J P G N: Espghan Naspghan

V O L U M E 4 3 ♦ S U P P L E M E N T 3 ♦ D E C E M B E R 2 0 0 6
JOURNAL OF PEDIATRIC GASTROENTEROLOGY AND NUTRITION

JPGN w w w. j p g n . o r g
The Official Journal of

ESPGHAN ♦ NASPGHAN
NUTRITIONAL SOLUTIONS TO MAJOR PUBLIC HEALTH

PROBLEMS OF PRESCHOOL CHILDREN:
HOW TO OPTIMISE GROWTH AND DEVELOPMENT
VOL. 43, SUPPL. 3, DECEMBER 2006 PAGES S1–S73

OLIVIER GOULET, EMANUEL LEBENTHAL, DAVID BRANSKI,
AND PETER J.H. JONES
GUEST EDITORS
JPGN
Volume 43
Supplement 3
December
2006

European Society for Pediatric Gastroenterology, Hepatology and Nutrition
and the
North American Society for Pediatric Gastroenterology, Hepatology and Nutrition
Nutritional Solutions to Major Public Health Problems of

Preschool Children: How to Optimise Growth and Development
Olivier Goulet, Emanuel Lebenthal, David Branski, and Peter J.H. Jones
Guest Editors
Publication of this supplement was supported by an unrestricted

educational grant from Danone Institute International
JPGN
A Journal of Clinical, Experimental, and Developmental Investigation in
Pediatric Gastroenterology, Hepatology, and Nutrition
www.jpgn.org
European Society for Pediatric North American Society for Pediatric
Gastroenterology, Hepatology and Nutrition Gastroenterology, Hepatology and Nutrition
www.espghan.org www.naspghan.org
ESPGHAN Editor NASPGHAN Editor
Alfredo Guarino, M.D. Eric Sibley, M.D., Ph.D.
Department of Pediatrics Department of Pediatrics
University Federico II Stanford University School of Medicine
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80131, Naples, Italy Palo Alto, CA 94304
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Founding Editor
Emanuel Lebenthal, M.D.
Editorial Board
representing ESPGHAN representing NASPGHAN
Marc Benninga, M.D./Amsterdam, The Netherlands Estella Alonso, M.D./Chicago, Illinois
Jean de Ville de Goyet, M.D./Birmingham, United Kingdom Warren P. Bishop, M.D./Iowa City, Iowa
Magnus Domellof, M.D./Umea, Sweden Steven J. Czinn, M.D./Baltimore, Maryland
Jean Michel Guys, M.D./Marseille, France Glenn T. Furuta, M.D./Boston, Massachusetts
Jean-Pierre Hugot, M.D./Paris, France Maria M. Oliva-Hemker, M.D./Baltimore, Maryland
Steffen Husby, M.D./Odense, Denmark Christopher Liacouras, M.D./Philadelphia, Pennsylvania
Marko Kalliomaki, M.D./Turku, Finland Carlo Di Lorenzo, M.D./Columbus, Ohio
Keith Lindley, M.D./London, United Kingdom Jean Molleston, M.D./Indianapolis, Indiana
Antal Németh, M.D./Stockholm, Sweden Joel R. Rosh, M.D./Morristown, New Jersey
Frank M. Ruemmele, M.D./Paris, France
Hania Szajewska, M.D./Warsaw, Poland representing LASPGHN
Mike Thomson, M.D./London, United Kingdom Jaime Belkind Gerson, M.D./Cuernavaca, Mexico
Heiko Witt, M.D./Berlin, Germany
representing APPSPGHN
Seng-Hok Quak, M.D./Singapore
Senior Associate Editor Associate Editors
Naples, Italy Palo Alto, California
Riccardo Troncone, M.D. Dorsey M. Bass, M.D.
William E. Berquist, M.D.
Associate Editors Ricardo O. Castillo, M.D.
Naples, Italy Kenneth L. Cox, M.D.
Eugenia Bruzzese, M.D. Melissa Hurwitz, M.D.
Roberto Berni Canani, M.D., Ph.D. John A. Kerner, M.D.
Ciro Esposito, M.D. Kenneth H. Brown, M.D./Davis, California
Luigi Maiuri, M.D. Ricardo Uauy, M.D., Ph.D./Santiago, Chile
Francesco Raimondi, M.D.
Maria Immacolata Spagnuolo, M.D. Consulting Biostatistician
Annamaria Staiano, M.D. Tyson H. Holmes, Ph.D./Palo Alto, California
Pietro Vajro, M.D. Selected Summary Editors
Raffaele Iorio, M.D. Warren P. Bishop, M.D./Iowa City, Iowa
Carlo Agostoni, M.D./Milan, Italy Joel R. Rosh, M.D./Morristown, New Jersey
Alberto Ravelli, M.D./Brescia, Italy Image of the Month Editor
Selected Summary Editors Christopher Liacouras, M.D./Philadelphia, Pennsylvania
Christian Braegger, M.D./Zurich, Switzerland Book Review Editor
Adrian Thomas, M.D./Manchester, England Steven J. Czinn, M.D./Baltimore, Maryland
News & Views Editor News & Views Editors
Yigael Finkel, M.D., Ph.D./Stockholm, Sweden Jean Molleston, M.D./Indianapolis, Indiana
Consulting Editor for Societal Papers Estella Alonso, M.D./Chicago, Illinois
Stefano Guandalini, M.D./Chicago, USA Maria Oliva-Hemker, M.D./Baltimore, Maryland
Officers of the European Society of Officers of the North American Society for
Paediatric Gastroenterology, Hepatology and Nutrition Pediatric Gastroenterology, Hepatology and Nutrition
President President
Michael J. Lentze, M.D./Bonn, Germany Philip M. Sherman, M.D., F.R.C.P.C./Toronto, Canada
Chairman, Publications Committee
Michael J. Lentze, M.D./Bonn, Germany Chairman, Publications Committee
Mitchell B. Cohen, M.D./Cincinnati, Ohio
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J P G N Volume 43
Supplement 3
December
JOURNAL OF PEDIATRIC GASTROENTEROLOGY AND NUTRITION 2006

European Society for Pediatric Gastroenterology, Hepatology and Nutrition
and the
North American Society for Pediatric Gastroenterology, Hepatology and Nutrition
CONTENTS
Editorial S1
Olivier Goulet, Emanuel Lebenthal, David Branski, Agnès Martin, Jean-Michel Antoine, and Peter J.H. Jones
Nutritional Solutions to Major Health Problems of Preschool Children: How to Optimise Growth S4
and Development
Francesco Branca
Causes of Nutrition-related Public Health Problems of Preschool Children: Available Diet S8

Lindsay H. Allen
Effect of Infections and Environmental Factors on Growth and Nutritional Status in Developing Countries S13
Zulfiqar Ahmed Bhutta
Nutritional Deficiencies in Learning and Cognition S22

S. Yehuda, S. Rabinovitz, and D.I. Mostofsky
(continued on next page)
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Prevention and Control of Obesity in Preschool Children: Importance of Normative Standards S26
Ricardo Uauy, Juanita Rojas, Camila Corvalan, Lydia Lera, and Juliana Kain
Tackling the Child Malnutrition Problem: From What and Why to How Much and How S38
Milla McLachlan
Successful Food-Based Programmes, Supplementation and Fortification S47

M.G. Venkatesh Mannar
Solutions to Nutrition-related Health Problems of Preschool Children: Education and Nutritional Policies S54
for Children
Ian Darnton-Hill, Eileen Kennedy, Bruce Cogill, and S.M. Moazzem Hossain
Priorities in Nutritional Rehabilitation S66

Stanley Zlotkin
The Danone Institutes S72
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Journal of Pediatric Gastroenterology and Nutrition
43:S1–S3 # December 2006 Lippincott Williams & Wilkins, Philadelphia
Editorial
Nutritional Solutions to Major Health Problems of Preschool

Children: How to Optimise Growth and Development
Olivier Goulet, Emanuel Lebenthaly, David Branskiz, Agnès Martin§, Jean-Michel Antoine§, and
Peter J.H. Jonesjj
Hôpital Necker Enfants-Malades, Paris, France, {Department of Paediatrics, Hadassah Hebrew University Hospital, Jerusalem,
Israel, {Department of Paediatrics, Shaare Zedek Medical Center, Jerusalem, §Danone Institute International, Palaiseau, France,
and jjSchool of Dietetics and Human Nutrition, McGill University, Montreal, Canada
Significant opportunities to improve child health glob- diseases, lack of exclusive breast-feeding and margin-
ally were provided in the second half of the 20th century. alization of females within society are also emerging as
However, malnutrition remains a major problem and in key issues. Many types of nutritional deficiencies have
many countries the situation seems to have worsened (1). been shown to be detrimental to child development. Most
In a recent report about survival rate in childhood (2), of the existing information pertains to the possible effects
UNICEF remained that the United Nation’s first Millen- of low birth weight, inadequate breast-feeding, stunting
nium Goal, was to eradicate extreme poverty and to and wasting, short-term food deprivation, and micronu-
reduce the proportion of people who suffer from hunger trient deficiencies. It is well established that deficiencies
by half between 1990 and 2015, as measured by the of micronutrients, such as vitamin A, increase the risk of
percentage of children under five years of age who are childhood infections and subsequent mortality (6). Nutri-
underweight. The first Millennium Goal of the United tional interventions have a major impact, as emphasized
Nations is to eradicate extreme poverty and to reduce the by both Allen and Bhutta in their articles in this supple-
proportion of people who suffer from hunger by half ment to the Journal of Pediatric Gastroenterology and
between 1990 and 2015, as measured by the percentage Nutrition. Child nutrition programs involving vitamin A
of children under 5 y old who are underweight. supplementation are recognized as important public
It is estimated that 146 million children under age 5 y health interventions among young children in areas of
are underweight. It was reported that undernutrition endemic vitamin A deficiency. Other deficiencies of
accounts for almost half of the deaths of children under micronutrients such as zinc and iron are also being
5 (3). Worldwide more than half of the underweight recognized as widespread in developing countries and
children reside in south Asia, primarily in India, Bangla- associated with increased risk of morbidity and mortality.
desh and Pakistan. Similarly, the prevalence of childhood The impact of infections on micronutrient status and their
undernutrition in sub-Saharan Africa has not changed subsequent impact on health outcomes have also been
appreciably since 1990 but, with population growth, the established. Increased losses of micronutrients such as
number of underweight children has increased. More- vitamin A and zinc during infectious illnesses, especially
over, the situation has worsened during the last 20 y, diarrhoea, are important contributors to micronutrient
especially in sub-Saharan Africa and South Asia con- deficiencies. The role of zinc supplementation in accel-
comitantly with the onset of HIV/AIDS (4,5). Indeed, erating recovery from diarrhoeal diseases in developing
through worsening malnutrition, this burden of disease countries supports its use in endemic areas from the
contributes to reversal of gains made by child survival viewpoint of public health strategies (7). Furthermore,
programs. Based on the same developments, it seems vitamin C and zinc reduce the incidence and improve the
unlikely that the nutrition component of the UN’s first outcome of pneumonia and malaria, especially in chil-
Millennium Goal will be achieved by 2015. dren in developing countries (8).
The main problem is not necessarily a shortage of food. It is clear that nutritional solutions for preschool
Micronutrient deficiencies, poor sanitation, infectious children remain a challenge for the third millennium.
It is well established that inappropriate feeding and
infections are the main causes of protein-energy malnu-
Address correspondence and reprint requests to Olivier Goulet, MD,
Hôpital Necker Enfants-Malades, 149 rue de Sèvres, 75015 Paris, trition, which contributes to morbidity and mortality in
France (e-mail: olivier.goulet@nck.ap-hop-paris.fr). preschool children. As mentioned previously, nutritional
S1
S2 GOULET ET AL.
interventions may improve infant and young child nutri- postnatal catch-up growth and the onset of metabolic
tion and health. This is central to human well-being and and cardiovascular diseases in adulthood (14).
as such contributes to both economic development and Establishing the links between nutrition and brain
poverty reduction. However, current circumstances development is challenging. However, there is increasing
reveal a nutritional paradox. As reported by Uauy and evidence that protein-energy malnutrition has deleterious
coworkers in Latin America and emphasized by Zlotkin effects on learning and cognition (15). Many studies have
in this issue, overweight and obesity are increasing suggested or even demonstrated that these effects are
rapidly in more developed areas of the world. The current dependent not only upon the type of nutrients involved
system of sharing world resources has resulted in a (eg, iron, iodine, selenium, zinc, vitamin A, essential
paradigm in which the number of obese and overweight fatty acids) but also upon the specific periods of devel-
children actually surpasses the number of undernourished opment including prenatal life, infancy, school age and
children globally. Improving weight gain is thus insuffi- aging. The postinfancy or preschool age is a period in
cient to promote child health (9). Thus, underweight, which a number of nutritional deficiencies have been
obesity and iron deficiency may coexist in the same shown to interfere with normal development and cogni-
country and even in the same household at the same time. tion (16). The most commonly studied deficiencies in
Nutritional rehabilitation and prevention may be children with protein-energy malnutrition are iodine, iron
achieved by carefully assessing the situation associated and essential fatty acids deficiencies. Yehuda and cow-
with an integrated combination of improved dietary orkers provide in this issue a short review that aims to
intake, supplementation, commercial and home-based examine the limited studies that have been performed on
fortification of complementary foods. As emphasized children of this age and offer a broader view on this topic.
by Mannar, several developing as well as developed Finally, previous experience as well as more recent
countries have implemented with sustained impact suc- knowledge establishes the link between early nutrition
cessful approaches to eliminate protein-energy malnu- and health, not only in childhood but also in adulthood.
trition and micronutrient deficiencies for nutrients Nutrition during pregnancy as well as feeding during
including iron, iodine, selenium, zinc and vitamin A. infancy and young childhood remain crucial issues for
These include provision of oral supplements in capsule, humanity, whether in developing or developed countries.
tablet or syrup form as well as fortified complementary Assessing the nutritional status of populations,
foods provided through public feeding programs and improving research and knowledge in the field of nutri-
commercially marketed foods. Mannar stresses that gov- tion and increasing food resources by developing agri-
ernment commitment, clear policy and program direc- culture and economies exist as the challenges of this
tion, advocacy and communication combined with a century and beyond. Globally malnutrition, whether
strong public–private partnership are essential for suc- intrauterine growth retardation, vitamin or micronutrient
cessful programs to improve the health and well-being of deficiency, inappropriate protein and/or energy supply,
millions of children around the world. persist as significant causes of disability, with young
Importantly, during the last 3 decades the links children the worst affected.
between infant nutrition and health in adulthood have As emphasized by Darnton-Hill in this supplement,
been established. Clinical and experimental data have improved health and nutrition will lead to enhanced
provided evidence that the concentrations of hormones, economic development, but having a poverty focus
metabolites and neurotransmitters during critical phases appears to be essential if poor people are not to be
of early human development may have detrimental marginalized further. The HIV/AIDS pandemic illus-
effects on brain development and metabolic processes trates this challenge clearly. The role of education,
and may cause diseases in subsequent adulthood. This especially girls’ education, in improved health and nutri-
phenomenon is recognized today as programming or tion status of children and in birth spacing, is now clear,
metabolic imprinting. Interactions between the genetic as is improving women’s status. Increases in female
background of the individuals and environmental influ- status and education have been estimated to account
ences during infancy and early childhood are supported for half of the reduction in child malnutrition rates during
by numerous experimental data (10). There is now the past 25 y.
evidence in humans that programming is 1 of the most Thus, it was logical to devote a symposium to how to
important risk factors for obesity and cardiovascular adequately feed preschool-age children and to overcome
disease (11). Barker and coworkers provided strong the double burden of malnutrition: undernutrition and
epidemiological evidence for a link between the quality obesity. This supplement of the Journal of Pediatric
of foetal growth as assessed by anthropometric measures Gastroenterology and Nutrition reports the proceedings
at birth and morbidity and mortality during adulthood, of the 2005 symposium on nutritional solutions to major
especially in terms of high blood pressure and cardio- public health problems of preschool children, organized
vascular disease (12,13). In addition, Barker et al. pro- by Danone Institute International in Durban, South
vided evidence for a strong link between the rate of Africa, on the occasion of the 18th International Congress
J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

EDITORIAL S3
of Nutrition. This collection of presented papers offers a 7. Bobat R, Coovadia H, Stephen C, et al. Safety and efficacy of zinc
unique opportunity to report the outstanding work of supplementation for children with HIV-1 infection in South Africa:
well-known international experts in the field. It is critical a randomised double-blind placebo-controlled trial. Lancet
2005;366:1862–7.
to promote the right of all of the world’s children to 8. Edejer TT, Aikins M, Black R, et al. Cost effectiveness analysis
achieve their full genetic growth potential and to guard of strategies for child health in developing countries. BMJ
against the side effects of an inadequate nutritional 2005;331:1177.
supply, whether caused by under- or overnutrition. 9. Uauy R, Lock K. Commentary: the importance of addressing the
rise of overweight and obesity–progress or lack of action during the
last fifty years? Int J Epidemiol 2006;35:18–20.
REFERENCES 10. Ozanne SE, Fernandez-Twinn D, Hales CN. Fetal growth and adult
diseases. Semin Perinatol 2004;28:81–7.
1. de Onis M, Frongillo EA, Blossner M. Is malnutrition declining? An 11. Plagemann A. Fetal programming and functional teratogenesis: on
analysis of changes in levels of child malnutrition since 1980. Bull epigenetic mechanisms and prevention of perinatally acquired
WHO 2000;78:1222–33. lasting health risks. J Perinat Med 2004;32:297–305.
2. UNICEF. Progress for Children: A Child Survival Report. Available 12. Barker DJP, Winter PD, Osmond C, et al. Weight in infancy and
at http://www.unicef.org/publications/index_23557.html. Accessed death from ischaemic heart disease. Lancet 1989;2:577–80.
November 27, 2006. 13. Eriksson JG, Forsen TJ, Tuomilheto J, et al. Early growth and
3. Salama P, Spiegel P, Talley L, et al. Lessons learned from complex coronary heart disease in later life: longitudinal study. BMJ
emergencies over past decade. Lancet 2004;364:1801–13. 2001;322:(7292):949–53.
4. Ainsworth M, Waranya T. Breaking the silence: setting realistic 14. Barker DJP, Osmond C, Forsen TJ, et al. Trajectories of growth
priorities for AIDS control in less-developed countries. Lancet among children who have coronary events as adults. N Engl J Med
2000;356:55–60. 2005;353:1802–9.
5. Black RE. Micronutrient deficiency—an underlying cause of mor- 15. Koizumi H. The concept of ‘‘developing the brain’’: a new
bidity and mortality. Bull WHO 2003;2:79–81. natural science for learning and education. Brain Devel 2004;
6. Wintergerst ES, Maggini S, Hornig DH. Immune-enhancing role of 26:434–41.
vitamin C and zinc and effect on clinical conditions. Ann Nutr 16. Bryan J, Osendarp S, Hughes D, et al. Nutrients for cognitive
Metab 2005;50:85–94. development in school-aged children. Nutr Rev 2004;62:295–306.

Nutritional Solutions to Major Health Problems of Preschool

Children: How to Optimise Growth and Development
Francesco Branca, MD, PhD
Regional Adviser Nutrition and Food Security, World Health Organization, Regional Office for Europe, Copenhagen, Denmark
ABSTRACT
Despite major economic development in the last few decades, socioeconomic strata are mainly affected and, in turn, malnu-
childhood nutrition remains a great challenge for the human trition hampers their development. The eradication of child
species. A combination of undernutrition, overnutrition, and malnutrition is crucial in the fight against poverty. This article
poor dietary quality affect to a variable extent all of the world’s examines whether this goal will be achieved within the time
populations, and are often combined in the same areas and even frame the United Nations has set. JPGN 43:S4–S7, 2006.
in the same families. Malnutrition is part of the life of many Key Words: Childhood malnutrition—Childhood obesity—
individuals since conception and is transmitted by 1 generation Iron deficiency—Essential fatty acid deficiency—Vitamin A.
to the next. Countries with lower income per capita and poor # 2006 Lippincott Williams & Wilkins
INTRODUCTION A major challenge that still is unrecognised is the one

referred to as hidden hunger, generated by poor dietary
The first United Nations Millennium Development quality and involving inadequate micronutrient intake.
Goal (MDG), set in 2000, is to ‘‘eradicate extreme hunger Implementing appropriate intervention strategies for
and poverty’’ (1). To achieve this goal, the target is to specific populations is the only way in which the MDGs
halve both the number of people suffering from hunger have any chance of being achieved.
and those whose income is less than $1/d by 2015. This
article focuses on why the eradication of child malnu-
trition is so crucial in the fight against poverty and UNDERNUTRITION
discusses whether this goal will be achieved within the Undernutrition remains a huge cause of mortality for
time frame the United Nations has set. children throughout the world, with approximately
In some regions of the world, such as Asia, great strides 10 million children dying before the age of 5 years.
have been made to alleviate hunger, but the difficulties in Although global childhood mortality declined from 147
other regions make the MDGs for nutrition look unac- deaths per 1000 live births in 1970 to 80 deaths in 2002,
hievable (2). Poor nutrition in childhood fuels the poverty improvements are not universal. In some regions, especi-
cycle, in which underachievement, reduced opportu- ally in sub-Saharan Africa, childhood mortality has not
nities, and greater morbidity and mortality ensue for that decreased, and 14 African countries have child mortality
and subsequent generations. rates that are higher now than in 1990 (5). HIV/AIDS has
In recent years overnutrition has resulted in a huge also had a significant impact in this region.
increase in the numbers of children who are overweight
or obese. This will become a considerable health burden
to many countries because the problem is of epidemic Low Birth Weight
proportions and runs alongside the age-old issue of
undernutrition. In some low-to-middle income countries An estimated 1 in 6 infants is born with a low birth
both ends of the nutritional spectrum are found (3,4). weight; that is, less than 2500 g (6). Worldwide, >20
million babies are born with low birth weight, around
95% of them in developing countries. Even this is an
Address correspondence and reprint requests to Dr Francesco Branca, underestimate because many babies born at home or with
World Health Organization Regional Office for Europe, Scherfigsvej 8, traditional birth attendants are not weighed at all. The
2100 Copenhagen, Denmark (e-mail: fbr@euro.who.int). problem arises because they either have been born too
S4
OPTIMISING GROWTH AND DEVELOPMENT OF PRESCHOOL CHILDREN S5
early, have experienced growth restriction, or both. The However, it is unlikely that the goals will universally be
health and nutrition of the mother significantly influence met. The great improvements are mainly due to the
these factors. A low birth weight predisposes an infant to formidable economic and social changes in Southeast
a wide range of other risk factors including developing Asia, whereas in other parts of the world, such as sub-
and dying from diarrhoea or infectious diseases. Con- Saharan Africa, the prevalence of underweight in chil-
tinued malnutrition and underweight can also lead to dren under age 5 years is forecast to increase from 24% to
decreased cognitive development (7) with a significant 26.8%. In this region, HIV/AIDS has had a huge impact
impact on productivity in adulthood, and an increased on the population, and continues to affect the health and
risk of wasting or stunted growth (8). development of infants and children (2).
In affluent societies, low birth weight is known to be a
significant risk factor for other health outcomes in later OVERNUTRITION
life. These outcomes include coronary heart disease,
stroke, type 2 diabetes mellitus, and the metabolic syn- For an increasing number of children, overweight and
drome. Their impact cannot be discounted in developing obesity have become the health issue of their generation.
countries, where early deprivation may ‘‘programme’’ a Even in countries that have traditionally been associated
child so that subsequent ‘‘overnutrition’’ may have a with good dietary health, such as the Mediterranean
significant effect on morbidity and mortality rates (9). countries of southern Europe, obesity is commonplace
Actions, including better maternal nutrition, breast-feed- in children (14). Italy, for example, has an estimated 35%
ing and improved complementary feeding, to ensure of primary-school children (7–11 y) with a body mass
optimal fetal development to reduce the immediate health index >25. Overnutrition is also found in populations that
impact and the future increased chronic disease risk are may also have malnutrition, and it is often the poor and
therefore warranted. disadvantaged sectors of the population who suffer (15).
Global estimates of overweight suggest that some
Stunting 20 million children and 1 billion adults are overweight.
Chronic noncommunicable diseases such as heart dis-
The first MDG target, halving the number of people ease, cancer, stroke and diabetes account for 60% of
suffering from hunger, uses the prevalence of under- global deaths and 47% of the burden of disease. The
weight in children under 5 years old as a key indicator. incidence of noncommunicable diseases is expected to
Underweight measures chronic malnutrition (low height grow as many low to middle income countries start to
for age or stunting) as well as acute malnutrition (low exhibit the diseases formerly associated with more
weight for age or wasting), but the contribution of affluent countries.
stunting to underweight is greater than that of wasting. The International Obesity Task Force has shown an
Stunting is generally declining worldwide. The World increasing incidence of childhood obesity in the last
Health Organization (10) reported that between 1990 and decade, and it is expected to continue to rise dramatically
2000, the global prevalence of stunting in children fell over the next several decades unless serious action is
from 34% to 29%. However, in eastern Africa, the undertaken to reduce the environmental pressure to avoid
number of children with stunting increased in this period energy overconsumption and sedentary lifestyles (16).
from 40 million to 45 million. Stunting is defined by the As with malnutrition, the obesity epidemic is multi-
World Health Organization as 2 standard deviations dimensional. The high availability of low-cost, high–
below the z scores for height and for age. Children energy content foods and drinks, with ever-expanding
who are underweight or stunted in growth may not show portion sizes available in fast food outlets promoted by
catch-up growth in later childhood and thus carry the risk heavy marketing is 1 of the main determinants (17). The
of continuing poor health into adult life (11). In some increased amount of leisure time spent in sedentary
countries, for example, South Africa, children who are activities such as television viewing and playing
growth stunted coexist with those who are overweight or electronic games (18), with a corresponding reduction
obese (12). This of course has complex implications of physical activity in schools and transportation policies
for policymakers. encouraging sedentary behaviour is another determinant
(19). A link between the decline in breast-feeding and a
Wasting concomitant rise in childhood overweight has also been
demonstrated (20).
Children who have low weight for age (wasted) are at
increased risk of dying from pneumonia, measles, HIDDEN HUNGER
malaria or diarrhoea (13). Throughout the world the
numbers of underweight children are decreasing and it Malnutrition is not just about insufficient energy
is thought this global decline will continue until 2015, the intake. In many parts of the world, inadequate dietary
date by which the MDGs should have been achieved. iron, zinc, iodine and vitamin A cause significant ill

