demonstrated improvements in
demonstrated positive effects on growth, in some cases these
indices of skeletal development (68). Walker et al. (69)
effects were limited to specific subgroups of the study popu-
conducted a randomized intervention trial in Jamaica where
lation. Also, the interaction of various micronutrients and the
a milk-based formula was provided for 1 y to children (9–24
potential negative effect of some minerals on the absorption of
mo) who were initially stunted, and their growth was
others (e.g., iron, zinc and copper, calcium) when combined in
compared to age- and sex-matched stunted controls who
a single supplement requires further assessment.
received no food supplement. Supplemented children gained
From a programmatic perspective, it may be more desirable
an additional 0.9 cm and 0.31 kg more than that of control
to consider intervention options other than supplement use.
children during the first 6 mo of the study, whereas no further
Food-based interventions may have several advantages, in-
benefit was observed in the latter half of the study. It was
cluding the provision of additional nutrients in a familiar form
noted that the gains in growth were greater among younger
that can be integrated with the usual diet and the provision of
children than they were among older children. Based on the
an additional source of energy and high-quality protein, which
results of these three trials, it appears that milk supplements
also have direct effects on the IGF-I/GH hormone system (70).
may provide a good source of nutrients that are limiting to
Animal source foods provide the richest and most bioavailable
growth in some settings, although the specific growth-limiting
sources of several micronutrients. Some of the food-based trials
have demonstrated that at least part of the positive effects of
It is difficult to summarize interventions studying the
the intervention on growth occurred by improving catch-up
efficacy of supplementary animal source foods on prevention
growth after diarrheal illness (61,63). Although it is conceiv-
of growth faltering because of the many different study
able that the additional micronutrients (provided by the
designs used and because most of the interventions included
pharmacological supplements or animal source food) supported
other components that may have contributed to the effects
catch-up growth during convalescence, the supplemental foods
observed. The only examples of animal source foods solely
also would have provided additional energy and protein, which
contributing to growth promotion are the trials that provided
may contribute to improved growth in the face of frequent
milk supplements alone: all four trials produced positive
effects on growth; however, it is not possible to determine
Unfortunately, very few studies have been reported that
what specific micro- or macronutrients contributed to the
confirm the evidence from cross-sectional studies suggesting
growth response. It also is unclear to what extent additional
that intake of animal source foods is associated with better
micronutrients would have provided further benefits to
growth in children. Several intervention studies have included
growth. In any case, all of the trials that included food
both food supplements and additional multiple micronutrients,
MICRONUTRIENTS, ANIMAL SOURCE FOODS AND GROWTH
but it remains uncertain as to whether the supplemental food
source alone could have been equally effective at preventing
during growth. J. Biol. Chem. 23: 231–254.
18. Orr, J. B. & Richards, M. B.
growth faltering. The few interventions that provided animal
source foods alone were restricted to those that provided milk
19. Lamb, A. J., Apiwatanaporn, P. & Olsen, J. A.
powder. Although milk powder may provide some additional
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20. Anzano, M. A., Lamb, A. J. & Olsen, J. A.
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sequence of pathological signs and survival following the induction of rapid,
iron and zinc or of vitamin A, as compared to beef for example.
synchronous vitamin A deﬁciency in the rat. J. Nutr. 109: 1419–1431.
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supplementation were conducted in Papua, New Guinea,
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Cooperative Agreement # DAN 1309-A-00–9090–00, April 1992. University of
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Going, going, gone By Kathy Method, Clinical Senior Editor, Centralized Content Group Patents set to expire soon on many brand-name drugs Time is running out on the U.S. patents for many of the most popular brand-name drugs. Unless original exclusivity dates are somehow extended, over the next several years generic versions of many well-known best-selling drugs will become available. Pharma
SOGC CLINICAL PRACTICE GUIDELINE SOGC Clinical Practice Guideline No. 248, September 2010 (Replaces No. 74, July 1998) Guidelines for the Evaluation and Treatment of Recurrent Urinary Incontinence Following Pelvic Floor Surgery Abstract This clinical practice guideline has been prepared by the Objective: To provide general gynaecologists and urogynaecologists Urogynaecology Committe