S6 BRANCA
health that affects generation after generation. Malnu- essential for good vision, deficiency leads to poor night
trition of the child feeds into an insidious vicious cycle of vision, xerophthalmia and ultimately to blindness.
poor health and poor outcomes throughout life. Poor
childhood nutrition does not equip women for pregnancy Cost of Micronutrient Malnutrition
and birth; a malnourished mother with low stores of
micronutrients gives birth to children who continue in Interventions to reduce micronutrient deficiency can
the same cycle. Elderly people are more susceptible to have a significant effect on subsequent generations and
infections and less able to take care of young children. improve the economic performance of segments of the
The cycle of malnutrition therefore continues from 1 population. Studies in China have clearly shown the
generation to the next. Interventions are needed not economic impact of interventions to reduce iron and
only for children but also for the mothers. There is no iodine deficiency and decrease stunting (27). It has been
doubt that improving maternal nutrition can improve estimated that the increase in productivity due to a 30%
the birth outcomes and the subsequent growth of the reduction in iron-deficiency anaemia over 10 years would
offspring (26). be worth 107 billion yen. If childhood anemia was also
reduced by 30% during the same time period, the
Iron economic gain would be as much as 348 billion yen,
considerably less than the cost of any intervention.
Iron deficiency is a less obvious form of malnutrition
than protein energy malnutrition but it permeates all CONCLUSIONS
aspects of child health in developing countries. Iron-
deficiency anaemia affects the growth, cognition, motor Despite major economic development in recent dec-
development and social development of children, result- ades, childhood nutrition remains a great challenge for
ing in reduced school performance and lowered pro- the human species. A combination of undernutrition,
ductivity. In conjunction with serious infection, it also overnutrition and poor dietary quality affect to a variable
can bring about irreversible and lifelong consequences, extent all of the world’s populations, often combined in
diminishing the potential of the child. Iron-deficiency the same areas and even in the same families. Malnu-
anaemia is an extremely common condition, especially in trition often accompanies the life of individuals from
Africa where the incidence is as high as 80% of children conception and is transmitted by 1 generation to the next.
under 5 years (21), closely followed by India and other Countries with lower income per capita and poor socio-
countries in southern and Southeast Asia. economic strata are mainly affected and, in turn, malnu-
trition hampers their development.
Iodine As shown by some success stories, general interven-
tions to reduce poverty and improve livelihoods are
Iodine deficiency remains a significant problem in necessary, but often not sufficient to improve nutritional
those parts of the globe with low water levels of iodine. status. Specific nutrition actions are therefore also
The consequences of this deficiency particularly affect needed. These must start from conception and early
pregnant women and their offspring with increased risk infancy.
of perinatal mortality and the mental retardation of the
child (22). In areas where iodine deficiency is endemic it REFERENCES
is estimated that up to 15% of the population can suffer
1. United Nations. The Millennium Development Goals Report 2005.
from cretinism (23). South central Asia has a high New York: United Nations; 2005.
prevalence of iodine deficiency, with 104 million school- 2. de Onis M, Blossner M, Borghi E, et al. Estimates of global
children having insufficient iodine. Iodine deficiency is prevalence of childhood underweight in 1990 and 2015. JAMA
often combined with iron deficiency, thus creating a 2004;291:2600–6.
long-term threat to neurodevelopment, as in the case 3. Beaglehole R. Responding to the dual burden of nutritional dis-
of Tajikistan (24). eases. Asia Pac J Clin Nutr 2004;13 (Suppl):S1.
4. James PT, Rigby N, Leach R. The obesity epidemic, metabolic
syndrome and future prevention strategies. Eur J Cardiovasc Prev
Vitamin A Rehabil 2004;11:3–8.
5. World Health Organization. World Health Organization Report
Vitamin A deficiency is one of the most common 2003—Shaping the Future. Geneva: World Health Organization;
deficiency syndromes in children in developing countries 2003.
(25). Deficiency leads to reduced immunity, with the 6. United Nations Children’s Fund, World Health Organization, Uni-
resultant increased severity and complications of infected Nations Children’s Fund and World Health Organization. Low
Birthweight: Country, Regional and Global Estimates. New York:
tions. There can be growth faltering and poor develop- UNICEF; 2004.
ment, and the breakdown of epithelial cells in the 7. Olness K. Effects on brain development leading to cognitive impair-
respiratory and digestive tract. Because vitamin A is also ment: a worldwide epidemic. J Dev Behav Pediatr 2003;24:120–30.

OPTIMISING GROWTH AND DEVELOPMENT OF PRESCHOOL CHILDREN S7
8. Khor GL. Update on the prevalence of malnutrition among children 18. Dennison BE, Erb TA, Jenkins PL. Television viewing and televi-
in Asia. Nepal Med Coll J 2003;5:113–22. sion in bedroom associated with overweight risk among low income
9. Prentice AM, Moore SE. Early programming of adult diseases in preschool children. Pediatrics 2002;109:1028–35.
resource poor countries. Arch Dis Child 2005;90:429–32. 19. Kaur H, Hyder ML, Poston WS. Childhood overweight: an ex-
10. de Onis M, Blossner M. Methodology for estimating regional and panding problem. Treat Endocrinol 2003;2:375–88.
global trends of child malnutrition. Int J Epidemiol 2004;33:1260– 20. von Kries R, Koletzko B, Sauerwald T, et al. Breast feeding and
70. obesity: cross sectional study. BMJ 1999;319:147–50.
11. Friedman JF, Phillips-Howard PA, Mirel LB, et al. Progression of 21. Measure Demographic and Health Surveys. 2003.
stunting and its predictors among school-aged children in western 22. Sachdev H, Gera T, Nestel P. Effect of iron supplementation on
Kenya. Eur J Clin Nutr 2005;59:914–22. mental and motor development in children: systematic review of
12. Jinabhai CC, Taylor M, Sullivan KR. Changing patterns of under- randomised controlled trials. Public Health Nutr 2005;8:117–32.
and over-nutrition in South African children-future risks of non- 23. Boyages SC. Primary pediatric hypothyroidism and endemic
communicable diseases. Ann Trop Paediatr 2005;25:3–15. cretinism. Curr Ther Endocrinol Metab 1994;5:94–8.
13. Caulfield LE, de Onis M, Blossner M, et al. Undernutrition as 24. de Benoist B, Egli I, Takkouche B, et al. Iodine Status Worldwide:
an underlying cause of child deaths associated with diarrhea, WHO Global Database on Iodine Deficiency. Geneva: World
pneumonia, malaria, and measles. Am J Clin Nutr 2004;80: Health Organization; 2004.
193–8. 25. Ag Bendech M, Malvy DJ, Chauliac M. Vitamin A deficiency:
14. Lobstein T, Frelut ML. Prevalence of overweight among children in epidemiological aspects and control methods. Sante 1997;7:
Europe. Obes Rev 2003;4:195–200. 309–16.
15. Darnton-Hill I, Coyne ET. Feast and famine: socioeconomic dis- 26. Stein AD, Barnhart HX, Hickey M, et al. Prospective study of
parities in global nutrition and health. Public Health Nutr protein-energy supplementation early in life and of growth in the
1998;1:23–31. subsequent generation in Guatemala. Am J Clin Nutr 2003;78:
16. Rigby NJ, Kumanyika S, James WP. Confronting the epidemic: the 162–7.
need for global solutions. J Public Health Policy 2004;25:418–34. 27. Ross J, Chen CM, He W, et al. Effects of malnutrition on economic
17. Nicklas TA, Baranowski T, Cullen KW, et al. Eating patterns, productivity in China as estimated by PROFILES. Biomed Environ
dietary quality and obesity. J Am Coll Nutr 2001;20:599–608. Sci 2003;16:195–205.

Causes of Nutrition-related Public Health Problems of Preschool

Children: Available Diet
Lindsay H. Allen, PhD
Director, USDA, ARS Western Human Nutrition Research Center
ABSTRACT
The primary goal of this review is to examine the timing and micronutrient intakes and resulting deficiencies are common in
nature of dietary inadequacy during the first 5 years of life. An preschoolers because of a lack of sufficient animal source foods,
important issue is that many children in developing countries and have been associated with delayed child development.
are already nutritionally depleted by the end of the first year of Dietary diversity is an especially important determinant of
life, because maternal undernutrition can cause low fetal micronutrient intakes when animal source food intake is low.
accumulation of nutrient stores and secretion of inadequate Interventions with animal source foods have produced improve-
amounts of some micronutrients in breast milk. Improvement of ments in growth, micronutrient status, cognitive performance
maternal diet and micronutrient status is required to remedy this and activity of children. Although much is now known about the
situation. During the period of complementary feeding, most role of inadequate diets in preschooler malnutrition, on a global
households may be able to provide their young children with scale the ability of households to apply this knowledge to
sufficient energy and protein from home-produced complemen- improve the diets of their children is still limited. JPGN
tary foods, but many do not feed foods with an adequate energy 43:S8–S12, 2006. Key Words: Preschoolers—Malnutrition—
density or a sufficient number of meals per day. Inadequate Diet—Micronutrients. # 2006 Lippincott Williams & Wilkins
INTRODUCTION IMPORTANCE OF NUTRITIONAL DEPLETION

ON ENTRY TO THE PRESCHOOL PERIOD
Among the several causes of preschooler malnutrition
discussed in this symposium, consumption of an When discussing the needs of preschoolers, it is
inadequate diet obviously is a primary causal factor. In important to recognize that a high proportion of children
this review we summarize current knowledge about lack in developing countries are already nutritionally depleted
of an adequate diet during specific stages of early child- when they enter this phase of life. Many are born low
hood development, and the relative importance of macro- birth weight or preterm, which results in their nutrient
nutrient intake versus dietary quality (dietary diversity (eg, iron) stores at birth being relatively depleted (1).
and the consumption of animal source foods [ASF]). Poor maternal micronutrient status during pregnancy
Although this review addresses the diet of preschoolers almost certainly contributes to lower infant nutrient
(2–5 y), data were often lacking from this age group so deposition in utero, for example, for iron (2) and vitamin
that some information was used from younger and B12 (3,4). These mothers are likely to continue to be at
older children. high risk for micronutrient deficiencies during lactation,
An ‘‘adequate diet’’ for children is one that contains an a time when nutrient requirements of the mother are even
appropriate density of nutrients, is sufficiently diverse higher due to the secretion of nutrients in breast milk.
that it supplies adequate but not excessive amounts of This means that the concentrations of some nutrients in
nutrients, is palatable and culturally acceptable, afford- the breast milk will be lower than normal, especially B
able and available year-round and overall supports nor- vitamins (except for folate), vitamin A, iodine and
mal growth and development. selenium, which puts the breast-feeding infant and child
at risk for these micronutrient deficiencies (5). Thus,
infants may often be subjected to in utero depletion and/
or low breast milk concentrations of nutrients, leading to
Address correspondence and reprint request to Dr Lindsay Allen,
3253B Meyer Hall, University of California, One Shields Avenue, nutritional deficiency during the first 6 to 12 months of
Davis, CA 95616 (e-mail: lhallen@ucdavis.edu). life (5). For example, we have reported that 49% of
S8
CAUSES OF NUTRITION-RELATED PUBLIC HEALTH PROBLEMS OF PRESCHOOL CHILDREN S9
lactating mothers in Guatemala City and 68% of their met only if large amounts of liver were to be included in
breast-feeding infants have low or deficient plasma the diet. If the amount recommended by the World Health
vitamin B12 concentrations at 12 months of age (6). Organization (1 rounded tablespoon per day) were to be
The fact that infant nutritional depletion can occur in consumed routinely, however, vitamin A intakes would
breast-fed infants in no way contraindicates the recom- be 20 times greater than recommended. An additional
mendation for exclusive breast-feeding during the first problem is that the per-capita amounts of meat, liver and
6 months of life, but rather indicates the need to improve egg available in Guatemala, Bangladesh and Malawi
maternal micronutrient status during pregnancy and were estimated to be less than the amounts required to
lactation. Even the breast milk of well-nourished women meet the iron requirements of infants ages 6 to 11 months,
does not contain sufficient iron and zinc to meet an pointing to the need for young children to receive iron-
infant’s requirements after the first 6 months of life, so fortified foods or iron supplements.
that after this age additional intake from micronutrient-
rich or -fortified complementary foods or supplements is ADEQUACY OF ENERGY INTAKE
required (5). However, commonly breast-feeding ends
too early and breast milk is substituted by complementary In places with food shortages, there is clearly a risk of
food of inadequate quality. inadequate energy intake and low weight-for-height
(wasting). Usually the adequacy of energy intake per
PERIOD OF COMPLEMENTARY FEEDING se is difficult to determine because a low intake of many
other nutrients will occur if food intake is inadequate.
During the transition from breast-feeding to comp- Interpretation of energy intervention trials is also often
lementary feeding, breast-feeding should be continued difficult because supplemental energy can displace the
while gradually adding complementary foods. Because usual diet. Using a more sophisticated experimental
the intake of breast milk falls with age, it is evident design, Krahenbuhl et al. compared the effects of a
that the amount and percent of nutrients required high-fat versus a high-carbohydrate energy supplement
from complementary foods increase with age. By 9 to against a nonintervention placebo group in rural
11 months old, the average breast-fed baby in low- Gambian children with stunting (9). The supplemented
income countries needs to obtain about 50% to 90% of children, ages 68 21 months, were provided with a
its vitamin and mineral requirements from complemen- high-fat or a high-carbohydrate biscuit for 12 months.
tary foods (7). The energy intake of the child depends on They were moderately stunted and wasted at the start of
the number and energy density of meals. It has been the intervention. Their usual diet was low in fat (17% of
estimated that at 1 to 2 years old, assuming the average energy) but adequate in protein (11%). Energy intake was
amount of breast milk that is consumed at this age in low- only 80% of that recommended, but adequate on a per
income countries, if two complementary feeds are given kilogram body weight basis. The high-fat biscuit
daily, then the energy density of the meals needs to be increased energy intake by 1551 kJ (378 kcal), and the
at least 1.5 kcal/g; for 3 meals per day it needs to be high-carbohydrate biscuit increased energy intake by
1.0 kcal/g and for 4 meals, 0.74 kcal/g (8). Children more 1659 kJ (404 kcal). In spite of these substantial increases
than 8 months old probably need about 3 meals per day. in energy intake, the supplements had no effect on growth
To evaluate how well nutrient requirements are met by in length or weight or on resting metabolic rate. The high-
complementary feeding in developing countries, food fat biscuit produced a small increase in fatness. Interest-
intake data were analyzed from Guatemala City, Bangla- ingly, weight gain during the 3-month harvest season was
desh and Malawi (8). The analysis revealed that families about 3 to 10 times as much as it was during the other
can prepare complementary foods that have an adequate seasons, perhaps indicating the importance of the other
energy density, and can feed them often enough to meet nutrients in food.
their childrens’ energy needs, but about one third of the
children in the different countries were given meals with DIETARY DIVERSITY
insufficient energy density for the number of meals
provided. Moreover, the amounts of food consumed by Dietary diversity can be defined as the number of foods
the children were much less than their gastric capacity. or food groups consumed in a defined period, such as
Intakes of energy (when expressed per kilogram of body 1 day or 1 week. Using Demographic and Health Survey
weight), protein and fat were adequate. However, the data from 11 countries, Arimond and Ruel compared the
intake of many micronutrients was inadequate, especially prevalence of stunting to diet diversity in children ages
the B vitamins, iron, zinc, calcium (if dairy product 6 to 23 months (10). Dietary diversity was a 7-point score
intake is low), and vitamin A (in Bangladesh). In fact, based on the number of groups of nutritionally important
the authors concluded that it would be difficult for these foods/food groups that the child had consumed on
children to meet their recommended micronutrient 3 days in the previous week; starchy staples, legumes,
intakes from food, and iron and zinc needs would be dairy products, other ASF, vitamin A–rich fruits and

S10 ALLEN
vegetables, other fruits and vegetables, and foods made adequacy of the diet is limited until intake is greater
with oil, fat or butter. After adjusting for the age of the than a minimal amount. Also, it was apparent that
child, maternal height and body mass index, the number increasing dietary diversity is especially important in
of children in the household <5 years old and 2 health cases in which the usual intake of ASF is low. It should
and welfare factor scores, there remained a significant be noted, however, that even the small amounts of ASF
correlation between dietary diversity and the prevalence usually consumed by children in developing countries
of stunting in all but 1 of the countries. have been reported to make a positive difference to
mental and motor function (16,17). The usual intake
IMPORTANCE OF ASF of ASF by Kenyan preschoolers 18 to 30 months old
was the main predictor of their subsequent cognitive
In most developing countries, the intake of ASF is too scores at age 5 years (18).
low to provide the population with sufficient amounts of
nutrients such as vitamin B12, bioavailable iron and zinc, INTERVENTIONS WITH ASF
riboflavin and calcium. For example, ASF provide <5%
of total dietary energy in many sub-Saharan countries, A review of the efficacy of various interventions for
5% to 10% in most other African countries and southern improving child growth elicited the following con-
Asia, 10% to 15% in most of eastern and northern Asia clusions (19). Energy supplements tend to increase body
and >20% in wealthier regions such as the United States weight but not length. Protein supplements provide little
and Europe. benefit to improve growth. In contrast, supplements
The ASF intake of preschoolers tends to parallel the containing dried skim milk as at least 1 component
general availability of milk, eggs and meat for the improved the growth of children in 12 of 15 trials. When
population. About 10 years ago, a multicountry study families of Dutch macrobiotic preschoolers increased
of preschoolers 18 to 30 months old in Egypt, Mexico and their children’s intake of milk or fish, their linear growth
Kenya showed that children in all 3 countries consumed improved more than those of the other macrobiotic
about 66 kcal/d in dairy products, but that meat plus egg children (20). In contrast, adding dry fish to complemen-
intake provided 85 kcal/d in Egypt, 60 kcal/d in Mexico tary foods did not affect the growth of infants ages 6 to
and only 6 kcal/d in Kenya (11). These low intakes of 12 months in Ghana (21).
ASF were accompanied by low intakes of vitamins (12) The benefits of adding supplemental meat to Kenyan
and minerals (13) but not protein (14) and a high preva- children’s diets have been tested in a recent study and
lence of micronutrient deficiencies. compared with those of adding milk (22). On a per-
More recently the investigators in the Kenya project kilocalorie basis, meat tends to be higher in available iron
returned to the same location to assess the effects and zinc and vitamin B12 than does milk, whereas the
of increasing ASF intake of schoolchildren ages 7 to latter contains more riboflavin, folate and calcium.
12 years in the same communities. The children’s diets Details of the study design and results have been pro-
had not improved, and they consumed only an average of vided elsewhere (22,23). Basically, the children, ages 7 to
12 kcal/d from meat and 52 kcal/d from milk; most of the 12 years, were given 1 of 3 types of snacks daily in school
energy was from maize and beans. Using food intake data while school was in session for 2 years. The 3 equicaloric
from this study, we asked the question whether the intake groups were: an ‘‘energy’’ supplement in the form of
of specific food groups or the overall diversity of the diets 250 kcal as the traditional food githeri, primarily maize
was the strongest predictor of the micronutrient adequacy and beans, plus oil; a meat supplement (ie, githeri plus
of the children’s diets (15). The outcome variable was the 60–80 g of ground beef); or a milk supplement (ie,
mean probability that a child would consume his or her githeri plus 1 cup of milk). Households in a noninter-
estimated adequate requirement for 15 micronutrients. vention control group received a goat at the end of the
The analyses revealed that the average number of food study. In general the meat supplement produced greater
groups consumed daily was associated with a gradual improvements in cognitive function assessed using
increase in micronutrient adequacy across the range Raven’s progressive matrices and arithmetic scores,
examined, from 2 to 7 groups per day. However, increas- resulted in the highest levels of physical activity, caused
ing the number of servings of ASF from 0 to 3/d had the biggest increase in initiative and leadership behavior,
only a small impact on micronutrient intake at baseline and provided the largest increment in muscle mass
because the usual intake of ASF was so low, only 17 g/d. (22,24–26). The latter may have been the cause or the
When ASF intake was increased to 52 g/d on average by result of the greater physical activity. Milk supplement-
supplements of meat or milk, the incremental benefits of ation significantly increased the growth of the shorter
increasing intake from 0 to 3 servings per day was much children.
greater. Thus, it was concluded that ASF certainly Vitamin B12 is found only in ASF and the high global
improve childrens’ abilities to meet their micronutrient prevalence of this vitamin deficiency is becoming recog-
requirements, but that their impact on micronutrient nized (27,28). At baseline, 69% of the children had a

CAUSES OF NUTRITION-RELATED PUBLIC HEALTH PROBLEMS OF PRESCHOOL CHILDREN S11
deficient or marginal plasma cobalamin concentration, and 2. De Pee S, Bloem MW, Sari M, et al. The high prevalence of low
the latter was significantly correlated with the usual total hemoglobin concentration among Indonesian infants aged 3–5
intake of ASF (r ¼ 0.308), or of meat, eggs or milk. months is related to maternal anemia. J Nutr 2002;132:2215–21.
3. Allen LH. Vitamin B12 metabolism and status during pregnancy,
Children in the lowest tertile of ASF consumption had a lactation and infancy. Adv Exp Med Biol 1994;352:173–86.
6.3 times greater risk of having a deficient or marginal 4. Allen LH. Impact of vitamin B-12 deficiency during lactation on
plasma cobalamin concentration, even though usual maternal and infant health. Adv Exp Med Biol 2002;503:57–67.
intakes of ASF were very low (E. McLean, MD, and 5. Allen LH, Graham JM. Assuring micronutrient adequacy
in the diets of young infants. In: Micronutrient Deficiencies
colleagues, unpublished data). Both the meat and milk in the First Six Months of Life. Edited by Delange FM, West
supplements significantly reduced the prevalence of vita- KPH. Basel: Vevey/S. Karger AG; 2003: pp. 55–88.
min B12 deficiency, with the meat increasing the plasma 6. Jones KM, Ramirez-Zea M, Zuleta C, et al. Highly prevalent
cobalamin concentration by 200 pg/mL and the meat vitamin B-12 deficiency in Guatemalan infants aged 12 months
increasing it by 125 pg/mL at the end of the study. is predicted by maternal B-12 deficiency and infant diet. J Nutr (In
press).
In many resource-limited households, it still may be 7. Brown KH, Dewey KG, Allen LH. Complementary Feeding of
possible to provide young children with larger amounts of Young Children in Developing Countries: A Review of Current
ASF than they are receiving. Caregivers often need to be Scientific Knowledge Geneva: World Health Organization; 1998.
taught about the importance of these foods for the nutri- 8. Brown K, Peerson J, Kimmons J, et al. Options for achieving
adequate intake from home-prepared complementary foods in
tion of children and their mothers. Dairy products or fish low income countries. In: Public Health Issues in Infant and Child
may be more affordable than meat in some locations, and Nutrition. Edited by Black R, Michaelsen K. Philadelphia: Lippin-
cheaper types of meat including concentrated nutrient cott Williams & Wilkins; 2002: pp. 239–56.
sources such as liver could be targeted in small amounts 9. Krahenbuhl JD, Schutz Y, Jequier E. High fat versus high carbohy-
to children and mixed with beans, fruits or cereal staples. drate nutritional supplementation: a one year trial in stunted rural
Gambian children. Eur J Clin Nutr 1998;52:213–22.
Tougher meats may need grinding or chopping to encou- 10. Arimond M, Ruel MT. Dietary diversity is associated with child
rage younger children to consume them. nutritional status: evidence from 11 demographic and health sur-
veys. J Nutr 2004;134:2579–85.
11. Allen LH. Malnutrition and human function: a comparison of
CONCLUSIONS conclusions from the INCAP and nutrition CRSP studies. J Nutr
1995;125:1119S–26S.
When addressing the role of inadequate diet as a cause 12. Calloway DH, Murphy SP, Beaton GH, et al. Estimated vitamin
of malnutrition in preschool children, it is important to intakes of toddlers: predicted prevalence of inadequacy in village
populations in Egypt, Kenya, and Mexico. Am J Clin Nutr
recognize that many children in developing countries will 1993;58:376–84.
already be nutritionally depleted by the end of the first 13. Murphy SP, Beaton GH, Calloway DH. Estimated mineral intakes
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mothers. During the period of transition to complemen- tions in Egypt, Kenya, and Mexico. Am J Clin Nutr 1992;56:565–
tary feeding, energy deficiency may occur if food is short 72.
14. Beaton GH, Calloway D, Murphy SP. Estimated protein intakes of
or if the energy density of the diet is low and not toddlers: predicted prevalence of inadequate intakes in village
compensated for by an adequate number of meals. How- populations in Egypt, Kenya, and Mexico. Am J Clin Nutr
ever, energy supplements generally tend to slightly 1992;55:902–11.
increase weight but not height, even where there is 15. Ruel ME, Graham JM, Murphy SP, et al. Validating simple in-
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The development community needs to appreciate the does it affect human function? Nutr Rev 1993;51:255–67.
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21. Lartey A, Manu A, Brown KH, et al. A randomized, community-
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birthweight infant. Arch Dis Child 1990;65:559. 391–404.

S12 ALLEN
22. Neumann CG, Bwibo NO, Murphy SP, et al. Animal source foods 26. Sigman M, Whaley SE, Neumann CG, et al. Diet quality affects the
improve dietary quality, micronutrient status, growth and cognitive playground activities of Kenyan children. Food Nutr Bull
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23. Murphy SP, Gewa C, Liang LJ, et al. School snacks containing 2004;62:S29–34.
animal source foods improve dietary quality for children in rural 28. Stabler SP, Allen RH. Vitamin B12 deficiency as a worldwide
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intervention on the cognitive development of Kenyan school foods. J Nutr 2003;133:3932S–5.
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children. J Nutr 2003;133:3957S–64S. 3875S–8.

Effect of Infections and Environmental Factors on Growth and

Nutritional Status in Developing Countries
Zulfiqar Ahmed Bhutta
Department of Paediatrics and Child Health, The Aga Khan University and Medical Center, Karachi, Pakistan
ABSTRACT
Despite numerous advances and improvements in child health effect of the infection itself on micronutrient status indicators.
globally, malnutrition remains a major problem and underlies a Recently the association of increased micronutrient losses such
significant proportion of child deaths. A large proportion of the as those of zinc and copper with acute diarrhea has been
hidden burden of malnutrition is represented by widespread recognized and a net negative balance of zinc has been shown
single and multiple micronutrient deficiencies. A number of in zinc metabolic studies in children with persistent diarrhea. It
factors may influence micronutrient deficiencies in developing is also recognized that children with shigellosis can lose a
countries, including poor body stores at birth, dietary significant amount of vitamin A in the urine, thus further
deficiencies and high intake of inhibitors of absorption such
aggravating preexisting subclinical vitamin A deficiency. Given
as phytates and increased losses from the body. Although the
effects of poor intake and increased micronutrient demands are the epidemiological association between micronutrient
well described, the potential effects of acute and chronic deficiencies and diarrhea, supplementation strategies in ende-
infections on the body’s micronutrient status are less well mic areas are logical. The growing body of evidence on the key
appreciated. Even more obscure is the potential effect of role of zinc supplementation in accelerating recovery from
immunostimulation and intercurrent infections on the micro- diarrheal illnesses in developing countries supports its use in
nutrient distribution and homeostasis. The association therefore public health strategies. JPGN 43:S13–S21, 2006. Key Words:
of relatively higher rates of micronutrient deficiencies with Infections—Micronutrient deficiencies—Zinc—Diarrhea—
infectious diseases may be reflective of both increased predis- Protein diversion—Amino acids. # 2006 Lippincott
position to infections in deficient populations as well as a direct Williams & Wilkins
INTRODUCTION global burden of malnutrition because a large pro-

portion of the hidden burden of malnutrition is
Despite numerous advances and improvements in represented by widespread single and multiple micro-
child health globally, malnutrition remains a major nutrient deficiencies.
problem, and in many parts of the world the situation The relationship between micronutrient deficiencies
seems to have worsened (1,2). In a recent estimation of such as vitamin A deficiency and increased risk of
approximately 10 million global under the age of childhood infections and mortality is well established
5 child deaths, malnutrition was estimated to underlie (6). Vitamin A supplementation is now recognized as an
almost half of such deaths (3). A large proportion of important public health intervention among young chil-
cases of malnutrition occur in the south Asia region dren in areas of endemic vitamin A deficiency. Other
(3), which also harbours almost three fourths of the micronutrient deficiencies such as zinc and iron
global burden of low birth weight (LBW) infants (4). In deficiency are also recognized as widespread in devel-
other parts of the world, high rates of HIV threaten to oping countries and associated with increased risk of
reverse all of the gains made by child survival pro- morbidity (7) and mortality (8).
grams, with malnutrition worsening (5). Such overt Although the effect of micronutrient deficiencies on
forms of malnutrition, however, do not reflect the true immunity and burden of infections in developing
countries is well documented, relatively little is known
about the impact of infections on micronutrient status and
Address correspondence and reprint requests to Zulfiqar Ahmed
Bhutta, Department of Paediatrics & Child Health, The Aga Khan
their subsequent impact on health outcomes. This article
University, PO Box 3500, Stadium Road, Karachi 74800, Pakistan focuses on the mechanisms and effect of infections on
(E-mail: zulfiqar.bhutta@aku.edu). nutrition status and growth in children.
S13
S14 BHUTTA
BIOLOGICAL PLAUSIBILITY OF THE EFFECT intake (24). Rotavirus diarrhoea appears to be associated
OF INFECTIONS ON GROWTH with more marked and prolonged nitrogen losses than
shigella or Escherichia coli infections (24). The energy
The association of recurrent infections on nutrition and cost of nitrogen losses during acute illness has been
growth during childhood is well described. The classic estimated at 5 to 7 energy units/kg/d (25).
studies in rural Guatemala by Scrimshaw et al. (9–15) Chronic diarrhoea, intestinal parasitism, and protein-
established the important relationship among infections, losing enteropathy are associated with sustained loss of
nutrition and growth. This relationship was also vividly protein through the gastrointestinal tract. It has been
described by Mata et al. (16,17) in follow-up studies that estimated that a moderate degree of intestinal hookworm
demonstrated the relationship of recurrent infections parasitation may cause an average loss of 100 energy
with growth failure. The recognition of the synergistic units/d (26). In particular, protein losses and impaired
relationship between nutrition and infection influences absorption may be both marked and sustained in persist-
most public health interventions to prevent malnutrition. ent diarrhoea (27), and the effect on protein metabolism
All infections, irrespective of the degree of severity, can be compounded by coexisting malnutrition and
decrease nutrient intakes and increase nutrient losses. micronutrient deficiency.
The nutrient losses include decreased intestinal absorp- The effects of subclinical gastrointestinal infections
tion, direct loss of nutrients in the gut through increased may be manifest by an increase in intestinal permeability,
secretion, internal diversion for metabolic responses to which may reflect subclinical intestinal inflammation
infection and increased basal metabolic rate when fever is and alteration in barrier function. This increase in intes-
present. In this way, infection influences not only protein tinal permeability has been shown to be associated with
and energy status but also that of most other nutrients. growth faltering in Gambian children (28,29). Although
The clinical importance of these consequences of infec- such growth failure may be a result of overt gastrointes-
tion depends on the prior state of the individual, the tinal infections, in recent years there has been much
nature and duration of the infection and the diet of interest in subclinical infections, especially those occur-
the individual during the infection, particularly dietary ring in early infancy. Helicobacter pylori infections are
intake during the convalescent period and whether full ubiquitous and have been shown to affect young infants
recovery takes place before another infection occurs. The and children in diverse settings in Africa (30) and Asia
principal mechanisms of effect of infections on growth (31). Altered intestinal permeability and gut barrier
include anorexia and poor intake, protein and energy function may lead to subclinical bacterial translocation
losses (eg, in diarrhoea and fever), impact on micronu- and bacteremia, causing increased mortality in malnour-
trient status, and effects of catabolism during infection ished children (32), and these have also been associated
and protein diversion on growth. with cytokine release from other intestinal bacterial
infections (33–36). In other instances chronic viral infec-
Anorexia and Poor Intake tion such as with HIV may be associated with systemic
immune activation and wasting (37), as well as increased
Many infections are associated with increased pro- losses from the gastrointestinal tract.
duction of inflammatory cytokines that may directly affect
appetite (18,19). In a study of malnourished children in Impact on Micronutrient Status
Goncalves Dias, Brazil, Schorling et al. (20) observed an
ablation of catch-up growth with progressively increasing A number of factors may influence micronutrient
diarrhoeal burdens. In addition, many parents themselves deficiencies in developing countries, including poor body
reduce dietary intake during or after infections such as stores at birth as a consequence of maternal intrauterine
diarrhoea, thereby compounding the impact on nutrient malnutrition, dietary deficiencies and high intake of
intakes (21). inhibitors of absorption such as phytates and increased
losses from the body. To illustrate, in the case of iron
Protein and Energy Losses deficiency, in addition to poor dietary intake and inhibi-
tors of absorption (38), increased intestinal losses follow-
Even subclinical gastrointestinal infections and ing parasitic infestation may also be an important cause
increased secretion are associated with direct nutrient of iron deficiency anaemia (39). Overall, although the
losses from the body. These losses may include both effects of poor intake and increased micronutrient
protein (22) and substantial losses of micronutrients such demands are well described, the potential effects of acute
as zinc and vitamin A from the intestine or urinary tract and chronic infections on the body’s micronutrient status
(23). Faecal nitrogen losses may contribute significantly is less well appreciated. Even more obscure is the poten-
to the negative nitrogen balance in children with acute tial effect of immunostimulation and intercurrent infec-
diarrhoea. Nitrogen malabsorption may be substantial tions on the micronutrient distribution and homeostasis.
during acute diarrhoea, ranging from 40% to 75% of There is little information on the short-term compartment

INFECTIONS AND GROWTH IN DEVELOPING COUNTRIES S15
changes of micronutrients such as iron, zinc and vitamin It is also recognized that children with shigellosis can
A. However, other mechanisms underlying net body lose a significant amount of vitamin A in the urine, thus
losses and homeostasis are well described. It is possible further aggravating preexisting subclinical vitamin A
to elucidate the mechanism of alteration in micronutrient deficiency (42). As already illustrated, the risk of micro-
status and consequent deficiency from other direct nutrient deficiency in infancy and early childhood can be
studies and observations. compounded severalfold by the presence of low body
The gut plays a special role in the pathogenesis and stores from birth as in low birth weight infants, and
severity of micronutrient deficiencies. The association of further aggravated by poor breast feeding and comp-
helminthic infections, especially hookworms, with iron lementary feeding practices (43).
deficiency in young children is well established and
largely relates to direct intestinal losses (40). Although Effects of Catabolism during Infection and Protein
the association between diarrhoeal disease control pro- Diversion on Growth
grams and malnutrition or growth rates has been ques-
tioned, in many parts of the world there is a close This is one of the most important mechanisms that
relationship between the two. In particular, prolonged may underlie the growth failure seen in children
and recurrent episodes of diarrhoea, frequently in associ- with infections. Subclinical infection with possible
ation with HIV infection, are a frequent cause of mor- immunostimulation has been hypothesized as a possible
bidity and micronutrient deficiency. In recent years the mechanism for growth failure and stunting in children
association of increased micronutrient losses such as from developing countries, where poor environmental
those of zinc and copper with acute diarrhoea has been hygiene and exposure to a high burden of infections are
well recognized (41). These findings may explain the ubiquitous (44). It has long been recognized that acci-
high rates of subclinical zinc deficiency among children dental injury, surgical trauma and infection lead to a
with frequent and recurrent bouts of diarrhoea, and may significant loss of body nitrogen (45). Although the
be particularly marked among children with persistent anorexia that often accompanies these insults will in
diarrhoea. itself lead to negative nitrogen balance, the nitrogen
TABLE 1. Gross amino acid composition of positive acute-phase reactant proteins and skeletal muscle protein with estimated amino
acid
Muscle Excess release,
a1-acid a1- Acute-phase protein mg
Amino acid C-reactive Fibrinogen Glycoprotein Antitrypsin Haptoglobin Amyloid A SMP response equivalent
Amino
acid Nitrogen
Leucine 91y 62 101 124 82 29 80 89 1090 72 8

Isoleucine 54 32 48 49 47 29 48 54 1120 41 4
Valine 77 48 46 59 84 8 54 67 1240 40 5
Lysine 71 77 75 92 92 33 98 90 920 104 20
Histidine 16 27 17 37 38 35 51 33 640 68 11
Phenylalanine 105 46 64 83 30 103 40 79 1980 0 0
Tyrosine 50 56 74 27 70 67 36 55 1530 16 1
Tryptophan 42 35 30 11 32 45 13 24 1850 2 <1
Methionine 16 32 11 28 16 22 25 23 910 26 2
Cysteine 13 15 18 6 24 0 13 14 1080 12 1
Arginine 36 84 52 23 28 116 69 54 780 83 28
Proline 44 48 34 41 44 34 48 50 1320 25 3
Glycine 46 59 19 33 44 61 45 50 1110 39 7
Serine 84 91 31 49 40 47 41 70 1700 11 1
Alanine 31 29 36 43 54 106 59 51 860 66 10
ASXz 82 113 102 106 113 128 92 121 1320 61 12
GLXz 112 119 173 136 115 87 145 147 1010 140 15
Threonine 58 60 74 66 54 30 47 65 1380 28 4

Gross amino acid composition of positive acute-phase reactant proteins and skeletal muscle protein with estimated amino acid needs to support a
‘‘typical’’ (assuming that the ‘‘typical’’ acute-phase response consists of an increase [mg/kg] of C-reactive protein [250], fibrinogen [200], a1-acid
glycoprotein [50], a 1-antitrypsin [200], haptoglobin [50], or amyloid A [100]) acute-phase protein response expressed in absolute terms (mg amino
acid/kg body weight/d) or in terms of muscle protein equivalent (mg muscle protein/kg body weight), together with an estimate of the excess amino
nitrogen release. Adapted from References (50,51).
y
Values are expressed as grams of amino acid per kilograms of protein and adjusted for water of hydrolysis.
z
ASX ¼ aspartate þ asparagines; GLX ¼ glutamate þ glutamine.

S16 BHUTTA
loss (220 mg/kg/d) (45,46) exceeds even that which is

expected under fasting conditions. Given the dominating
influence of muscle mass protein pool on whole-body
protein, it is expected that much of the nitrogen mobilized
during acute need derives from the skeletal muscle
protein mass. However, following infection or injury,
mechanisms are activated that lead to depletion of muscle
protein. These changes are presumably induced by the
combined actions of the cytokines (eg, interleukin-1,
tumour necrosis factor-a) and stress hormones (eg, the
glucocorticoids, glucagons, epinephrine).
Recent advances in stable isotope techniques have
allowed measurements of protein synthesis and losses FIG. 2. Effect of vaccination on protein kinetics.
in a variety of physiological states (47–49). These studies
indicate that subclinical and acute infections accelerate
control of bone elongation by protein availability. Other
protein catabolism and diversion to the production of
studies (53) showed that bone growth continued at
acute phase proteins. Reeds et al. (50,51) have estimated
reduced but substantial rates even when dietary energy
the approximate amino acid composition of various
intake was reduced by 50%, as long as protein intake
acute-phase proteins and the protein or amino acid
remained constant. The ability of dietary protein to
‘‘cost’’ of a typical acute-phase response (Table 1). In
increase growth, particularly during periods of catch-
a study of children (ages 6–24 months) with persistent
up growth after illness is well recognized (54,55). The
diarrhoea we estimated whole-body protein kinetics
amino acid composition of dietary proteins has a direct
using 15N-glycine and indicated that despite adequate
effect on growth by determining the supply of essential
nutrient intake, most children with subclinical infections
amino acids at the cellular level. Protein synthesis
were in negative protein balance (Fig. 1). In a subsequent
requires the presence of each component amino acid at
phase following nutritional rehabilitation and treatment
the time of chain elongation. Thus, a dietary protein
of infection, these children were exposed to a vaccine
intake deficient in 1 essential amino acids will not
challenge. Evaluation of protein kinetics indicated that
be able to sustain protein synthesis. Many vegetable
the immunostimulation was associated with a phase of
proteins have 1 limiting amino acids (eg, with levels
negative protein balance (Fig. 2). These studies indicate
below those in high-quality reference proteins such as
that in many children with subclinical infections and
egg or milk).
immunostimulation, a limiting factor may be amino acid
Among the adaptive changes in plasma amino acid
and protein intakes during rehabilitation.
concentrations with malnutrition are a temporary
increase in the levels of branched-chain amino acids,
Amino Acid Supply, Growth and Implications an increase in glycine levels, and a fall in alanine
for Therapy concentration (56). This specific and early effect on
branched-chain amino acids is an indication that these
The role of dietary protein as a determinant of
are among the first to become limiting for protein syn-
growth is well recognized. Millward (52) proposed a
thesis in malnourished children. The presence of inter-
protein-driven regulatory mechanism, centered on the
mediary metabolites of histidine and tyrosine in the urine
of malnourished children (57) suggests a widespread
impairment of enzyme activity. It must be emphasized
that the plasma amino acid profile in most malnourished
children also reflects the superimposed effects of infec-
tion and anorexia. In the well-nourished host, infection
episodes trigger a cascade of adaptive responses, aimed at
enhancing immune competence and preserving vital
cellular activities and preventing colonization of the
infective agent. The role of cytokines as mediators of
systemic responses to infection has become clearer
during the past decade (58). Although the precise mol-
ecular mechanisms are unclear, the cellular biology of
tumour necrosis factor suggests a role in promoting the
transfer of amino acids from peripheral tissues to liver for
FIG. 1. Effect of coincidental infection on protein metabolism. use in acute-phase protein synthesis and gluconeogenesis

(59). It is important to emphasize that this cytokine- ameliorate the nutritional penalty of infections. These
induced catabolic state cannot be overcome merely by can be broadly classified as follows.
enhancing substrate availability.
As indicated above, acute infection has a major nega- Preventive Strategies
tive impact on nitrogen balance. Studies by Biesel (60)
showed that the infection process was responsible for The major environmental penalty of poverty is
higher nitrogen losses than could be accounted for by a increased burden of infections, and clearly this must
decreased protein intake. This specific effect of infection be a long-term goal for most developing countries.
varied depending on the etiological agent and on the The reality of global inequity and poverty, however, is
initial nutritional status of the host. In the relatively well- totally different in many parts of the world, especially
nourished host, mild infection was associated with an sub-Saharan Africa, which has slid down the poverty
increased protein turnover (61), although the modest rise ladder. Thus, there is continued interest in intervention
in protein synthesis could be negated by the associated strategies to accelerate the reduction in childhood diar-
marked increase in the rate of protein breakdown (62,63). rhoea and acute respiratory infections.
The host response to infection requires the rapid syn- It has been shown that targeted education strategies do
thesis of immune proteins. The catabolic response to have an impact on reducing diarrhoea burdens and
infection leading to breakdown of skeletal muscle protein improving breast-feeding practices (70,71). In addition,
and release of free amino acids into the bloodstream interventions focused on improving the supply of safe
provides most of the extra amino acids needed to mount water through filters (72,73), chlorination (74) or other
that response. Although the impact of protein deficiency strategies (75) have been shown to have a significant
on altering the acute-phase response is well recognized impact on diarrhoea rates. Community education and
(64), the precise amino acid requirements to mount this hand washing strategies through promotion of the use
immune response have been the subject of speculation. of soap have been shown to reduce rates of diarrhoea and
The issue is particularly important for developing acute respiratory infections in community-cluster
countries, where childhood infections are common and randomized trials (76–78), indicating the benefit of
the cumulative burden that these episodes can have on incremental strategies for community behaviour change.
amino acids requirements of the small child is substantial Although these studies are important and systematic
(65). reviews (79) support the benefit of hand washing and soap,
Table 2 indicates the alterations in plasma amino acid the reality is that this is an expensive intervention that is
profiles in response to short-term dietary alterations, difficult to roll out and sustain. As a recent analysis (80) of
malnutrition or infection (66,67). These complex changes the global costs for child survival interventions indicates,
do not provide much help in understanding the dynamics we are currently spending almost $2 billion on safe water
of protein metabolism in malnourished infected indivi- and sanitation in developing countries, yet the intervention
duals. Preliminary animal data suggest that it is possible does not reach those in greatest need. There is thus the
to modulate the endogenous production (68) as well as continued need for additional preventive strategies. Given
the metabolic response to tumour necrosis factor-a the close relationship between malnutrition and infections,
(69) by modifying the amino acid composition of the nutrition interventions are widely regarded as critical to
diet. public health programs.
Macronutrient Interventions
Intervention Strategies to Reduce the Nutritional
Impact of Infections Although the role of balanced energy-protein supple-
mentation for nutritional rehabilitation is well described,
Given the above findings, it is important to ensure that the critical role of adequate protein intake in malnutrition
a wide variety of intervention strategies are employed to is also widely recognized (81,82). Although some regard
the absolute intake of protein as a more important factor
TABLE 2. Alterations in serum amino acid profile in various
(83), others have evaluated specific amino acids in
pathological states (66,67) malnourished children with infections (84,85) and found
them to be equally beneficial. Some of this uncertainty
Starvation Protein-free Infection Malnutrition stems from observations that during acute stress if infec-
tions some amino acids become conditionally essential
Valine " # # #
Leucine " # # # and that replenishing the need acute phase proteins would
Isoleucine " # # # result in breakdown of muscle protein (51). Manary et al
Phenylalanine — — " # (86,87) specifically demonstrated the benefits of using an
Alanine # " # # egg whites–based tryptophan source in infected severely
Glycine " " # #
malnourished children.

S18 BHUTTA
Micronutrient Interventions substantial benefits in growth, and this has been demon-
strated in several intervention studies (96,97).
In addition to the role of protein and amino acid intakes, The important contribution of some infections to
a number of epidemiological studies support the close aggravation of micronutrient deficiencies in at-risk popu-
association of infections with micronutrient deficiencies. lations cannot be ignored. Increased losses of micronu-
These include findings of lower serum concentrations of trients such as vitamin A and zinc during infectious
zinc with increasing burden and duration of diarrhoea (88), illnesses such as diarrhoea are important contributors
as well as lower serum concentrations in patients with HIV to micronutrient deficiencies. This may be particularly
infection (89). Although children with hypovitaminosis A marked with prolonged diarrhoea and dysentery and may
and low serum concentrations of vitamin A have higher lead to clinically significant deficits and overt micronu-
rates of associated infections, the specific contribution of trient deficiency.
infection to vitamin A deficiency cannot be discounted. Given that the epidemiological association between
The relationship between low serum vitamin A and sever- micronutrient deficiencies, such as zinc and diarrhoea, is
ity of disease has been observed with increasing severity of well established, supplementation strategies are logical in
HIV infection (90). Several infections are, however, endemic areas. The growing body of evidence on the key
directly associated with an increased risk of micronutrient role of zinc supplementation in accelerating recovery
deficiency. These include diseases such as measles, which from diarrhoeal illnesses in developing countries sup-
have been directly implicated in unmasking as well as ports its use in public health strategies in endemic areas
triggering vitamin A deficiency (91). The association of (98–100). The association of measles with overt and
relatively higher rates of micronutrient deficiencies with subclinical vitamin A deficiency also recognized that
infectious diseases may be reflective of both increased the administration of vitamin A to all such malnourished
predisposition to infections in deficient populations as well and at-risk children forms a cornerstone of such manage-
as a direct effect of the infection itself on the micronutrient ment strategies. Population-based micronutrient inter-
status indicators (92). Low serum concentrations of micro- ventions and targeted replenishing of critical nutrients
nutrients have been frequently described in subclinical that may become deficient during infective stress may
infections. These levels also appear to be lowest at the have significant public health benefits in developing
highest levels of inflammatory proteins. High serum con- countries.
centration of C-reactive protein and haptoglobin are
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Nutritional Deficiencies in Learning and Cognition

S. Yehuda, S. Rabinovitz, and yD.I. Mostofsky
Psychopharmacology Laboratory, Bar Ilan University, Ramat Gan, Israel, and {Department of Psychology,
Boston University, Boston, MA
ABSTRACT
The postinfancy period is crucial for normal brain development, performed in preschool children and offers a broader view of
providing subsequent optimal conditions for learning and cog- the relationships among nutrition, nutrients and cognition.
nition. Both iron deficiency and essential fatty acids deficiency JPGN 43:S22–S25, 2006. Key Words: Learning—Cognition—
may impair normal neurological development. This review Iron deficiency—Essential fatty acids deficiency. # 2006
examines the limited number of studies that have been Lippincott Williams & Wilkins
INTRODUCTION For example, depletion of the bioavailability of tyrosine

to the brain will halt the production of catecholamine
Many studies demonstrate the destructive effects of neurotransmitters. However, if the nutritional insult
malnutrition and nutrient deficiencies on learning and occurs in a ‘‘critical period,’’ the damage will no longer
cognition. Most studies examine specific periods of be temporary but rather have long-term consequences.
development (eg, prenatal, infancy and school age or Many studies tend to concentrate on nutritional
aging) while neglecting the postinfancy period, in which deficiencies during the early infancy period when many
a number of nutritional deficiencies including but not accelerated developmental events occur. It was recently
limited to choline, selenium, zinc, folate, vitamin B12 and concluded that while the brain undergoes rapid develop-
iodine, have been shown to interfere with normal devel- ment during infancy, the maturation of the brain is not yet
opment and cognition (1). completed. Maturation of areas of the brain is not
The most commonly studied deficiencies in children uniform, and different areas mature at different ages. It
are protein-energy malnutrition, including Kwashiorkor seems that the areas of the brain that mediate cognitive
and marasmus, iron deficiency and essential fatty acids function mature last. There are several indicators for
deficiency. The aim of this review is to examine the brain maturation, such as synaptogenesis, myelin for-
limited studies that have been performed on children of mation and dendrite formation (2,3). Several techniques,
this age, and to offer a broader view of the relationships such as the PET scan or magnetic resonance imaging (4),
among nutrition, nutrients and cognition. demonstrate brain development well into the preschool
period, and the glucose utilization test shows a higher rate
RELATIONSHIP OF NUTRITIONAL of brain glucose metabolism in the postinfancy period
DEFICIENCY TO THE TIMING OF BRAIN than during adulthood (5). The 2 brain areas that mediate
DEVELOPMENT most of the cognitive functions, the frontal and prefrontal
cortex and the hippocampus, mature during postinfancy
Malnutrition, undernutrition, and nutrient imbalance or later. Several investigations have correlated the
may affect learning and memory by modifying or inter- appearance of different types of cognition and memory
fering with brain physiology or with brain structure. Two with the rate of maturation of specific brain areas (6).
conditions of nutritional insults may prevail: temporary Some researchers estimate that the frontal cortex finally
damage (which lasts only as long as the nutritional matures at age 10. Insults to the process of the synapto-
problem exists) includes short-term blockage in the genesis or to the rate of myelination induce severe delay
bioavailability of nutrients essential for a specific action. in development and maturation of brain areas, which
results in delayed cognitive development.
Address correspondence and reprint requests to Shlomo Yehuda,
The sensory system matures before the cognitive
Psychopharmacology Laboratory, Bar Ilan University, Ramat Gan system. Delay in maturity (eg, disturbance in the myelin
52900, Israel (e-mail: yehudas@mail.biu.ac.il). formation process) in the visual or auditory system,
S22
NUTRITIONAL DEFICIENCIES IN LEARNING AND COGNITION S23
severely impacts the cognitive system, where sensory- neurotransmitters. In contrast to infantile ID, which is
motor coordination is essential for normal cognitive hard to treat and has a long-term effect, ID that occurs
development. Even a correction of the nutritional deficit later in life is much easier to treat. Despite discussions of
may leave persistent long-term effects on the auditory ID-impaired learning or memory or motivation and con-
system. centration, the ultimate resulting condition is decreased
cognitive function (11,12). In our study with rehabilitated
Micronutrients Deficiency ID children we did not find any decrease in motivation or
concentration, but we did find a tendency toward lower
Protein energy malnutrition (PEM) is a state that IQ scores.
mainly affects infants as a result of energy restriction Nutritionally induced ID modifies other body systems
and a protein- and amino acid–deficient diet. Although in addition to the brain and its biochemistry. Modifi-
most children with PEM exhibit cognitive deficits, the cations of the endocrine system (an increased insulin
magnitude of the disorder among postinfancy children is sensitivity and a decreased thyroxin level) were reported.
not known. This syndrome is a combination of the effects Several aspects of the 2-way relationship between ID and
of undernutrition and a severe decrease in essential cell-mediated immunity have been described. On the one
enzymes and neurotransmitters. Other known nutritional hand, interleukin-1 (IL-1) induces ID; on the other hand,
disorders may be confounded by a history of energy our results showed that among ID rats the level of IL-1
restriction. (proinflammatory) is increased and the level of IL-2
(anti-inflammatory) is decreased (7). An increased level
Iodine of IL-1 and a decreased level of thyroxin leads to deficits
in the learning process and cognition. In addition, the
Iodine may be responsible for mental retardation and effects of ID on the immune system can explain the
can appear at any age, although it is most devastating finding that the rate of children with ID who are sick
when it occurs during infancy. The mechanism is clear: with infectious diseases is much higher than that for
iodine is required for the formation of thyroxin, which is non-ID children.
an essential nutrient for the brain. It is important to note another effect of ID, namely that
the bioavailability of molecules in the brain is highly
Iron dependent on proper function of the blood-brain barrier
(BBB). Although the neonate is born with an immature
Iron deficiency (ID) is the most prevalent nutritional BBB, the BBB matures quickly to protect the developing
disorder at all ages. There are many animal and human brain. We found that the pattern of penetration of several
studies describing the effects of ID and its effects on compounds into the brain of ID rats is different from that
dopamine and dopamine D2 receptors (7). Behaviorally, of the control rats (13). It is interesting to note that the
children with ID showed lethargy, irritability, apathy, ID state does not damage the BBB but rather induces
fatigue, inability to concentrate, pica, inattention and a specific changes in the penetration rate. One of the
decreased IQ. Some theories relate ID to attention-def- compounds that is able to cross the BBB in ID rats is
icit/hyperactivity disorder (ADHD). In animal studies, ID b-endorphin, which is unable to cross the BBB in normal
induces a delay in maturation of the frontal cortex, which rats. Here again, higher brain levels of b-endorphin are
may explain the cognitive deficits found in animal and associated with poor learning and memory.
human studies, and hippocampus, which may explain the
spatial cognitive decline (7,8). ESSENTIAL FATTY ACIDS DEFICIENCY
Recently the authors found that most of the neurologi-
cal reflexes (galabella, palmer grasp, planter grasp, pass- The activity of the brain is highly dependent on the
ive movement arm, passive leg movement, and Babinsky) integrity of the neuronal membrane (14,15). The neuro-
were severely delayed in ID/low ferritin premature nal membrane is composed mainly of proteins and lipids.
infants (9). The long-term effects of infancy ID has been The proteins in the membrane are relatively stable,
studied in a group of rehabilitated children. At ages 9 to whereas the lipids exhibit a fast turnover rate. Also, it
10 (with normal values of hemoglobin, iron and ferritin) should be remembered that the neuronal membrane, the
their IQ score was the same as non-ID infant children; myelin sheath, surrounds the membrane, and that the
however, their scores on subset tests that required spatial myelin is composed mainly of lipids.
cognition were significantly lower. In addition, in audi- The physical state of the neuronal membrane is critical
tory tests they exhibited statistical but not clinical delay for the neuronal functions. The ideal state is a gel state.
in processing auditory signals (10). One of the mechan- There are known molecules that are able to change the
isms that may explain these results is the interference of physical state of the membrane, for example, alcohol
ID in the normal rate of myelination. In addition, ID may fluidizes the membrane, whereas cholesterol hardens the
slow down the development and maturation of brain membrane. The change in the physical state of the

S24 YEHUDA ET AL.
neuronal membrane modifies some of the membrane learning performance (as assessed by the Morris Water
functions, including neuronal information along the axon Maze and passive avoidance), elevating pain threshold,
and neuronal information in the synapse. improving sleep and improving thermoregulation. This
Essential fatty acids (EFA) are essential for the devel- ratio was also able to correct learning deficits induced by
oping brain. It is outside the scope of this review to deal the neurotoxins AF64A and 5,7-dihydroxytryptamine
with the most important issue of EFA supplements to and by 6-OH-DA (ie, reduction in brain dopamine
baby formulas. EFA are involved in most of the aspects of level).
brain development and maintenance. They are major Our studies in animal models were not limited to an
components of myelin and are able to induce myelina- examination of memory disorders. The PUFA compound
tion, determining the index of membrane fluidity. EFA was effective in decreasing elevated cortisol levels in an
are also involved in neurotransmitters and the production experimental model of stress (18). The PUFA mixture
of peptides. In EFA deficiency (EFAD) states the mem- was also found to improve the status of an experimental
brane becomes much harder and cannot perform its rat model of multiple sclerosis and a decrease in the
functions. frequency of seizures in pentetrazol-treated rats. Ongoing
Whereas the brain uses linoleic (n-6) and a-linolenic clinical trials with patients with refractory seizure, using
(n-3) acids for many functions, their derivatives (ie, the a commercial fatty acid preparation, appear to confirm
longer chains of polyunsaturated fatty acids [PUFA]) are the success of seizure control that was observed in the
also important. The same enzymes that are responsible animal data (14).
for the elongation of the fatty acids act upon both families A question of major concern in pediatric neurology
of PUFA and compete with each other. Numerous studies relates to the establishment of the degree of nutritional
have confirmed that that the level of PUFA in the deficiencies that is able to induce behavioral disturb-
neuronal membrane is important, and recent studies have ances, even in the preschool period. In a recent survey the
shown that the types of PUFA and the ratio between n-3 authors found that a large percentage of children with
and n-6 PUFA are just as important. For example, the ADHD are iron deficient, EFAD, and some are both. We
ratio between the total PUFA and cholesterol level in the were unable to establish that the nutritional deficiency
membrane determines the membrane fluidity index. Not was the unequivocal cause of the behavioral disturb-
all ratios of PUFA are equally effective in decreasing the ances, or that because the children tend to be anorectic
level of cholesterol in the membrane. The ratio of 1:4 and consume large amounts of junk food, the nutritional
(n-3:n-6) was found to be the most effective in decreasing deficiencies are the results of the behavioral disturbance.
the cholesterol level in the membrane (14). However, recent studies showed that ID induces changes
The role of n-3 in various brain functions is facilitated in the index of membrane fluidity. In addition, children
greatly by diet-induced deficiency. Studies have shown with EFAD exhibited the same auditory changes as
that n-3-deficient rats exhibit poor learning and memory children with ID, and changes in the BBB functions
in a variety of tasks, including but not limited to Morris were found among EFAD rats.
Water Maze performance and olfactory-based learning in
addition to sensory deficits such as selected visual func- CONCLUSIONS
tions (16). In n-3 deficiency there is a significant decrease
in the neuron size in the hippocampus, hypothalamus The succinct message of this review is that the post-
and cortex, the areas of the brain that mediate spatial infancy or preschool period is not a quiet period in brain
and serial learning. In addition, n-3 deficiency induces development. Although it is true that no critical devel-
a significant reduction in cerebral catecholamines, in opments were identified in the postinfancy or preschool
glucose transport capacity and glucose utilization in periods, it is clear that the brain continues to develop and
the brain and in the rate of myelinization (17). Each of that any damage incurred during these periods may have
these variables can be responsible for learning deficits. long-term results. The critical brain areas that mediate
Clearly, the various fatty acids serve different roles in reasoning (prefrontal cortex) (19) and spatial learning
the nervous system and throughout the body’s machinery. (hippocampus) (20) do not reach maturation in this
It has been suggested that the nervous system has an period. Various types of learning such as sequential
absolute molecular species requirement for proper func- learning (21), spatial cognition (22) or inhibitory control
tion. Studies in our laboratory confirm this finding and (23) must wait until the brain area is ready to perform the
even suggest an added qualifying requirement (eg, the task. Nutritional deficiencies will delay these perform-
need for a proper ratio between the EFAs. Many studies ances for a long time (24,25).
examined the effects of various fatty acids on learning
and memory, but few examined the ratio between various Acknowledgments: The authors would like to thank the
PUFA. We tested a wide range of PUFA ratios and found Rose K. Ginsburg Chair for Research into Alzheimer’s Disease
that a mixture of linoleic (n-6) and a-linolenic acids (n-3) and the William Farber Center for Alzheimer Research for
with a ratio of 4:1 was the most effective in improving their support.

NUTRITIONAL DEFICIENCIES IN LEARNING AND COGNITION S25
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Prevention and Control of Obesity in Preschool Children:

Importance of Normative Standards
zRicardo Uauy, yJuanita Rojas, §Camila Corvalan, Lydia Lera, and Juliana Kain
Institutode Nutrición y Tecnologı́a de los Alimentos (INTA), University of Chile, Santiago, {Junta Nacional de Jardines Infantiles
(JUNJI), Santiago, {London School of Hygiene and Tropical Medicine, London, and §Rollins School of Public Health,
Emory University, Atlanta, GA
INTRODUCTION NORMATIVE GROWTH STANDARDS FOR

YOUNG CHILDREN
The combined objectives of promoting child growth
while preventing obesity are often not recognized as Reference Growth Standards to Define Normal
intertwined components of good nutrition; rather, they Weight, Height and Body Mass Index
are often considered to be opposite poles of the malnu-
trition spectrum. Providing complementary foods to young To assess normal growth we need an adequate refer-
children with the worthy objective of preventing malnu- ence of central tendency and variability in anthropo-
trition without considering the need to avoid obesity in metric indices. Because good health and nutrition are
stunted children may in fact do potential harm. Nutrition defined by the capacity to support normal growth, the
programs addressed at preventing malnutrition may have reference/standards used to assess growth are fundamen-
built-in mechanisms that can easily promote positive tal for both clinical practice and to establish public health
energy balance and thus increase risk for obesity. This recommendations. Thus, the definition of ‘‘normal’’
is particularly relevant when feeding underweight stunted growth is of paramount importance to secure the normal
children who may be of normal or even excessive weight health and nutrition of populations. Normative gender-
for stature. Thus, it is of the utmost importance to define and age-specific data of weight, height and body mass
what is normal weight and height and to apply normative index (BMI) are needed to define who is undernourished,
standards to assess growth and to establish energy intake normal, and obese. Anthropometry is only an indirect
recommendations that are consistent with good nutrition markerofbodycomposition(leanbodymassandfat stores),
and health during childhood and beyond (1). therefore, weight and length measurements serve only as
This manuscript examines recent advances in defining proxy markers for increased or reduced adipose tissue
norms to assess the growth of young children, the latest energy stores. Weight, height and weight/height and BMI
energy intake recommendations for children released by for age and sex have been used as indicators of nutritional
Food and Agriculture Organization/World Health adequacy in infancy, childhood and adolescence (2).
Organization/United Nations University (FAO/WHO/ Present growth charts are based on what is observed
UNU), the need to include obesity prevention in the growth for a normal reference population rather than
design and implementation of nutrition programs for recommended growth-based on health outcomes
children with a special emphasis in Latin America, and throughout the life course. The most commonly used
propose recommendations to prevent malnutrition from growth charts are based on the National Center for Health
energy deficit and excess in countries undergoing rapid Statistics ([US]NCHS), implying that children growing
epidemiological changes. in an affluent society in North America should be con-
sidered the standard of healthy growth. The NCHS
growth reference served as the basis for the present
Address correspondence and reprint requests to Prof Ricardo Uauy, WHO international growth standards for infants 0 to
Instituto de Nutricion (INTA), University of Chile, Casilla 138-11, 36 months, which was derived from children growing
Santiago, Chile. (e-mail: uauy@inta.cl).
We gratefully acknowledge the collaboration of the administrators
in an affluent rural society in the town of Yellow Springs,
and staff of the Junta Nacional de Jardines Infantiles (JUNJI) Chile that OH (3). The present WHO infant growth norm has major
allowed us to access the information and supported our efforts. flaws: it is derived from a nonrepresentative sample of
S26
NORMATIVE STANDARDS IN PREVENTION AND CONTROL OF OBESITY S27
the population and the data are drawn from a group of norms being used. Most important, this reference sets
predominantly formula-fed infants who received energy- the growth of the breast-fed infant as the normative
dense complementary foods. standard. Optimal infant feeding, as presently defined
The WHO/UNU growth standards released in by WHO, is exclusive breast-feeding for the first 6
May 2006 correspond to a representative sample of months of life, followed by continued breast-feeding
disease-free individuals in 6 sites around the globe. with adequate complementary foods for up to 2 years
The new Multicountry Growth Reference Standards and beyond. The issue of whether this standard should be
(MGRS) were developed based on the growth of infants applied to all children 0 to 5 y requires ample discussion,
who were predominantly breast-fed for 4 to 6 months and yet for most the breast-fed infant represents the gold
appropriate complementary foods after weaning (4). In standard for infant growth. The long-term consequences
fact, infants fed according to present WHO recommen- of this pattern of growth remain to be fully determined,
dations and living under conditions that favor the however. Existing national and international standards
achievement of genetic growth potential, grow less have defined normal growth based on the weight and
rapidly in weight than the present WHO/NCHS refer- length gain observed in apparently healthy children. This
ence, particularly after 4 to 6 months. Present distri- has led in practice to support the notion that ‘‘bigger is
butions of normal weight-for-age and weight-for length better.’’ This is a reasonable proposal if the objective is to
are skewed toward higher values, relative to those enhance survival in infancy and early childhood in areas
observed in predominantly breast-fed infants; this may where malnutrition and infection in synergy claim the
be a contributory factor to the increase in childhood lives of infants and young children. However, it is
obesity because normal children are being considered certainly not the case in countries where deaths of
underweight and are thus prescribed additional energy. young children are rare and the concern has shifted to
These drawbacks led a WHO Expert Committee in 1995 the prevention of obesity and related burden of chronic
to support the development of a new growth reference. disease (6). To make appropriate comparisons across
The multicountry (Brazil, Norway, India, Ghana, the US countries and to monitor trends in childhood overweight
and Oman) growth reference study, mentioned above, is prevalence it is crucial to have appropriate growth
specifically designed for this purpose; data collection standards and to agree on a clear definition of childhood
began in 1997 and was completed by 2003. Analysis of overweight and obesity. The former is available, at least
the data has been completed and new reference standards for children 0 to 5 y, but the latter remains a problem.
were released in May 2006. The study undertaken in
diverse geographical areas included population-based Reference Standards to Define Overweight and
samples of infants and children whose mothers were Obesity in Children
nonsmokers of middle to high income so that environ-
mental conditions were not restrictive and caregivers There is a lack of consistency in the use of the terms
followed the established WHO feeding recommen- overweight and obesity in children. The WHO Expert
dations. The research design combined a longitudinal Committee on Physical Anthropometry provided in
study from birth to 24 months of age of 300 newborns per 1995 a definition for overweight and recommended that
country, with a cross-sectional study of 1400 children the term obesity not be used for children (3). More
ages 18 to 71 months per site. More than 13,000 healthy recently, the NCHS proposed to classify children in
infants and children were involved in the study. The new the upper end of the reference distribution as either at
international growth reference provides a scientifically risk of overweight or overweight, again avoiding the use
reliable descriptor of physiological growth and a power- of the term obesity (7). However, in 1999, the Inter-
ful tool for advocacy in support of good health and national Obesity Task Force (IOTF) Expert Committee
nutrition. Another objective is to support, based on actual used the terms overweight and obesity to provide their
evidence, the concept that human growth during the first recommendations for assessment of children from 2 to
years of life is similar across groups of children of 18 y to be consistent with adult definitions (8). All of the
different ethnic/genetic backgrounds (5). There are recommendations take into account 2 levels of excess
genetic differences in linear growth, but these appear weight, but use of different definitions may lead to
to be of a similar nature across population groups. confusion in interpreting results, monitoring trends or
Adverse environmental factors by themselves or those comparing prevalence within and across countries. This
that interact with genetic makeup explain differences in is further complicated by the need to define the appro-
growth observed in low income groups. The corollary for priate anthropometric indices and cutoff points that best
this concept is that existing differences in growth are predict long-term adverse health outcomes. The use of
predominantly environmentally derived and can be sub- weight-for-height z scores to assess the nutritional status
ject to improvement. Prevalence estimates of undernutri- of children is still a common practice in pediatrics;
tion and obesity in children will clearly be affected to the recently BMI has been incorporated, after 2 y old, to
extent that the new reference differs from the WHO achieve concordance with adult assessment. In 1995, the

S28 UAUY ET AL.
WHO Expert Committee recommended the use of in absolute values, trends are similar independent of the
weight-for-height >2 z score to define overweight in standard used. At the individual level, the use of different
children under 10 y old (9). Body mass index is being criteria has an impact on the assessment of the nutritional
progressively adopted as a valid measurement of obesity status both for underweight and overweight children.
in childhood, adolescence and adulthood. Body mass This is exemplified in Table 1, which uses 3 hypothetical
index changes substantially with age and sex and thus children of equal height but different weights at each age
recommendations are age- and sex-specific. The 2000 between 2 and 5 y.
Centers for Disease Control (CDC) growth charts pro- Table 1 shows weight-for-height and BMI-for-age for
vide BMI-for-age curves for the US population. Based NCHS-CDC 2000; both measures show excellent agree-
on the NCHS recommendations, children with BMI ment in the identification of overweight and obesity (4/4
95th percentile are classified as overweight, whereas and 3/4, respectively). The WHO 1978 scale compared
children with BMI between the 85th and the 95th per- with the BMI-for-age criterion of NCHS-CDC 2000 have
centile are classified as at risk of overweight (10). The an excellent concordance for overweight (4/4), but no
use of BMI curves based on projected adult cutoff points agreement for obesity; the WHO 1978 criteria are sys-
has been recommended by the IOTF. These cutoffs are tematically more tolerant. When comparing weight-for-
based on age- and sex-specific percentiles for children height criteria, these agree in every case for the diagnosis
that project to the adult cutoffs of 25 kg/m2 for over- of overweight, but in only 1 case when the diagnosis is
weight, and 30 kg/m2 for obesity (8). The IOTF approach obesity. Again, the WHO 1978 criteria are systematically
has been considered to have a low sensitivity to detect more tolerant. There was scant agreement in the classi-
excess adiposity; in fact, IOTF obesity cutoff projects to fication of overweight and obesity between BMI-for-age
the 97th to 99th percentile values of the WHO standard. and the IOTF criteria–based classification, and the latter
This may prove helpful in terms of specificity. Another has a systematically lower sensitivity. In the case of
limitation of the IOTF approach is that it does not provide undernutrition for both sexes and all ages, NCHS-CDC
a way to assess the full distribution of values, so BMIs in 2000 weight-for-height and BMI-for-age have excellent
excess of the obesity cutoff cannot be quantified. When concordance and a higher sensitivity than the WHO 1978
z scores are used as part of the evaluation, the magnitude criteria. This implies that more children would be diag-
of the excess can be established with greater precision. nosed as underweight using either of the CDC indices as
At the population level, overweight and obesity preva- compared to WHO 1978 weight-for-height z score. These
lence vary depending on the definition used. We have differences in estimates of both underweight and over-
demonstrated, using a large data set for school children weight have clear implications in terms of the preventive
across 13 y of monitoring, that obesity prevalence interventions to which children may be subjected to
estimates determined using the IOTF cutoff points are improve their nutritional status. Overall, these results
significantly lower than those based on the WHO or the support the idea that at this age, weight-for-height
NCHS-CDC 2000 references (11). Despite differences and BMI-for-age perform equally well as measures of
TABLE 1. Nutritional status of hypothetical boys 2–5 y old using 4 different criteria
Weight-for-height BMI-for-age

WHO 1978 NCHS-CDC 2000 NCHS-CDC 2000 IOTF 2000
2
Age, y Weight, kg Height, cm BMI, g/m Pctl z score ND Pctl z score ND Pctl z score ND Pctl ND
2 10.5 85.5 14.4 5.7 1.6 N 1.8 2.1 U 2.0 2.1 U —

14.0 85.5 19.2 88.8 1.2 O1 95.7 1.7 O1 94.0 1.6 O1 94.0 O1
14.5 85.5 19.8 94.0 1.6 O1 98.3 2.1 O2 96.9 1.9 O2 96.9 O1
3 12.5 95.0 13.9 6.3 1.6 N 1.7 2.1 U 1.3 2.2 U —
16.0 95.0 17.7 86.1 1.1 O1 88.9 1.2 O1 89.4 1.3 O1 89.4 N
17.0 95.0 18.8 95.7 1.7 O1 97.5 2.0 O2 97.7 2.0 O2 97.7 O1
4 14.5 103.0 13.7 7.6 1.4 N 3.1 1.9 U 1.8 2.1 U —
18.5 103.0 17.4 89.1 1.2 O1 90.0 1.3 O1 91.7 1.4 O1 91.7 N
19.5 103.0 18.4 97.0 1.9 O1 96.3 1.8 O2 97.6 2.0 O2 97.6 O1
5 16.0 110.0 13.2 4.9 1.7 N 0.9 2.4 U 0.6 2.5 U —
21.0 110.0 17.4 90.1 1.3 O1 89.1 1.2 O1 91.0 1.3 O1 91.0 N
22.0 110.0 18.2 97.0 1.9 O1 94.5 1.6 O1 96.2 1.8 O2 96.2 O1
Pctl indicates percentile; ND, nutritional diagnosis; U, underweight equal to <2 z score for WHO 1978; <5th percentile for CDC 2000; —, not
defined in IOTF 2000; N, normal status; O1, overweight level 1 (1–2 z score for WHO 1978, 85th–95th percentile for NCHS-CDC 2000, equivalent to an
adult BMI 25–29.9 for IOTF 2000); O2, overweight level 2 (>2 z score for WHO 1978; 95th percentile for NCHS-CDC 2000, equivalent to an adult
BMI 30 for IOTF 2000).

z score not defined for IOTF 2000.

overweight and highlight the relevance of establishing an neonates and young infants. However, the expenditure
adequate reference population and cutoff points based on approach to estimate energy needs was used in children
long-term health outcomes rather than populations that older than 13 y based on estimates of basal energy
shift according to stage of epidemiological transition that expenditure, plus the energy required for normal growth
they face (12,13). Given the need for a continuous and defined level of physical activity (17). The dissemi-
indicator across age groups into adulthood we consider nation of the doubly labeled water method to assess total
BMI to be the best measure of overweight and obesity. energy expenditure during the past decades, and the
The need for specific cutoff values based on normative development of methods to assess activity levels
population or projected BMI into adulthood has not been applicable to young children, permitted measurements
fully agreed upon. The merit of the IOTF criteria in of daily energy expenditure in children from different
providing child BMI values projecting to adult BMI of 25 parts of the world. This allowed the 2001 FAO/WHO/
and 30 for overweight and obesity is offset by not having UNU committee to define recommendations based on
a continuous measure of the range. This is especially actual expenditure.
relevant for children who are above the obesity cutoff Energy recommendations for infant and child age
point; the IOTF criteria cannot discriminate whether a groups published by FAO/WHO/UNU in 2004 are based
child is 3 or 5 SD above the median BMI for age. on actual measurements and estimates of total daily
Acceptable international criteria to evaluate overweight energy expenditure either by the doubly labeled water
and obesity in children remain to be defined; for now the method or estimates based on heart rate monitoring
best practice is to record BMI data for age and present during active periods coupled with individual calibra-
median and SD values by gender (14). tions of oxygen consumption. The energy needs for tissue
deposition related to growth in infants, children and
EVOLUTION OF RECOMMENDED ENERGY adolescents were added to the estimate of daily energy
INTAKES FOR YOUNG CHILDREN expenditure. In the case of infants, the new recommen-
dations were based on breast-fed infants rather than
Optimal nutrition should be defined based on growth in formula-fed infants; for the first year of life, the mean
weight and length associated with the lowest risk of values for the former are 5% to 10% lower than figures
adverse health outcomes during infancy, but they also for formula-fed babies. Table 2 illustrates the changes in
should consider the burden of chronic disease in later life. energy recommendations for breast- and formula-fed
The redefinition of normal growth for children 0 to 5 y by infants during the first year of life and the differences
WHO/UNU is a step in the right direction because these with respect to the recommendations given in the
growth standards are based on longitudinal data from 1985 report.
infants fed according to the internationally agreed-upon The present recommendations based on expenditure
norms, exclusively breast-fed for the first 6 months of life are also substantially lower for children up to age 10 y in
and with added complementary foods after that. How- comparison with those derived on observed food intake
ever, the long-term effect of this dietary prescription as used in 1985 by FAO/WHO/UNU. Figure 1 compares
remains to be fully established (15). The prevention of the 2004 estimates with the 1985 estimates for boys and
obesity will indeed be supported by having a standard girls. The proposed energy requirements are 18% to 20%
that is based on breast milk feeding, which is known to lower for boys and girls under 7 y, and 12% lower for
decrease the risk of childhood obesity. In addition, there boys 7 to 10 y (Table 2). From age 12 onward, the
is an added dimension to this policy because the pre- proposed requirements are 12% higher for both boys
scription for energy intake of normal children has also
been redefined by the FAO/WHO/UNU report published TABLE 2. Comparison of present estimates of energy
in late 2004. requirements of infants with those calculated in 1985 FAO/
The energy recommendations for infants and children WHO/UNU report (selected ages)
published by FAO/WHO/UNU in 1985, based on the
work of the Expert Committee Group that met in Rome in Present estimates % difference
(kJ/kg/d) from 1985
1981 (16), were estimated from observed energy intakes 1985
of children from industrialized countries who were grow- Age, mo All infants Breast-fed estimates All infants Breast-fed
ing optimally according to the Harvard Growth Standard
(the best available measure at the time). To this, 5% was 0–1 460 430 519 11 17
2.1–3 395 380 456 13 17
added to support growth in conditions prevailing in 3.1–4 345 330 431 20 23
developing countries where infection was more prevalent 4.1–5 345 330 414 17 20
and diets may have lower digestibility. The need to 5.1–6 340 330 404 16 18
consider actual expenditure rather than intake was recog- 7.1–8 330 320 395 16 19
9.1–10 335 325 414 19 21
nized at the time, but there was insufficient data 11.1–12 335 330 437 23 24
on energy expenditure of young children, except for

S30 UAUY ET AL.
460 460
Boys Girls
440 440
420 420 1985
1985
400 400
380 380
360 360
340 340
ER, kJ/kg/d
ER, kJ/kg/d
320 320
300 300
2004 2004
280 280
260 260
240 240
220 220
200 200
180 180
160 160
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Age, years Age, years
FIG. 1. Energy recommendations for children and adolescents based on habitual energy intake as per FAO/WHO/UNU 1985 and derived
from energy expenditure FAO/WHO/UNU 2004.
and girls, assuming moderate levels of physical activity. the energy needs associated with the deposition of tissues
These modifications of the recommendations for infants or the secretion of milk at rates consistent with good
and children should serve to correct the overestimations health’’ (17). For infants and young children, energy
of the dietary energy needs of children from birth to 10 y. needs are equal to the sum of expenditure and energy
Interventions such as child feeding programs, formulated stored as growth. Total expenditure is the sum of several
based on the 1985 recommendations, could have easily components: basal metabolism, thermal effect of feeding,
led to excess energy intake among target populations. thermoregulation and physical activity. A lower recom-
The higher energy prescribed and the greater tolerance of mended energy intake for all children <10 y, except for
the anthropometric indices with overweight and obesity those that are highly physically active as prescribed by
could have contributed to the observed excessive weight FAO/WHO/UNU 2004, will contribute to the prevention
gain among these children. This may have been a critical of systematic energy excess and will stress the need to
problem for children living in urban settings, especially improve nutrient density of diets rather than increase
in countries undergoing economic and dietary changes energy intakes. For infants the new recommendations
associated with modernization. will serve to strongly support exclusive breast-feeding
The 2004 recommendations include a need for because as energy needs drop, the sufficiency of breast
physical activity to maintain fitness and health and milk energy supply is prolonged. This means that for
to reduce the risk of developing obesity and diseases most infants, exclusive breast-feeding will provide suffi-
associated with sedentary lifestyles. Moreover, different cient energy for normal growth for at least 6 months and
requirements for populations with lifestyles that involve possibly beyond this period. FAO/WHO/UNU 2004 will
different levels of habitual physical activity, starting at also serve to stress the need to enhance nutrient density of
6 y old are given. Recommendations for physical activity complementary foods after 6 months to meet infants’ and
levels based on classification of habitual activity con- children’s micronutrient needs rather than overemphasiz-
sistent with good long-term health are provided. The ing the need for high energy intakes to promote weight
energy requirement of an individual was defined by FAO/ gain. If the energy needs are lower and the micronutrient
WHO/UNU as ‘‘the level of energy intake from food that needs are the same, then the micronutrient density of the
will balance energy expenditure when the individual has diet becomes critical. Thus, both normative standards
a body size and composition and level of physical activity will act in synergy to prevent excess weight gain and to
consistent with long-term good health; and that will allow promote good linear growth in accordance with the only
for the maintenance of economically necessary and proven gold standard ‘‘the breast-fed infant.’’ This pre-
socially desirable physical activity. In children and preg- scription has stood the test of successful human evolution
nant or lactating women, the energy requirement includes for the past several million years. We still face the

challenge of defining the optimal energy intakes and A Weight/age

growth rates in early life, conducive to long-term health
across the life course.
Deficit Excess
NUTRITION PROGRAMS FOR YOUNG

CHILDREN IN TRANSITIONAL COUNTRIES:
NEED TO INCLUDE OBESITY PREVENTION
B -2.0 0 +2.0
Basic Considerations
To address food insecurity and protect vulnerable

groups from the scourge of hunger and malnutrition,
developing countries have implemented various forms
of food supplementation and/or income transfer pro-
grams to prevent the consequences of malnutrition
(18). It has been estimated that close to 1 of 5 Latin
Americans lives in poverty conditions and can be con- -2.0 0 +2.0
sidered undernourished/food insecure (19). However, Standard Deviations
these programs have the potential to induce energy excess FIG. 2. Model examining the effect of universal food supplement-
unless they consider critical issues in the selection of ation of children on the distribution of weight-for-age. A, Baseline
beneficiaries and in the type of food supplement pro- with a significant group of underweight (<2 SD). B, Shift in
vided. In the case of income transfer, choices made by distribution after universal food supplementation. Undernutrition
has been reduced considerably, whereas overweight and obesity
recipients of the programs may favor energy-dense, have increased.
nutrient-poor foods that may also contribute to over-
weight and obesity in women of reproductive age and
young children. A recent FAO survey with data from of those >2 SDs; in this case, the distribution of weight-
19 Latin American countries found that >20% of the for-age for the population is normal, with few individuals
population—approximately 83 million people of an esti- underweight or obese. The evidence emerging from
mated 414 million in these countries—receive some level countries undergoing the epidemiological transition
of food assistance benefits from nutrition-related programs indicates that if food supplements are provided without
(19,20). In contrast, the number of malnourished people in careful targeting, the situation becomes similar to that
the studied countries was 10 million, 12% of the total depicted in Fig. 2b. Some planners may even consider
beneficiaries of food programs. This indicates that nearly 9 this phenomenon to be an unavoidable consequence,
of 10 beneficiaries may be of normal weight or even whereas others suggest it as a desirable outcome because
overweight. Nutrition programs have evolved beyond it serves as evidence of the impact of a successful
the immediate needs of the malnourished and have become intervention (22).
part of the social and economic benefits demanded by A critical issue in defining the nature of this problem is
populations living in poverty. The Brazil Zero Hunger recognizing that underweight children are usually
Program, which is directed at those suffering from hunger, stunted, thus most malnourished children will be of
is predominantly an income-transfer program that pro- low weight- and length-for-age, but will have a near-
vides food and other commodities and does not include normal weight-for-length/height. In other words, they
biological or nutritional vulnerability in the criteria to are underweight and stunted, but not wasted. Because
select beneficiaries. In fact, the program has been criti- recovery in length-for-age is incomplete if nutrition
cized recently because the poor in Brazil are mostly improvement occurs after 24 to 36 months of age, these
stunted and overweight, rather than suffering from wasting children will gain significantly more weight-for-age than
(21). length-for-age when given additional food. In older
The nature of the problem is exemplified in a simple children, little or no gain in length-for-age is observed
manner in Fig. 2a, which presents the weight-for-age (23). Later in the article, we examine these issues in
distribution of children in a typical developing country various settings where additional food energy is pro-
with high prevalence of underweight children. As vided to children who are underweight and evaluate the
depicted in Fig. 2b, if food is provided for all children, consequences in terms of obesity prevalence. We also
not just those who are underweight, then the whole curve analyze how supplementary feeding programs may con-
will be displaced to the right, generating a significant tribute to rising obesity trends, what factors may explain
proportion of overweight and obese children. The desir- this phenomenon and the potential strategies needed to
able outcome, if targeting is efficient, is the elimination avoid a rise in obesity as a byproduct of malnutrition
of the tail below 2 SD without increasing the proportion prevention efforts.

S32 UAUY ET AL.
Most programs do not have targeting criteria based on incorporate the need to improve the quality of diets as a
actual anthropometry but rather on socioeconomic con- complement to food security. We analyzed these pro-
dition. The benefits are given to all, independent of grams derived from data collected by Uauy and Rivera in
whether there is evidence of low body weight. Significant the context of obesity prevention in developing countries
reductions in underweight and wasting have occurred in and the considerations made in the introduction to
most countries; undoubtedly supplementary feeding pro- this section.
grams have played an important role in this decline. Colombia has 6 widescale programs targeting chil-
Unfortunately, they may have also contributed to the dren, adolescents and pregnant women; these programs
rising trend in obesity (1). Stunting remains a problem are under the technical supervision of the Instituto
in most developing countries, despite the virtual eradica- Colombiano de Bienestar Familiar. Beneficiaries are
tion of wasting in many (24). In this setting, providing from the lowest socioeconomic level from both urban
food supplements may be beneficial for some, whereas it and rural areas. The objectives of these programs include
may be detrimental for others. Careful selection of family support, improvement in nutritional status, pro-
beneficiaries of food assistance programs and determi- motion of breast-feeding and healthy lifestyle. All of
nation of the right combination of nutrients/foods, edu- these programs have national coverage and for targeting
cation, and lifestyle interventions are required to opti- criteria use age and biological vulnerability. Four pro-
mize nutrition and health at each stage of the life cycle. grams also include anthropometry to target beneficiaries
This is a crucial problem that should be addressed before who are mostly malnourished. The food that is distributed
initiating specific programs (25). bienestarina provides between 30% and 80% of recom-
mended energy units and proteins and can include 1 of
Latin American Food and Nutrition Programs the energy and protein requirements, respectively. The
Targeting Children and Adolescents usual ingredients of bienestarina include a fortified vege-
tal mix made from powdered milk, soy flour, any cereal
Information on those programs from selected countries flour (rice, wheat or corn), legumes, sugar, molasses and oil.
(Colombia, Costa Rica, Cuba, Chile, Guatemala, Mexico, Costa Rica has 4 programs with national coverage that
Peru and Venezuela) can be found at http://latinut.net/f- target pregnant women, children and adolescents; 1
global/index.asp. A total of 40 nutrition or food programs program gives away money to buy a specific menu
target pregnant women and children, however, only 12 and another 1 tries to reduce micronutrient deficiencies.
include anthropometric indices to select their benefici- None of the 4 programs include anthropometric indices in
aries. Most are targeted to the low socioeconomic status the targeting criteria. Cuba has 6 programs of national
groups, based on biodemographic characteristics inde- coverage, of which 5 have as main objective to reduce
pendent of whether there is objective evidence that micronutrient deficiencies. Foods provided by these pro-
people require extra energy or are underweight for sta- grams include either fortified pureed fruit or flour.
ture. Moreover, FAO and other international bodies have Guatemala has 8 national programs and 3 regional pro-
defined hunger to meet the mandate of the World Food grams that target pregnant women and children. They
Summit and the Millenium Development Goals based on predominantly target malnourished populations; only 1
achievement of energy intake to meet theoretical energy of them considers anthropometry (weight-for-height) for
needs. This has been labelled ‘‘undernourishment’’ and targeting purposes. These programs provide beneficiaries
its the assessment is based on energy available from food a food ration consisting of legumes, cooking oil and flour
balance sheets, energy needs of the population and (a corn-soy blend). Other programs provide either micro-
distribution according to socioeconomic levels, with no nutrient-fortified sugar or flour. Mexico has 6 large-scale
actual measurement of any indicator of nutritional status. food programs. One of the most important was called
This in itself tends to overestimate the number of under- Progresa (the Spanish word for progress) but was
nourished people, and because no provision to assess renamed Oportunidades (the Spanish word for opportu-
body weight or physical activity is made, is often in sharp nities) (27). This is an incentive-based welfare program
contrast to the direct assessment of BMI of these popu- whose main objective is to invest in the nutrition, health
lations (9). In areas of the world, such as Latin America and education of young children from poor families to
and southeast Asia, where populations are progressively improve their chances of obtaining better opportunities
becoming urban and sedentary and energy availability is later in life. Apart from receiving a food supplement, the
not a limiting factor, the FAO definition of undernour- family receives money. Low-income families who are not
ished misguides policy (it assumes that the problem is beneficiaries of Oportunidades may participate in a
solved by providing food energy to poor populations). program that provides a daily breakfast and a food
Under these conditions, poverty is related to adequate or package that provides 20% of the daily energy recom-
even excess energy relative to physical activity levels and mendations (includes cooking oil, legumes and corn flour
diet is of poor quality in terms of healthy foods, rather to prepare tortillas). Oportunidades is an exception
than the amount of energy (26). This requires that we among the large-scale programs in Latin America

because it includes anthropometric measurements as part schoolers. Coverage is close to 70% of those in need.
of its targeting criteria. In 2003, approximately 120,000 children under 5 y of age
In Peru, there are 4 programs targeting low-income attended JUNJI. Of those, 95% were preschoolers from
pregnant women and/or children. Apart from socioeco- 2 to 5 y of age; the rest were infants under 2 y. The food
nomic considerations, 3 of them include anthropometry to distributed is programmed to cover 58% to 75% of
target beneficiaries. In general the supplement provides children’s daily energy needs, depending on whether
30% of the energy recommendation and includes fortified they attend a half-day or a full day. The energy supplied
specific foods such as baby food, cookies or a food by age grouping is 800 kcal/d from 2 to 3 y and 900 kcal/d
package. Venezuela has 5 programs with national cover- from 3 to 5 y. If a nutritional deficit (underweight) is
age, all of which target according to socioeconomic level. detected, then an additional 100 kcal/d are provided. This
One of these programs applies subsidies to what are program most likely has contributed to the notable
considered staple foods (corn flour, margarine, cooking decline in underweight and stunting observed in the
oil, sugar, whole milk, canned fish and legumes). The other preschool population during the past decade, but it
programs provide daily meals for vulnerable groups. may also beassociated with the increase in obesity rates
From this summary we conclude that only 1 of 4 food (29). Figure 3A illustrates the dramatic decline in under-
programs in Latin America includes anthropometry to nutrition evaluated by height-for-age, weight and weight-
target beneficiaries. The most commonly used anthro- for-height (note that the cutoff in this case is <1 SD, so
pometric index for targeting purposes is weight-for-age. the expected prevalence would be about 16%). The rise in
Because most underweight children in Latin America are overweight and obesity shown in Fig. 3B depicts the
stunted and not wasted, the target group may in fact be parallel increase in the height of children. We have
subjected to energy excess. Most energy-dense food recently addressed this issue in school-age children in
supplements provided to children after 3 y of age, when Chile, noting a significant association between the rise in
there is a limited chance to gain length, may in fact lead to
overweight and obesity (28). About 75% of the programs A
provide micronutrient-fortified supplements that are 30
important in promoting linear growth, but unless bioa- Height for age
vailability of micronutrients is taken into account, this 25 Weight for age
may also be of limited value. Our analysis suggests that Weight for height
Latin American countries should reexamine the type of 20
interventions in place and consider provision of micro-
nutrient-ich supplements with limited energy except for 15
populations or individuals who are wasted.
10
Chile, a Case Study for the Effect of the Nutrition
Transition in Young Children 5
Chile is often presented as a paradigm of the success of 0

supplementary feeding programs. Indeed, there is a close 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005
association between the presence of these massive and
expensive interventions and the decline in malnutrition in B
all age groups. Close examination of these data demon- 30 Height for age
strate that for infants, preschool and schoolchildren, under- Weight for height
nutrition based on weight-for-age was virtually eradicated 25
by the late 1980s, and stunting rates remained low but
significant until the mid-1990s. It is exactly at this stage of 20
the transition that obesity needs to be considered in the
15
implementation of programs and necessary changes need
to be incorporated. In fact, over the past 2 decades the 10
impact of the programs in reducing malnutrition was
progressively lost, whereas the association with rising 5
obesity prevalence has become notable (29).
0
The National Nursery Schools Council Program 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005
(JUNJI) created in 1971 under the Ministry of Education
FIG. 3. A, Dramatic decline in undernutrition (evaluated by height-
is of special relevance to our discussion of nutrition of for-age, weight and weight-for-height). B, Rise in overweight and
preschool children. JUNJI provides child care as well as obesity and the parallel increase in the height of children. Preva-
supplementary food for low-income infants and pre- lence(%)anthropometricindicesbelow-1SD(A) andabove1SD(B).

S34 UAUY ET AL.
obesity and the improved length of 6-y-old children; who presented a nutritional deficit received an extra
nearly half of the increase in obesity could be accounted 150 kcal/d. From 1987 onward, the energy content of
for by the increase in length (30). the meals has been adjusted according to age and the
In addition, as shown in Fig. 4, we evaluated the child’s weight status. If the child presented a deficit (low
change in the prevalence of obesity (BMI for age weight-for-height), an extra supplement was provided.
95th percentile; CDC/NCHS) of children between This remained the case until 1995, when the energy
March (school entry) and November (end of school year) content of this additional supplement was reduced to
for 1992 and 1996. The figure illustrates a marked rise in 100 kcal/day and was used for the few children who
obesity in all age groups during this period. The com- required this extra food based on being underweight
parison between March and November for the same year for their length.
showed that in 1992, the largest increment in obesity was These adjustments occurred between 1977 and 1987;
observed in 3-year-olds, whereas in more recent years, first, the energy content of the meals was reduced to
this was observed in 2-year-old children. The prevalence 1200 kcal/d (between 75% and 80% of daily energy
of obesity has remained stable from 1996 onward until needs) because it was determined that the children only
recently, when a possible drop was observed. stayed awake about two thirds of school time. In addition,
The rise in obesity during the past decade has led to the energy content of the meals was differentiated
significant changes in the energy prescribed and the according to 3 age groups. This last classification only
foods provided in an effort to curb the rise in obesity lasted 1 y because of implementation problems, and since
prevalence; these changes are summarized next. 1988, only 2 age groups are in place: 2 to 3 and 3 to 5 y
old. From 1988 until 1995, the energy content was further
Changes in Criteria to Prescribe Energy Provided by the reduced to 1000 kcal/d and 1200 kcal/d, respectively.
Program
Adjustment of Energy Content
Initially, the program provided a fixed amount of
calories which was not differentiated by age. Between In 1996, evaluation of the nutritional status of pre-
1970 and 1977, the energy content of the meals amounted school children under JUNJI’s supervision showed high
to 1500 kcal/d, that is, every preschool child independent rates of overweight and obesity. In addition, there was a
of age received the full daily energy recommendation high prevalence of inactivity. These 2 considerations led
based on FAO/WHO 1973 or 1985. In addition, children to a further reduction of the energy content to 900 kcal/d
A B
OBESITY IN PRESCHOOL CHILDREN IN CHILE 1992 OBESITY IN PRESCHOOL CHILDREN IN CHILE 1996
24 24
March March
% %
20 November 20 November
16 16
12 12
8 8
4 4
0 0
<3 3 to 4 4 to 5 2 to 3 3 to 4 4 to 5
n=3490 n=5834 n=5970
AGE years AGE years

FIG. 4. Cross-sectional comparison of obesity (BMI >95th percentile) prevalence at start of school year (March) and end of school year
(November) according to age in 1992 and 1996.

for children ages 2 to 3 y and 1000 kcal/d for those from Chile, is likely due to multiple factors acting in synergy.
3 to 5 y old. These modifications remained until 2001, To document the effect of trends of economic and social
when further reductions were made to 800 kcal/d and changes affecting diet and physical activity on obesity
900 kcal/d, respectively. This corresponds to an average prevalence of 6-y-old children in Chile, we conducted a
of 60% of energy recommendations based on FAO/ correlation analysis of these data. The study revealed that
WHO/UNU 1985 (16) and 72% of the recommen- social indicators such as gross national product per
dations published in 2004. (17). These changes were person, percentage living in poverty and social expendi-
implemented initially in 2001 in one third of the country, ture per person plus energy and macronutrient avail-
and the process was completed by 2004. As stated above, ability, car ownership, low birth weight prevalence and
if a child presents a nutritional deficit, then an additional deaths caused by diarrheal disease were highly associated
100 kcal/d is provided. with obesity in childhood (31). The multivariate
The potential impact of the nutrition programs in the regression of these data indicated that changes in income
rise of obesity was examined comparing the nutritional and car ownership explained virtually all of the changes
status of children at 2 y old when they entered JUNJI with observed in the univariate model. The only 2 additional
that observed 3 y later when they were 5 y old. The factors that entered into the multivariate analysis beyond
analysis for 2 longitudinal follow-up time periods (1992– income were percentage of fat energy units in the diet and
1994 and 1996–1998) are summarized in Table 3. The the number of deaths from diarrhea as an index of enteric
first study considered 8086 children. Of the 6238 children infections with a negative coefficient. In other words, less
who entered the program with normal nutritional status, infection was linked to higher obesity prevalence.
1503 (24.1%) and 506 (8.1%) became overweight and The effect of food and nutrition programs could not be
obese, respectively, over the 3 y. Of the 1440 who were isolated from other factors, but because they were main-
initially overweight, 730 (50.7%) became obese. In total, tained stable or increased while the number of people
there was a 3-fold increase in the number of obese living in poverty decreased, the net result was a major
children, from 408 to 1236. The second study period increase in the amount of food provided per beneficiary.
shown in Table 3 included preschool children from This effect was further amplified because recent economic
Santiago studied from 1996 to 1998. The proportion of growth led to self-exclusion of high- and middle-income
normal and overweight children becoming obese was beneficiaries and thus there was a significant association
lower than was previously observed. However, the base- between the increased availability of food provided by the
line data indicated that >10% were already obese on programs with the increase in obesity. This association by
entry, and this figure increased by about half. Therefore, no means proves causality. The necessary changes in the
there was less of a rise during the program, but obesity programs to decrease energy content while maintaining or
was already high on entry. increasing micronutrient supply were slow to come, but
The dramatic increase in obesity of young children went in the right direction overall. Recent evaluations of
during the past 15 years across the world, including obesity prevalence and incidence in preschool children
suggest that the problem is being controlled although it has
TABLE 3. Comparison of nutritional status at entry and exit of not been reversed.
preschool children participating in JUNJI during 3-y
longitudinal follow-up CONCLUSIONS

1989–1991
There is an urgent need to improve the evaluation of
Nutritional status 3 y later nutritional status and the categorization of undernutri-
tion. The systematic measurement of stature needs to be
Nutritional
status at entry Normal Overweight Obese Total
incorporated into the assessment of nutritional status in
all countries. This provides a way to separate individuals
Normal 4229 1503 506 6238 who are underweight from those who are stunted, of
Overweight 341 612 487 1440 normal weight or overweight for their stature. The
Obese 59 106 243 408
Total 4629 2221 1236 8086
assessment of height provides a clear indication that
1996–1998y the main nutritional problem of children in most devel-
Normal 444 111 37 592 oping countries is stunting and not underweight. This
Overweight 71 57 49 177 realization should lead to a rethinking of the interventions
Obese 18 24 50 92 needed, placing a greater emphasis on the improvement
Total 533 192 136 861
of linear growth.

Children entered at 24–36 mo of age and received 1000 kcal/d The recognition that stunting is the major nutritional
(1992–1994). problem should lead to strengthening the prescription of
y
Children entered at 24–36 mo of age. They received 900 kcal/d at exclusive breast-feeding as a norm for young infants up to
that age and 1000 kcal/d after 36 mo (1996–1998). 6 months old. There is also a need to improve the

S36 UAUY ET AL.
micronutrient content of complementary foods. Iron, 6. Implement programs for treatment of childhood
zinc, vitamin A and other micronutrients should be obesity early to prevent present and future adverse
incorporated in the foods provided by government pro- consequences.
grams for infants and young children. Programs targeted 7. Monitor growth using appropriate standards and take
at malnourished infants and children (defined based on necessary actions to prevent stunting in all children
insufficient weight for age or in poor weight gain) need to and avoid unhealthy weight gain in all children.
include assessment of weight-for-length as criteria for
discharge after a trial of food supplementation. If a child
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Tackling the Child Malnutrition Problem: From What and Why to

How Much and How
Milla McLachlan
Codirector, Full Circle Consulting, Boulder, CO
ABSTRACT
There is strong economic evidence to invest in improving the nations. New initiatives to redefine nutrition science and to
economic status of young children, yet programs remain under- apply innovative problem-solving technologies to the global
resourced. Returns on investment in child nutrition in terms of nutrition problem suggest that steps are being taken to accel-
improved health, better education outcomes and increased
productivity are substantial, and cost estimates for effective erate progress toward a malnutrition-free world. JPGN 43:S38–
programs are in the range of $2.8 to $5.3 billion. These amounts S46, 2006. Key Words: Investment in nutrition—Copenhagen
are modest when compared with total international develop- Consensus—Affordability—Nutrition policy change—Social
ment assistance or current spending on luxury goods in wealthy technologies. # 2006 Lippincott Williams & Wilkins
INTRODUCTION Nobel Laureates, was asked to review commissioned

papers on 10 identified global challenges and answer
The Adams family has done the sums; they have the question, ‘‘What would be the best ways of advancing
checked and rechecked their assumptions. Over the global welfare, and particularly the welfare of developing
short-, medium- and long-term they and their business countries, supposing that an additional $50 billion of
are going to benefit from investing in an insurance policy. resources were at governments’ disposal?’’) In fact, in
It is not exciting, it does not make the news headlines, but their characteristically modest way they concede that
they know it is essential, a very good thing. They can their paper does not break new ground; it uses recent
afford to buy it now; they can even pay cash for it. They evidence to confirm what others have concluded before
have more than enough information, they are aware of them, namely that the economic argument for investing in
what could happen if they do not do it. Yet they get nutrition is solid. Why then does nutrition action
distracted, their attention wavers, they move on to some- remain underresourced?
thing else, and spend the money on their rifle collection Why does the gap between evidence and action per-
instead. sist? Do nutritionists simply need to work harder, com-
Sometimes I think the global community is like the municate smarter, advocate more ardently? Or is it
Adams family when it comes to tackling issues of hunger institutional arrangements and leadership that need
and malnutrition. refreshing? Or could it be that the guiding frameworks
Nutrition programs, many of which are evidently and approaches of the field are out of touch with the
sound economic investments, and unquestionably are complexities of the nutrition problems of the
‘‘good things,’’ are chronically underfunded. Behrman 21st century?
et al. (1) make this all-too-familiar observation at the The focus of this article is on the economic evidence
conclusion of their paper on nutrition investment oppor- for investing in nutrition. It first presents the economic
tunities for the Copenhagen Consensus (2). (The Copen- argument and demonstrates that the question, how much?
hagen Consensus aimed to set priorities among the many is being answered thoroughly and convincingly. It then
available mechanisms to address major global chal- argues that this evidence is not matched by action, and
lenges. A panel of 8 eminent economists, including 3 that equal rigor must now be applied to the question.
There are encouraging signs that this is beginning to
Address correspondence to Milla McLachlan, 1320 Yellow Pine Av, happen. An adequate response to the nutrition challenges
Boulder, CO 80304 (e-mail: milla@rcn.com). of the 21st century requires nothing less.
S38
TACKLING THE CHILD MALNUTRITION PROBLEM S39
INVESTING IN NUTRITION MAKES seat at the table when resource allocation decisions are
ECONOMIC SENSE made. This article, therefore, attempts a brief overview of
the economics of child nutrition from a practitioner’s
The nutrition community owes a debt of gratitude to perspective before turning to the pressing issue of turning
Behrmann and coauthors for representing nutrition so evidence into action.
effectively in the Copenhagen Consensus. Based on The following section explores 4 key economic ques-
detailed analyses and using conservative estimates and tions related to child malnutrition. First, it explores the
discount rates, they lay out a carefully argued and con- relationship between nutritional status and economic
vincing case that reducing the prevalence of low birth productivity. Then it asks what it costs to improve nutri-
weight (LBW), addressing infant and child malnutrition tional status, and whether the benefits from improving
and breast-feeding promotion, reducing micronutrient nutritional status outweigh the costs. Given the private
malnutrition, and investing in technology for agriculture benefits to investing in nutrition, it then asks whether
in developing countries are sound development invest- public investment to improve nutritional status is justified
ment opportunities. The top economists who made up the on economic grounds. Finally, it weighs the aggregate
Copenhagen Consensus panel concurred, and ranked the cost to society of removing malnutrition as a public
nutrition investments second, fifth, 11th and 12th among health problem.
their recommendations for the best applications of a
hypothetical $50 billion in additional development assist-
ance (Table 1). WHAT IS THE RELATIONSHIP BETWEEN
A person who is not an economist can hardly do justice NUTRITIONAL STATUS AND ECONOMIC
to the intricacies of the economic theory underlying this PRODUCTIVITY?
work, and the detailed analysis used to arrive at the
Copenhagen Consensus conclusions is beyond the scope It is well known that the relationship between nutri-
of this article. Nevertheless, it is incumbent on nutritional status and individual productivity is bidirectional,
tionists to speak the economists’ language if they want a that the pathways are complex, and that different nutri-
tional conditions have different effects. Figure 1 provides
a framework for understanding these relationships
TABLE 1. Copenhagen Consensus: ranking investment (Behrmann et al. (2004) make the point that we can
opportunities (2) make more accurate estimates by tracing causal relation-
Project rating Challenge Opportunity ships rather than associations. This involves controlling
for endogeneity, in other words, they attempt to isolate
Very good the impact of nutritional status per se on the outcome
1 Diseases Control of HIV/AIDS
2 Malnutrition Providing micronutrients
variable in question, rather than merely capturing associ-
3 Subsidies and trade Trade liberalization ations between variables. [Nutritional status may be an
Good indicator for some other condition, for example,
4 Diseases Control of malaria unknown intrahousehold dynamics, rather than being
5 Malnutrition Development of new
agricultural technologies
the factor which itself has a direct impact on the outcome
6 Sanitation and water Small-scale water variable, such as cognitive development]).
technology for livelihoods Other articles in this supplement lay out the extent and
7 Sanitation and water Community-managed causes of malnutrition, detail the impact of malnutrition on
water supply and sanitation physical and cognitive development, and propose effective
8 Sanitation and water Research on water productivity
in food production intervention strategies. The present article briefly reviews
9 Government Lowering the cost of the pathways through which nutritional status influences
starting a new business economic productivity, and presents consolidated infor-
Fair mation on economic losses caused by malnutrition. The
10 Migration Lowering barriers to migration key pathways are increased morbidity and mortality,
for skilled workers
11 Malnutrition Improving infant and health care costs, and productivity losses resulting from
child nutrition learning and schooling deficits and reduced stature. Based
12 Malnutrition Reducing the prevalence on the available literature, this article provides evidence
of LBW that the benefits of addressing malnutrition conditions
13 Diseases Scaled-up basic health services
Bad outweigh the costs of nutrition programs and considers
14 Migration Guest worker programs for the implications of these findings.
unskilled workers The focus is on fetal and young child malnutrition,
15 Climate Optimal carbon tax given that the earliest years of a child’s life represent
16 Climate Kyoto Protocol the period in which nutritional requirements per kilo-
17 Climate Value-at-risk carbon tax
gram of body weight are highest, when the child is most

S40 MCLACHLAN
Mortality $$$?
Immune
Morbidity Health
function School
care cost
access &
Cognitive quality
Days lost
dev’t
from school
Early
Nutritional Growth Days lost Schooling
Status from work productivity
Stamina,
endurance
Labor
Physical market
capacity
Current
nutritional Max. Individual
status workload Economic
productivity
FIG. 1. Pathways of nutritional status and economic productivity.
susceptible to infection, and when insufficient food, 2499 g was 4 times more likely to die in the neonatal period
care and health have the most debilitating effects on than an infant weighing 2500 to 2999 g and 10 times more
growth and cognitive development. Furthermore, likely than an infant weighing 3000 to 3499 g. In the
growth faltering at that time is at best only partially postneonatal period, these ratios were 2 and 4, respectively.
overcome later in life (3). With LBW, genetic rather than nutritional factors may play
a greater role in mortality. A study in the United States
Malnutrition, Morbidity and Mortality and Health found that genetics played an important role in neonatal
Care Costs death rates, but was less significant after 28 d. The study
observed a 14% decrease in mortality, with a 450-g
The synergy between malnutrition and infectious dis- increase in body weight at birth.
eases is well established (4). In a widely quoted study, With regard to micronutrient malnutrition, eliminating
Pelletier and coworkers (5) estimated that 56% of child vitamin A deficiency can reduce mortality from all
deaths can be attributed to the potentiating effect of causes in children 0 to 4 y old, by 13% (8). Exper-
malnutrition (including LBW), with most of those deaths imental field research found that twice-yearly supple-
linked to mild or moderate malnutrition, rather than mentation with vitamin A reduced overall child mortality
severe malnutrition. Although severely malnourished by 25% to 35% (9).
children are more likely to die, they are far fewer in The value placed on saving a life has a significant
number. Children with mild, moderate or severe malnu- impact on the calculated benefit to the society of averting
trition would be, respectively, 2.5, 4.6 and 8.4 times more LBW, reducing stunting or improving micronutrient
likely to die than children whose weights are within the status. Estimating the monetary value of a human life
normal range for their ages. Not only can a significant lost is controversial, however, and researchers have used
proportion of child deaths from common infectious dis- a number of different approaches, none of which are
eases be attributed to malnutrition (measles, 44.8%; without problems. One option is to use actual resource
malaria, 7.3%; diarrhea, 60.7%; and pneumonia, costs applied by a society to avert a death through an
52.3%) but malnutrition also increases the likelihood alternative technology (eg, measles immunization) rather
of having an attack of malaria, diarrhea or pneumonia than using an assumed ‘‘absolute’’ value a society may
(but not measles) (6). There is also increasing evidence wish to ascribe to a life (1). Using this measure, Behrman
that fetal malnutrition predisposes to the metabolic syn- et al. arrive at an average estimate of $1250 for saving an
drome later in life (7). infant’s life in a developing country. The problem with
Behrman and coworkers (1) review a number of studies, this approach is that it would place a lower value on the
which identify low birth weight as a significant contribu- life of a child in a country with a poorly developed health
tory factor in neonatal and infant deaths. In an analysis of infrastructure than in a country with a sophisticated
12 national data sets, including those from Guatemala and health care system. An alternative approach, proposed
India, it was found that a full-term infant weighing 2000 to by the Copenhagen Consensus (2), is to assign an

arbitrary value of $100,000 to a life. Such a valuation TABLE 2. Summary of productivity losses associated with
increases the benefits of averting a death from LBW by a malnutrition (%)
factor of 80, but has the unrealistic implication that
Losses based on
saving a child’s life in a low-income country with an Type of Current losses childhood malnutrition
average adult wage of for example $500/y would be malnutrition (manual labor) (cognitive)
equivalent to 2000 adult-years of earnings, whereas in
countries with higher wage rates of for example $5000/y, Protein–energy 2–6 (moderate stunting) 10
malnutrition
it would represent only 20 adult-years of earnings. 2–9 (severe stunting)
Malnutrition can directly contribute to increased Iron deficiency 17 (heavy labor) 4
health care costs through a number of mechanisms. A 5 (blue collar)
review of studies on the cost of LBW (1) conclude that Iodine deficiency NA 10
Vitamin NA NA
LBW (not all caused by malnutrition) results in longer A deficiency
hospital stays where births occur in hospital settings and
higher risk for future hospitalization and outpatient facil- Reproduced with permission from Asian Development Review.19
ity use at a cost in the US of $263/case in 1995. Cross- Copyright 1999, Asian Development Bank.
country comparisons are made difficult by the differences
among countries’ medical systems, markets and policies. attained body size in adulthood in several countries
Health care costs will be substantially lower in countries (11,12). In Zimbabwe, Alderman and coworkers (13)
in the south, but this comes at the expense of higher found that children exposed to drought at ages 12 to
mortality and reduced productivity in adulthood. 24 mo were malnourished in later childhood, whereas
children who were older during the drought were not,
Malnutrition, Schooling, Learning and Productivity suggesting that early childhood malnutrition (during the
12- to 24-month window) is not easily reversed. Several
Malnourished children tend to start school later, pro- studies (14–17) found associations between smaller sta-
gress less rapidly, have lower attainments, and perform ture in adulthood and reduced earnings. In a study in
less well on cognitive achievement tests, even into adult- urban Brazil, for example, a 1% increase in height
hood. These indirect effects of malnutrition on pro- corresponded to a 2% to 2.4% increase in wages and
ductivity are substantially more than the direct effects earnings for women and men in the market sector (18).
of height on schooling and hiring. Table 2 summarizes findings from several studies on
Malnourished children may receive less education than productivity losses resulting from deficits in cognitive
their well-nourished peers for a number of reasons. Care- ability, schooling and stature in Asian countries (19).
givers may invest less in their education or schools may use
physical size as a rough indicator of school readiness, and
thus bar children of short stature from entering school at Malnutrition and National Economic Productivity
the appropriate age. Malnourished children are also sick
Several studies have attempted to express the impact of
more often and so absent more often, and learn less well
nutritional factors on individual productivity in terms of
when they are in school. Studies show that delayed entry to
national economic productivity. These estimates are useful
school leads to lower expected lifetime earnings because
to graphically demonstrate the impact of malnutrition and
of fewer years in the workforce (1).
have been used effectively in advocacy campaigns. They
In addition to its impact on adult productivity through
are based on a series of assumptions about the linkages
less schooling, severe malnutrition also affects learning
between individual productivity and national productivity,
capacity or cognitive development directly, with conse-
and often do not take account of other intervening vari-
quent impact on schooling productivity and labor pro-
ables, such as infrastructure development, including health
ductivity. Birth weight and breast-feeding both correlate
and schooling, and are therefore more difficult to sub-
with cognitive development; malnourished children per-
stantiate. Because of these limitations, authors are gener-
form poorly on cognitive tests, have poorer psychomotor
ally conservative in their estimates. Table 3 provides a
development and fine motor skills, have lower activity
summary of findings from a number of studies in India,
levels, interact less frequently with their environments
Pakistan, Bangladesh and Vietnam (19).
and fail to acquire skills at normal rates (10).
Malnutrition, Stature and Earnings WHAT DOES IT COST TO IMPROVE

NUTRITION? DO THE BENEFITS OUTWEIGH
As indicated earlier, growth deficits in the first 2 to 3 y THE COSTS?
of life are only partially regained during childhood and
adolescence, particularly when children remain in poor Doing cost calculations as part of an impact evaluation
environments. Stature at age 3 is strongly correlated with of direct and indirect approaches to improving nutritional

S42 MCLACHLAN
TABLE 3. Estimates of productivity costs of malnutrition (19) specific measures to address malnutrition conditions, and
the programmatic costs, based on the best-available
Country Stunting Iodine deficiency Iron deficiency
information.
India 1.4 0.3 1.25
Pakistan 0.15 3.3 0.6 IS PUBLIC INVESTMENT TO IMPROVE
Vietnam 0.3 1.0 1.1
Losses including childhood cognitive impairment associated with iron NUTRITIONAL STATUS JUSTIFIED?
deficiency
The benefits of investing in nutrition outweigh the
Cognitive þ costs but are not sufficient for motivating the use of
Cognitive only manual work
public money for such activities. At first glance, one
Bangladesh 1.1 1.9 would argue that nutrition is a private good; after all, most
India 0.8 0.9 of the benefit accrues to the individual in better quality of
Pakistan 1.1 1.3 life, better education, better job prospects, and ultimately
Reproduced with permission from Asian Development Review.19 better lifetime earnings. However, there is often insuffi-
Copyright 1999, Asian Development Bank. cient private incentive for families to invest in nutrition.

Selected countries, as percent of gross domestic product. This may be due to a lack of information on the benefits
of good nutrition. If capital and insurance markets do not
status is a difficult and costly undertaking. Unfortunately, work optimally, families may also not see benefits in
gathering cost information is not considered theoretically investing in young children’s nutrition. They may recog-
interesting by most academics (J. Hoddinott, personal nize that preventive action would not protect children
observation), and has tended to be neglected. More from illnesses in the absence of proper affordable health
attention is now being given to program evaluations, care and sanitation. Furthermore, if unemployment is
and programs are being encouraged to collect more high and future employment prospects low, parents may
detailed costing information. To specify the economic not see the value of investing in their children’s growth.
gains from better nutrition more accurately, accurate The social benefits of investing in nutrition may be
information on the costs and effectiveness of programs considerable. Improved nutrition may decrease the like-
is needed. lihood that communicable diseases will spread in a
Evidence compiled from available studies (1) indicates community. A novel perspective proposed by Harold
that the benefits of effective interventions to address key Alderman (personal observation) is that in communities
nutrition conditions exceed the programmatic costs by a where malnutrition rates are high, short and thin children
considerable margin, even when a high discount rate is may be the norm, and parents may not recognize the need
used to put less weight on the long-term benefits of the to attend to their children’s nutritional status. Under such
investment, and when the upper limits of cost calcu- circumstances, if some children in the community grow
lations are used. Table 4 provides a summary of the well, then the norm may indeed be challenged and begin
calculated monetary value of benefits to be derived from to shift toward taller and sturdier children, with parents
TABLE 4. Benefits and costs of selected nutrition interventions (1)

Opportunities and targeted populations Benefits (US$) Costs (US$) Benefits–costs (US$)
Reducing LBW for pregnancies with high LBW probabilities

Treatments for women with asymptomatic bacterial infections 580–986 200–2000 0.58–4.93
Treatments for women with presumptive sexually transmitted diseases 580–986 92–460 1.26–10.71
Drugs for pregnant women with poor obstetric history 580–986 28–280 4.14–35.20
Improving infant and child nutrition
Breast-feeding promotion in hospitals 5952–8929 133–1064 5.6–67.1
Integrated child care programs 376–653 40 9.4–16.2
Intensive preschool programs with nutrition for poor families 1.4–2.9
Reducing micronutrient deficiencies
Iodine (per women of childbearing age) 75–130 0.25–5.0 15–520
Vitamin A (preschool children <6 y) 37–43 1–10 4.3–43
Iron (per capita) 44–50 0.25 176–200
Iron (pregnant women) 82–140 10–13.4 6.1–14
Investing in agriculture technology
Dissemination of new cultivars for higher yields 8.8–14.7
Dissemination of iron- and zinc-dense rice and wheat varieties 11.6–19
Dissemination of vitamin A–dense ‘‘golden rice’’ 8.5–14

Estimates are based on extensive assumptions, subject to considerable uncertainties, and are indicative only. Discount rates of 3%–5% apply.

finding reasons to invest in their children’s nutrition, in TABLE 5. 10-y nutrition investment program cost estimates
line with the new norm. It can also be argued that in cases (20)
in which governments are already investing substantially
Micronutrient supplementation $billion
in education and health services, investment in nutrition
can help to improve the efficiency of those investments Vitamin A for under-5s at 7.5–15.00
and is therefore justifiable on efficiency grounds. $1.50/child (full coverage)
If a policy objective is to achieve greater equality Iron folate/pregnancy at $14/pregnancy 7.0–14.00
at 50–100 million pregnancies
through the use of public funds, then a finance minister Integrated IDD control 1.0–1.5
will be interested to know whether investing in nutrition Micronutrient fortification
would benefit the poor at least as much as or more than Wheat flour 0.85
the wealthy. Given that malnutrition rates are higher Maize meal flour 0.84
Cooking oil 0.70
among the poor than the rich, it may be argued that Biofortification 0.15
the benefits of malnutrition reduction initiatives are Community-based health and
likely to be concentrated among the poor. Of course, nutrition programs
although nutrition programs can have this impact, the Focus: South Asia and priority 12
design and implementation of the programs themselves sub-Saharan African countries
100 million children 2 y at $5–$10/y 10.0–20.0
will determine whether they are in fact pro-poor. Total 28.0–53.0
For fortification programs, the public sector share is estimated to be

<25% of the total cost. IDD indicates iodine deficiency disorders.
CAN SOCIETY AFFORD IT? Reproduced with permission from Asia Pacific Journal of Clinical
Nutrition.20 Copyright 2005, HEC Press.
Having made the case that it makes economic sense to
invest in improving children’s nutrition and that cost-
effective intervention approaches exist, the question Can the world afford this? Affordability at a global
remains whether countries and society at large can afford level is not the primary reason for slow action to improve
the outlay needed to address malnutrition. What will childhood malnutrition. The estimates given above, how-
it cost? ever imprecise they may be, are modest when compared
A number of recent initiatives have included total cost to other expenditures. The upper estimate ($5.3 billion),
estimates for selected interventions and countries. Given which includes private spending, represents a small
the uncertainties that surround these numbers, they are fraction (4%) of total estimated development assist-
best used as indicative figures. What they suggest is that ance, which as is widely recognized, falls far short of the
for most interventions, the costs are affordable to the target of 0.7% of gross domestic product in developed
global community. How they will be financed and countries. When these estimated costs are compared with
specifically, how to deal with recurrent costs and building annual expenditures on other ‘‘priorities,’’ as was done in
sufficient implementation capacity to absorb the the United Nations Development Program Human Devel-
additional development financing are hotly debated opment Report of 1998 (21) (Table 6), it is evident that
topics in the broader development community. money is not the limiting resource in achieving global
A study for the Millennium Project Task Force on nutrition goals.
Hunger (20) provides estimates for a 10-year global
investment program. The study concluded that an HOW IS THE ECONOMIC EVIDENCE FOR
annual investment of between $2.8 and $5.3 billion NUTRITION INVESTMENT BEING USED?
would provide broad coverage with vitamin A and
iron supplements, fortification of commonly consumed How many more studies and reviews documenting
foods, and community-based action in countries with nutrition as a sound investment are needed before invest-
the highest levels of childhood malnutrition (Table 5) ment in nutrition will increase substantially? There are a
(20).
Using different assumptions and cost estimates, the
TABLE 6. Can we afford to stop malnutrition? (21)
analysis for the Copenhagen Consensus (1,2) estimated
that it will cost about US$ 2.8 billion annually to reach Annual expenditure, $billion
25% of eligible mothers and children with interventions
Cosmetics in the US 8
to improve LBW, improve infant and child nutrition and Ice cream in Europe 11
provide micronutrient supplementation and fortifica- Perfumes in Europe and the US 12
tion to vulnerable groups. The authors estimate that Pet foods in Europe and the US 17
it would become progressively more expensive and Cigarettes in Europe 50
administratively more challenging to reach vulnerable Alcoholic drinks in Europe 105
Military spending in the world 780
groups, as malnutrition rates improve.

S44 MCLACHLAN
number of cases in which economic data were effectively problem. As Kurt Levin has said, ‘‘You cannot under-
used to increase investment in nutrition. For example, stand a system unless you change it’’ (25).
beginning in 1975, Berg skillfully used economic data to In 1992, Alan Berg noted the gap between evidence
show that nutrition programs could be seen as investment and action. He proposed that more attention needed to be
rather than simply consumption and thus stimulated given to implementation capacity, and he called for the
World Bank investment in nutrition (22). The use of development of a cadre of ‘‘nutrition engineers’’ who
the Modeling Program Profiles to estimate the economic would help to resolve the implementation issues that
cost of malnutrition, in Bangladesh for example (23), has hampered the successful realization of lofty nutrition
also been credited with helping to convince policy policy goals (26). In a similar vein, Heaver (27) proposed
makers of the need to invest in nutrition. However, as systematic attention to building organizational capacity
mentioned earlier, Behrman and coworkers (1) point out to address the evidence-action gap in nutrition. It is
that in spite of the evident favorable cost–benefit ratios imperative that capacity development and organizational
for nutrition programs, investment in nutrition remains arrangements for nutrition be addressed in a more sys-
stagnant. tematic manner. Organizational arrangements through
Is more of the same needed? Should nutritionists try to which nutrition policy decisions are made and imple-
convince ministers of finance and heads of development mented at global, regional and national levels are chan-
agencies of the economic merits of dealing with malnu- ging. For example, civil society and nongovernmental
trition and of investing in proven, cost-effective inter- organizations have become key actors, as has the private
ventions? Yes, indeed, they should. Nutritionists need to sector. The new reality is that the complex social chal-
be economically literate, able to speak with economists lenges of the 21st century require that the 3 sectors of
and finance ministers and understand enough of their society (public, private and civil) find ways to work
language to speak with confidence in their forums. They together toward solutions that would benefit all. Uncom-
need to make the arguments with country-specific data, fortable as it may be, given their different perspectives
offer solutions based on sound evidence, emphasize the and ways of working, partnerships are the way forward
short- and medium-term benefits, and not overstate the for solving complex global problems (28).
case. In particular, it is important to stress the need for In addition, there is a need to develop the nutrition
complementary developments, including programs to policy process as a field of study. The same rigor should
improve women’s status, address infectious diseases be applied to studying the policy process as is evident in
and improve water and sanitation as well as employment epidemiological and economic studies of nutrition. A
and income growth; otherwise families will not be able to review of the current state of policy studies in nutrition
take advantage of the benefits that accrue from improved shows limited activity and little coherence in this field.
nutrition. Furthermore, the figures seldom speak for Most studies are of the case study variety and lack an
themselves; skillful advocacy and careful timing helped explicit theoretical framework. In cases in which a
to lead from evidence to action in the cases cited above. theoretical framework is made explicit, the rationale
Will more of the same be enough to address the for selecting 1 approach over another is seldom made
evidence-action gap mentioned earlier? Unfortunately, clear (29). This rather haphazard approach means that
there are several factors that make the task of increasing studies are not building on one another, they are difficult
action on nutrition difficult and contribute to the intract- to compare across studies, and progress in developing the
ability of the global nutrition problem. For example, the field has been slow.
interests of policy makers and their constituencies may be In contrast to other practice-oriented fields, such as
remote from the interests of poor women and children. rural development or social work, nutrition does not have
Even in families, children and women may have too little a long history of theorizing about its policy and practice.
voice to be taken into consideration when families make Consequently, there is little vested interest in particular
decisions about allocation of resources. Nutrition must approaches and theories. There is therefore a great
compete for attention with sectors that are better orga- opportunity to find innovative solutions to the how
nized and institutionalized. It shares with other preven- question of the Introduction. By drawing on the most
tive approaches the characteristic that the problem, and up-to-date literature and experience in other fields, as
its benefits when removed, is generally not immediately well as on practical experience of nutrition policy pro-
visible. ‘‘Slow, silent catastrophes’’ simply do not gen- cesses, robust and rigorous analytical approaches can be
erate and maintain public interest the way crises do (24). developed to understand how nutrition policy change
The list goes on, and the literature is replete with con- processes work.
jecture about the causes of the gap between evidence and A number of recent initiatives suggest that nutrition is
action and the need to close it. It is time to stop mention- in fact on the cusp of a great leap forward on this front.
ing the evidence-action gap as the footnote to learned For example, some are paying attention to the underlying
papers and talks and start doing something about it, and in assumptions informing nutrition science and suggesting
the process, developing a deeper understanding of the that new paradigms are emerging. The New Nutrition

Science Project, a joint undertaking of the International 2. Copenhagen Consensus Center Web site. Available at: http://
Union of Nutrition Sciences and the World Health Policy www.copenhagenconsensus.com. Accessed August 12, 2005.
Forum, has set itself the task of ‘‘redefining nutrition 3. Martorell R. The nature of child malnutrition and its long-term
implications. Food Nutr Bull 1999;20:288–92.
science’’ (30,31). This initiative should provoke lively 4. Schrimshaw NS, Taylor CE, Gordon JE. Interaction of Nutrition and
discussion and help to shape the conceptualization of Infection. Monogr Ser 57. Geneva: World Health Organization,
nutrition theory and practice. Others are addressing the 1968.
policy process directly. Thus, nutrition policy researchers 5. Pelletier DL, Frongillo EA Jr, Schroeder DG, Habicht JP. The
effects of malnutrition on child mortality in developing countries.
(29,32) have proposed that the policy sciences approach Bull WHO 1995;73 (4):443–8.
(33,34) be adopted as a meta-framework for policy 6. Caulfield LE, de Onis M, Blössner M, et al. Undernutrition as an
research programs. The policy sciences approach is underlying cause of child deaths associated with diarrhea, pneu-
comprehensive, covering such dimensions as social pro- monia, malaria, and measles. Am J Clin Nutr 2004;80:193–8.
cesses, decision processes, and problem orientation. It 7. Barker D. Mothers, Babies and Health in Later Life. 2nd ed.
London: Churchill Livingstone, 1998.
makes explicit the role of the policy analyst and promotes 8. Mason JB, Musgrove P, Habicht J-P. At Least One-Third of
the use of multiple methods, acknowledging that there are Poor Countries’ Disease Burden Is Due to Malnutrition. Working
multiple ways of knowing, and that moral goals are Paper No. 1, Disease Control Priorities Project. Bethesda,
inherent in the policy process. Closer to the field, still MD: Fogarty International Center, National Institutes of Health,
2003.
others are applying new thinking on complex social 9. Beaton G, Martorell R, Aronson K. Effectiveness of Vitamin A
problem solving to nutrition. For example, in India, Supplementation in the Control of Young Child Morbidity and
UNICEF, in collaboration with Synergos and Hindustan Mortality in Developing Countries. Nutrition Policy Discussion
Lever, are working with local stakeholders in the state of Paper No. 13, ACC/SCN State-of-the-Art Series. New York: United
Maharashtra to test a social technology for solving Nations, 1993.
10. Grantham-McGregor SM, Fernald LC, Sethuraman K. Effects of
complex social problems (35). The technology, known health and nutrition on cognitive and behavioural development in
as the U-Process draws on phenomenology, dialogue and children in the first three years of life. Part 1. Low birthweight,
collaborative action research to develop a shared under- breastfeeding and protein-energy malnutrition. Food Nutr Bull
standing of systems and the capacity to design innovative 1999;20:53–75.
11. Martorell R, Khan KL, Schroeder DG. Reversibility of stunting:
solutions together and implement them (36). Innovations epidemiological findings in children from developing countries.
like these in the areas of the field’s basic assumptions, its Eur J Clin Nutr 1994;52 (S1):S43–53.
policy processes and social change technologies are a 12. Simondon K, Simondon F, Simon A, et al. Preschool stunting, age at
rich resource for learning to answer not only the what, the menarche and adolescent height: a longitudinal study in rural
why and the how much of nutrition, but also the all- Senegal. Eur J Clin Nutr 1998;52:412–8.
13. Alderman H, Hoddinott J, Kinsey B. Long term consequences
important action question, how, to achieve the desired of early childhood malnutrition. Oxford Econ Pap 2006;58:450–
nutrition goals. 74.
14. Deolalikar A. Nutrition and labor productivity in agriculture:
estimates for rural South India. Rev Econ Stat 1988;70:406–13.
CONCLUSIONS 15. Behrman JR, Deolalikar A. Wages and labor supply in rural India:
the role of health, nutrition and seasonality. In: Sahn D (ed).
Economic evidence reviewed for this article Causes and Implications of Seasonal Variability in Household
Food Security. Baltimore: Johns Hopkins University Press; 1989.
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The question of how much is being answered productivity: wage evidence from the Philippines. Oxford Bull Econ
thoroughly and the evidence is convincing. Not only Stat 1991;53:45–68.
17. Strauss J, Thomas D. Health, nutrition, and economic development.
are the returns on investment in terms of improved J Econ Lit 1998;36:766–817.
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addressing malnutrition is also clearly cost effective women in urban Brazil. J Econometrics 1997;77:159–87.
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matched by action, it is now necessary to focus on Asia. Asian Devel Rev 1999;17:246–73.
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Successful Food-Based Programmes, Supplementation

and Fortification
M.G. Venkatesh Mannar
President, Micronutrient Initiative, Ottawa, Ontario, Canada
ABSTRACT
This review highlights interventions and delivery mechanisms nutrients have expanded rapidly, with evidence of impact. A key
to alleviate macro- and micronutrient deficiencies in preschool need is to deliver micronutrients to remote and impoverished
children. These deficiencies can be addressed through an inte- populations in an affordable and sustainable manner. Govern-
grated combination of improved dietary intake, supplement- ment commitment, clear policy and programme direction,
ation, commercial and home-based fortification of advocacy and communication combined with a strong pub-
complementary foods. Several developed and developing lic–private partnership is essential for successful programmes.
countries have implemented successful approaches to eliminate Often a period of voluntary fortification needs to be followed by
protein-energy malnutrition and micronutrient deficiencies with mandatory requirement to ensure full compliance and sustained
sustained impact. These include provision of oral supplements
impact. The review concludes that proven technologies, com-
in capsule, tablet or syrup form. Certain micronutrients
(eg, vitamin A) can be provided as high-dose supplements munications and infrastructure can be harnessed to ensure that
twice per year. Most other vitamins and minerals (eg, iron, the nutrient needs of preschool children are met. When admi-
zinc, iodine) need to be provided in daily doses. Fortified nistered systematically with the commitment of and participa-
complementary foods provided through public feeding pro- tion by the public and private sectors, most of the major
grammes and commercially marketed foods have also made deficiencies can be bridged on a sustained basis, contributing
a positive impact. There is growing evidence of the impact of to improved health and well-being of millions of children
home-based fortification of complementary foods using pre- around the world. JPGN 43:S47–S53, 2006. Key Words:
mixes in single-serving sachets. The fortification of commer- Micronutrient deficiencies in preschoolers—Targeted public
cially marketed staple foods such as cereal flours, cooking oils programmes—Commercially marketed foods—Food industry
and dairy products could have a small but significant impact on policy—Mandatory/voluntary enrichment. # 2006 Lippincott
preschool children. Cereal flours with iron, folic acid and other Williams & Wilkins
INTRODUCTION continue to be major health burdens in developing

countries. Such malnutrition prevents as many as one
It is now well established that the major damage third of the world’s people from reaching their physical
caused by malnutrition takes place in the mother’s womb and mental potential. Malnutrition combined with a poor
and during the first 2 y of life. This damage is often diet and infectious disease forms a vicious cycle, with 1
irreversible and causes lower intelligence and reduced condition affecting the others. Consequently, malnu-
physical capacity, which in turn reduce productivity, slow trition is the most important risk factor for the burden
economic growth and perpetuate poverty. Countries risk a of disease in developing countries and is directly and
‘‘lost generation’’ unless they improve nutrition addres- indirectly responsible for about half of all deaths in young
sing both protein-energy and micronutrient needs for children (1). Although higher incomes and better food
preschool children, the stage of life when the body security improve nutrition over the longer term, malnu-
and brain experience maximum growth and development trition is not simply the result of food insecurity; many
potential. children in food-secure environments are underweight or
Protein-energy malnutrition, resulting in people being stunted because of inappropriate infant feeding and care
underweight or stunted, and micronutrient malnutrition practices, poor access to health services or poor sani-
tation. Child nutrition is an essential element in human
Address correspondence and reprint requests to Venkatesh Mannar,
development and is best improved in the context of
Micronutrient Initiative, 250 Albert Street, Ottawa, Ontario K1R 7Z1, coordinated investments in primary health care and early
Canada (e-mail: vmannar@micronutrient.org). and basic education.
S47
S48 VENKATESH MANNAR
Much more attention, therefore, needs to be given to growth monitoring, especially about maternal care and
the betterment of nutrition via an integrated combination rest during pregnancy; exclusive breast-feeding and
of health and nutrition education, improved dietary appropriate complementary feeding practices; education
intake, supplementation and commercial and home- on how to care for sick children; and links to essential
based fortification of complementary foods and staple health services. Some programmes have also provided
foods more broadly. There are proven and cost-effective micronutrient supplements and/or food supplements for
methods available that can greatly accelerate the children and pregnant and lactating women; this, how-
improvement in nutrition. In addressing malnutrition, a ever, implies there is a need for good training and
combination of interventions involving the promotion of fostering counselling skills. The programmes are targeted
breast-feeding, improving food availability and micro- to children <2 y of age. Successful, large-scale child
nutrient bioavailability and increasing food consumption, growth promotion programmes were established in the
food fortification and pharmaceutical supplementation 1980s in India’s Tamil Nadu state, Indonesia and
will need to be emphasized and implemented in a comp- Thailand, and are ongoing in Bangladesh, Honduras,
lementary manner. These factors need to go well beyond Madagascar and Senegal, among others. Such pro-
conventional health and nutrition systems and be based grammes led to a sharp decline in severe malnutrition in
upon enabling people and communities so that they will the first 1 to 2 y, with a slower rate of decline in moderate
be capable of arranging for and sustaining an adequate and mild malnutrition thereafter. A recent cross-country
intake of micronutrients, independent of external support. review of successful programmes concluded that they led
Strategies are necessarily multisectoral and integrated to an average decline of 1 to 2 percentage points per year
interventions with strong social communications, evalu- in rates of malnutrition in young children, 2 to 4 times
ation and surveillance components. the 0.5% rate calculated as the average secular trend in the
Optimally, we should be able to meet nutrient require- absence of such programmes (2).
ments through the food we eat. Maybe we will reach that Malnutrition in young children is also being addressed
goal one day, but we are not there yet. For several in several countries through facility-based services
reasons—economic, geographic, social and cultural— such as the Integrated Management of Childhood Illness
this has not been a practical solution, and even if this Program, developed in 1992 with the aim of prevention or
were possible there are issues related to the lack of early detection and treatment of the leading childhood
bioavailable minerals and vitamins from staple diets. killers. Although these programmes focus on treatment
This inability to meet energy requirements is exacerbated of childhood illnesses, they also emphasize prevention of
by commonly consumed foods and beverages, including illness through education on the importance of immu-
rice, wheat, corn, legumes, tea and coffee being high in nization, micronutrient supplementation, and improved
inhibitors and low in enhancers of micronutrient absorp- nutrition, especially breast-feeding and infant feeding
tion. The objective of this review is to identify successful (3).
and effective interventions to alleviate malnutrition in
preschool children. SUPPLEMENTATION PROGRAMMES
ADDRESSING MALNUTRITION THROUGH Oral supplements in capsule, tablet or syrup form

COMMUNITY-BASED PROGRAMMES provide immediate relief to vulnerable populations and
age groups with special micronutrient needs (eg, preg-
The best window of opportunity for addressing mal- nant and lactating mothers, preschool children). Certain
nutrition lies between pregnancy and 2 y of age. Improv- micronutrients, such as vitamin A, can be provided as
ing maternal knowledge and care during pregnancy to high-dose supplements twice per year. Most other
address low birth weights, especially in Asia, and infant vitamins and minerals (eg, iron, zinc, iodine) need to
feeding and caring practices, such as exclusive breast- be provided in daily doses. In some cases supplement-
feeding and adequate and timely complementary feeding, ation for women during adolescence and through the
are critical to improving nutrition outcomes. Well- childbearing years, especially during pregnancy, needs to
designed and consistent nutrition education approaches be continued indefinitely.
aimed at changing specific practices are key. In addition, A clear success story is the improvement in the vitamin
because moderate and mild malnutrition are not readily A status of preschool children using high-dose supple-
apparent, regular monitoring of children’s weights on a mentation. Vitamin A supplements lend themselves to
growth chart is important so that mothers know whether distribution through a campaign approach because
their children are growing properly and can see the children require only 2 annual doses. Vitamin A supple-
benefits of changes in practices. mentation (VAS) has been associated with a reduction in
During the past 20 y successful programmes have been excess mortality of up to 35% among preschool children
developed in several countries using a combination of in populations in which vitamin A deficiency is endemic.
nutrition education or counselling, either with or without In 1998 the World Health Organization recommended

SUCCESSFUL FOOD-BASED PROGRAMMES, SUPPLEMENTATION, FORTIFICATION S49
administering VAS with routine and other immunization with such packages but also to integrate VAS into pro-
contacts as a way of integrating provision with other tective child survival and health services in a sustainable
health services. As National Immunization Day cam- manner.
paigns became widespread, many countries integrated Iron supplementation has proved more challenging
VAS and oral polio vaccine distribution, enabling large than VAS because the supplement must be taken daily
numbers of children to receive at least 1 VAS dose and sometimes has unpleasant side effects; consequently,
annually. At least 90 countries routinely provide vitamin there have been problems with the logistics of supply and
A supplements to young children in developing sometimes with compliance among clients. As a result
countries. More than 75% of all young children in 40% to 60% of the children in most developing countries
countries where vitamin A deficiency is known to be continue to suffer from iron deficiency anaemia and
common received high-dose vitamin A capsules in 2002, many more have functionally significant iron deficiency.
compared to only about one third in 1994 (4). Countries Prevalence rates are particularly high and devastating in
as different as Nicaragua (5), Niger (6) and Nepal (7) their functional consequences for children ages 6 mo to
have reached coverage levels >80%. 2 y, when the brain is continuing to grow. Indonesia and
A good example that clearly establishes the effective- Thailand are among the few developing countries that
ness of VAS is Nicaragua, where coverage has gradually have made the most progress in reducing anaemia. In
increased in both rounds since 1994 and levels >70% Thailand between 1986 and 1996, anaemia prevalence
have been sustained since 1999, with levels >80% since in pregnant women fell from 40% to 15.5% and anaemia
2003. The average coverage rate by round from 1997 to in children <5 y old declined from 40.6% to 25.2%.
2001 amounted to 79% in first rounds and 78% in second Based on such successes, guidelines have been developed
rounds. The latter is a remarkable achievement because to guide effective iron supplementation programmes and
obtaining high second round coverage rates has been a replicate proven programme models (9).
formidable challenge for many countries. Only 1% to 2% In settings where the risk of zinc deficiency is high and
of the total coverage has been achieved through non- where other strategies may be difficult to implement in
national health campaign routine health service distri- the short term, the distribution of zinc supplements as
bution. A 2000 National Micronutrient Survey carried prophylaxis may be considered. The efficacy of supple-
out about 4 months after the second health campaign of mental zinc to improve specific health outcomes among
1999, revealed a dramatic reduction (72%) in the preva- high-risk population groups has been well demonstrated
lence of vitamin A deficiency in children 12 to 59 mo of in a variety of geographical settings. However, country-
age, from 31.1% in 1993 to 8.6% in 2000 (8). This level assistance is required for the design and integration
significant improvement may be mostly attributed to of zinc supplementation strategies within existing health
the cumulative effect of VAS as a result of the consist- programmes (10).
ently high coverage rates in children over the 6-y period Given the multiplicity of deficiencies, the idea of
preceding the survey, given the absence of other specific providing multiple micronutrient supplements for infants
interventions during the same period. Successive rounds and preschool children is appealing. More research is
of supplementation may have gradually increased serum needed to identify both physiological and health out-
retinol levels over time. comes and the relative value of alternative micronutrients
As polio National Immunization Days phase out, or in and potential competition between them, from absorption
some cases terminate abruptly, there is a need to develop to physiological outcome.
alternative delivery mechanisms to ensure that VAS
reaches all eligible children twice each year. (Recent FOOD FORTIFICATION
assessments by UNICEF and the Micronutrient Initiative
have found that many countries are working to implement Food fortification involves the identification of com-
integrated packages of health services for their popu- monly eaten foods that can act as vehicles for 1
lations, and phasing out ‘‘vertical programmes,’’ includ- micronutrients and lend themselves to centralized pro-
ing stand-alone VAS distribution [unpublished data, cessing on an economical scale. Fortification, when
2004].) Governments and international institutions are imposed on existing food patterns, may not necessitate
turning to alternative supplement delivery channels as a changes in the customary diet of the population and does
means of sustaining these gains (eg, piggybacking on the not call for individual compliance. It can often be dove-
Day of the African Child, World AIDS Day in Tanzania tailed into existing food production and distribution
[H. Masanja et al., unpublished data]) or creating twice- systems. For these reasons, fortification can often be
yearly national micronutrient days, following the Philip- implemented and yield results quickly and be sustained
pines’ and Niger’s examples. Clearly,VAS must be more over a long period of time. It can thus be the most cost-
closely integrated with other interventions such as effective means of overcoming micronutrient malnu-
deworming, malaria prevention, and antenatal checks. trition. The World Bank has reported that ‘‘No other
The challenge is thus to ensure not only adequate reach technology offers as large an opportunity to improve lives

at such low cost and in such a short time’’ (11). Food Also, because basic and value-added foods are processed
fortification is aimed to provide meaningful levels of the from staple commodities, fortifying foods at the base of
nutrient, usually 30% to 50% of the daily adult require- the pyramid results in fortifying products throughout the
ments, at normal levels of consumption of the food food chain. Often a period of voluntary fortification
vehicle. The levels also need to take into account vari- needs to be followed by mandatory requirement to ensure
ations in food consumption so that the safety of those at full compliance and sustained impact.
the higher end of the scale and impact on those at the Cereals are important food vehicles for fortification.
lower end are ensured. They should also consider pro- Although several foods could be used for carrying micro-
rated intakes by young children to ensure efficacious and nutrients, wheat flour and maize meal are excellent
safe dosages. vehicles because they are staple foods in many parts
The most successful global fortification experience of the world and exist as key ingredients in so many food
is the fortification of salt with iodine. A number of preparations. When micronutrient deficiencies are popu-
countries have successfully iodized their salt supplies, lation-wide and result from a combination of low intake
thus reducing goiter and cretinism, preventing metal and/or low bioavailability, fortification of commonly
retardation and subclinical iodine deficiency disorders, consumed cereal flours with iron, folic acid and other
and contributing to improving national productivity. vitamins offers a number of strategic advantages because
There has been remarkable growth in salt iodization cereals flours are widely and regularly consumed, and
application globally during the past decade. A significant mostly processed in centralized facilities with established
proportion of the populations in more than 110 countries distribution and marketing capacity. Costs of fortification
have access to iodized salt (12). As of 2004 nearly two range from 3 to 10 cents per person per year. For these
thirds of the salt consumed in the developing world is reasons cereal fortification has played a major role in
being iodized, protecting nearly 70 million newborns improving the health of the world populations at large.
each year from the threat of mental impairment caused Nearly 40 countries now fortify flour. In Latin America
by iodine deficiency. flour fortification covers significant numbers of people
Many countries are progressing toward the goal of and sugar fortification has taken hold in Central America.
universal salt iodization. Most of the salt used for human There is growing interest and action on wheat flour
and animal consumption in Latin America is iodized. fortification in south and southeast Asia. In Africa the
Bolivia, Peru and Ecuador, formerly severely affected fortification of wheat and maize flours with multiple
countries, are now free of iodine deficiency. In many nutrients has been made mandatory in South Africa
Asian countries, including Bangladesh, China, Indonesia and Nigeria.
and India, salt iodization is rapidly gaining ground. Folic acid fortification of cereal flours is having a
In sub-Saharan African countries including Nigeria, remarkable impact on reducing women’s risk of having a
Madagascar, Eritrea and Cameroon, salt iodization levels baby born with spina bifida or anencephaly. Food for-
are >80%. Once established in a country, salt iodization tification was determined to be the best strategy for
is a permanent and long-term solution to the problem of increasing blood folate levels because the critical period
iodine deficiency. Toxicity issues are negligible and for adequate intake of folic acid is in the first weeks of
cost considerations fairly small, amounting to only 1 pregnancy, before most women know that they are preg-
to 3 cents per person per year. Although considerable nant and begin taking supplements. In the United States
progress has been made in streamlining control pro- the fortification of enriched cereal grain products with
grammes through salt iodization in several countries,
producer compliance, quality assurance, logistic pro-
blems and bottlenecks remain. The challenge is to sys-
tematically identify and tackle these constraints through
effective advocacy, social communications, monitoring VALUE-ADDED FOODS
of salt iodine levels, regulation and enforcement. Salt, e.g. condiments, beverages
convenience foods, candies
which forms the ubiquitous part of our diets, can also
carry a range of other nutrients including iron, zinc and
vitamin A.
Fortification of other staple foods such as flour, oils, BASIC FOODS
e.g. breads, biscuits, packaged
sugar, condiments, dairy products and a range of pro- cereals, dairy products
cessed foods with other minerals and vitamins is also
growing in the developing world. Potential food vehicles STAPLE FOODS
can be visualised as a 3-tiered pyramid (Fig. 1). e.g. whole grain & milled cereals,
Fortifying less expensive staple foods at the base of the oils & fats, sugar, salt
pyramid results in broader dissemination of micronutri-
ents throughout the population, particularly in the poor. FIG. 1. Food product pyramid.

folic acid began in 1996. By 1999 the National Health cation on appropriate infant feeding practices and psy-
and Nutrition Examination Survey conducted by the chosocial care of the infant.
Centers for Disease Control and Prevention found that
the average level of folic acid in the blood of US women TARGETED FORTIFICATION THROUGH
of childbearing age had almost tripled in 5 y (13). In SUPERVISED PUBLIC PROGRAMMES
Canada, where fortification of flour, pasta and cornmeal
became mandatory in 1998, a study in Ontario showed Fortification of foods that are targeted to vulnerable
that the incidence of neural tube defects had fallen to and low-income groups needs high priority. There are
8.6 cases/10,000 pregnancies, down from 16.2/10,000 in several opportunities in developing countries that if taken
1995 (14). advantage of and applied could make a vast difference
Developed countries have long fortified milk and to millions of people suffering from micronutrient
breakfast cereals with vitamin A as well as other vitamins deficiencies.
and minerals, but in developing countries sugar has so far Fortified complementary foods provided through pub-
been the most successful vehicle. Guatemala’s sugar lic feeding programmes and commercially marketed
fortification programme has virtually eliminated vitamin foods have also had a positive impact. In some states
A deficiency. Significant reductions have also been noted in India food provided to children and to mothers under
in El Salvador and Honduras, where fortification was the Integrated Child Development Scheme in cooked or
combined with supplementation (15). Sugar fortification ready-to-eat form is micronutrient enriched. In Ecuador
and VAS were also combined in Zambia beginning in the Ministry of Public Health developed a complemen-
1998, with demonstrated success in urban areas (16). In tary feeding programme that sought to prevent poor
much of Africa and Asia the poor do not consume as growth, anaemia, and other micronutrient deficiencies
much sugar as they do in Latin America, however, so by targeting all infants and young children between 6 and
other countries such as Nigeria, Morocco, Yemen, 24 mo of age living under conditions of extreme poverty
Bangladesh and Pakistan are experimenting with fortify- by providing micronutrient-fortified complementary
ing wheat flour or cooking oils with vitamin A. foods such as Mi Papilla specifically designed to meet
their unique nutritional needs (17). It contracted the
production and distribution of the food to a private
FORTIFICATION OF COMPLEMENTARY company through a competitive bidding process. This
FOODS enabled the health workers to focus on providing health
services and nutrition counseling. During health center
The fortification of commercially marketed staple visits for well- or sick-child care, coupons for the for-
foods such as cereal flours, cooking oils and dairy tified complementary food are provided to eligible
products could have a small but significant impact on children. Mothers or caregivers can redeem these cou-
preschool children. (Infants and children under the age of pons for Mi Papilla at a nearby pharmacy or store selected
24 mo consume a different dietary pattern than do older by the community as the distribution point. At the final
individuals.) There are no major differences in consump- survey, the hemoglobin levels in children in the pro-
tion among children ages 2 y and older. Industrially gramme group were significantly higher and they were
produced fortified complementary foods are recom- significantly less likely to be anemic compared with
mended by pediatricians worldwide as an essential part children in the nonprogramme group (27.6% vs 44.3%).
of a nutritionally adequate infant diet beyond the age of In Mexico under the Progresa programme, a large
6 mo and are complementary with breast milk and home- incentive-based development programme that today
prepared foods. Fortification, especially of iron and reaches 4.5 million families and included a nutritional
zinc, is essential to meet the micronutrient requirements component, children and pregnant and lactating women
of infants. Beyond the superior micronutrient content of in participating households received fortified nutrition
industrially fortified complementary foods over home- supplements, and the families received nutrition edu-
prepared rice porridge and other traditional infant foods, cation, health care, and cash transfers. Progresa was
this approach possesses advantages of delivering micro- associated with better growth in height and haemoglobin
nutrients of higher bioavailability, higher energy density values among the poorest and younger infants (18).
and protein quality, not to mention safety and conven- Nutrition interventions are also an important com-
ience. ponent of social planning in Chile. Since the 1950s,
From the food technology perspective, the challenge is the National Supplementary Food Program administered
to increase both the energy density of complementary by the Chilean Ministry of Health through primary care
foods and levels of micronutrients at an affordable price. health centres has provided free milk-based complemen-
From the public health perspective, we need a combi- tary foods to children from birth to 5 y. The monthly
nation of proper regulation that protects infant health yet health care programme, which includes growth and
supports industrial innovation and strong public edu- development monitoring, breast-feeding promotion and

immunization and education in nutrition, is offered in through which supplements are channelled or to com-
conjunction with the National Supplementary Food mercially marketed fortified foods.
Program. Since 1999 the programme has delivered free Research so far has focused on 5 crops: rice, wheat,
of cost 2 kg/mo of a full-fat powdered milk to 70% of maize, cassava and common beans and 3 nutrients: iron,
infants from birth to 18 mo. Lactating mothers consume zinc, and b-carotene. For all of these crops, there is
this milk until their infants are weaned. The milk is adequate genetic variation in concentrations of b-caro-
fortified with iron, ascorbic acid, zinc and copper. The tene, other functional carotenoids, iron, zinc, and other
programme has helped reduce anaemia in Chilean infants trace minerals in varieties available in germplasm banks
from 21% to around 1% (19). to increase micronutrient densities through conventional
Where fortified foods are not available, there are breeding by a multiple of 2 for trace minerals and by
multiple ways to deliver micronutrients to enable mothers higher multiples for vitamin A. A new 10-year challenge
to either add them to the cooking pot or to mix them into programme of Consultative Group on International
what they feed their infants. These food supplements are Agricultural Research known as Harvest Plus proposes
available as water-dispersible or crushable tablets, sprin- to further increase the micronutrient content of these
kles or spreads that can be added to complementary foods crops through conventional breeding, test their nutritional
just before feeding infants and young children. These efficacy and then widely disseminate them in developing
supplements are designed to provide up to the full level of countries for adoption by farmers.
the Recommended Dietary Allowance for vitamins and
minerals in a small volume at a low cost and are easily DELIVERY AND SUSTAINABILITY
integrated into existing food practices.
Fortified lozenges, containing a combination of vita- A key need is to deliver and distribute micronutrients
mins and minerals: vitamin A, vitamin C, zinc, iron and to remote and impoverished populations in an affordable
folic acid, offer a new approach to providing micronu- and sustainable manner. Government commitment, clear
trients to beneficiaries who are children between 2 and policy and programme direction, advocacy and com-
5 y, adolescent girls and pregnant and lactating mothers. munication combined with a strong public–private part-
In India lozenges are distributed to children and mothers nership is essential for successful programmes. We have
on a daily basis along with the regular supplementary also realized that addressing malnutrition cannot happen
food provided through the Integrated Child Development through stand-alone vertical programmes. We have also
Scheme. The distribution is supported by a strong become much more effective in inserting nutrition into
communications component imparted to the mothers. broader health and social development goals, rather than
Some advantages of this approach are that distribution wait for them to be addressed to serve the cause of
is simple, measured quantity of micronutrients can be nutrition. We must focus increasingly on intersecting
ensured and compliance is high. micronutrient programmes with major development
challenges. These challenges include HIV/AIDS,
malaria, hookworm and reproductive health and emer-
MICRONUTRIENT-RICH STAPLE FOODS gency programmes. In addition, nutrition should be
included on the agenda of important reproductive and
Breakthroughs in plant breeding and nutritional geno- child health initiatives. Vitamin A deficiency should be
mics could simplify and hasten the development of placed on the agenda of ophthalmologists. Similarly, iron
nutrient-rich varieties of crops. New efforts to enhance deficiency needs to become a priority in early child
the micronutrient content of staple foods such as rice, development, school health and maternal health pro-
maize, sweet potato, cassava, common beans and wheat grammes.
that are consumed by poor people in developing countries A programming environment is emerging globally and
through plant breeding are showing promise. Advanced at the individual country level. The move from projects to
biotechnology tools, such as genome mapping and programmes, from financing and implementing vertical
marker-assisted selection, could enable us to identify, disease-specific projects to sector-wide approaches and
select, and transfer desirable traits, including those linked budget support, as well as a reinvigorated focus on
to high micronutrient content for nutrients such as iron, multisectoral action, poverty reduction and issues of
zinc and b-carotene, from 1 variety to another with or equity, are part of this new environment. The role of
without transfer of genes across species (20). By produ- civil society and the private sector is becoming more
cing plants that are dense in minerals and vitamins, a important in global health and nutrition. At the same
process referred to biofortification, we could have crop time, focus on results has never been higher on the agenda
varieties with improved nutritional content in the staple of both development partners and developing countries.
foods people already eat. This can be a feasible means of These changes call for new approaches in moving the
reaching malnourished populations in relatively remote nutrition agenda forward, accelerating the move from
rural areas with limited access to health programmes project to more coordinated programme approaches,

repositioning nutrition appropriately in country-develop- 2. Mason J, Galloway R, Martines J, et al. Community health and
ment strategies, reorienting existing large-scale invest- nutrition programs. In: Jamison D, Breman J, Claeson M, et al., eds.
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York: Oxford University Press for the World Bank.
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ness and cost of facility-based integrated management of childhood
CONCLUSIONS illness (IMCI) in Tanzania. Lancet 2004;364:1583–94.
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It is often said that malnutrition persists because of a Deficiency. A Global Progress Report. New York: United Nations,
2004.
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ment coupled with weak policies and ineffective pro- Nicaragua. Newsletter 3. Washington, DC: MOST (United States
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Solutions to Nutrition-related Health Problems of Preschool

Children: Education and Nutritional Policies for Children
Ian Darnton-Hill, yEileen Kennedy, zBruce Cogill, and S.M. Moazzem Hossain
UNICEF Headquarters, New York, NY, {Tufts University, Boston, MA, and {Academy for Educational Development,
Washington, DC
ABSTRACT
Objective: By reviewing the literature, lessons learned and or multisectoral interventions must be addressed to all children
experience regarding the nutrition-related health problems of at risk for death, poor health and compromised growth and
preschool children, draw conclusions and make development. Adequate health care and nutrition is a human
recommendations on education and nutrition policies for right, legally established in the Convention on the Rights of the
young children. Child.
Results: The most common causes of under-5 mortality in low- Conclusions: Improved health and nutrition will lead to
income countries have been identified as neonatal disorders, enhanced economic development, but having a poverty focus
diarrhoea, respiratory infections, malaria, measles, and in appears to be essential, if poor people are not to be marginalized
some developing countries, AIDS. More than half (56%) of further. The HIV/AIDS pandemic illustrates this challenge
all child deaths have underlying malnutrition and undernutrition clearly. The role of education, especially girls’ education, in
as a contributing factor. Children must have optimal growth and improved health and nutrition status of children and birth-
physical and intellectual development to learn and achieve their spacing is now clear, as is improving women’s status.
potential in society. Solutions include both preventive and Increases in female status and education have been estimated
curative interventions at all levels and include both improved to account for half of the reduction in child malnutrition rates
health and education systems. Recent focus has been on health during the past 25 years. JPGN 43:S54–S65, 2006. Key Words:
systems interventions that address averting deaths by cause for Undernutrition—Overnutrition—Double burden of disease—
the 42 countries that account for 90% of worldwide under-5 Nutrition policies—Education and nutrition. # 2006
deaths (the majority in sub-Saharan Africa). However, parallel Lippincott Williams & Wilkins
INTRODUCTION stunted and underweight children. In these same

countries, large numbers of people live in conditions
More than 10 million children younger than 5 y old die of extreme poverty, struggling to survive on less than
every year. If proven interventions were to be applied, US$1/d. Although poverty is undoubtedly a cause of
then more than 60% of these deaths could be averted (1). hunger, malnutrition and undernutrition, poor health
A few countries account for a large proportion of all child and nutrition are also conversely causes of poverty.
deaths, with more than 50% of global deaths occurring Numerous studies have confirmed that hunger seriously
in just 6 countries, and 90% of deaths occurring in impairs the ability of the poor to develop their skills and
42 countries, most of them in sub-Saharan Africa and reduces the productivity of their labour (5–9).
in south Asia (2). More than half of all deaths from Poor nutrition and inadequate education have perva-
infectious diseases have underlying malnutrition and sive effects on health and well-being and addressing these
undernutrition as a contributing factor (3,4). will have both direct and indirect benefits for child
Measures of poor access to food, undernutrition and survival, growth and development (5–9). Alleviating
poverty are also strongly correlated, so that countries poverty and addressing geopolitical factors such as fair
with food insecurity also have high prevalences of trade and debt relief must also be addressed if sustainable
solutions are to be had (10). Although understandable,
Address correspondence and reprint requests to Dr Ian Darnton-Hill, the decision of the Bellagio Child Survival Study Group
Officer-in-Charge, Nutrition, Section, and Senior Adviser, Child Sur- (11), when they examined the reasons for sustained high
vival and Nutrition, UNICEF, 7th Floor, 3 UN Plaza, New York, NY levels of child mortality, not to address interventions with
10017 (E-mail: idarntonhill@unicef.org).
The opinions in this review article are those of the authors and do not a more distal focus or ones that would normally be
necessarily the views of their organisations. implemented by sectors other than health (eg, maternal
S54
SOLUTIONS TO HEALTH PROBLEMS OF PRESCHOOL CHILDREN S55
education, reduction in crowding) meant that their micronutrient malnutrition, which was estimated to save
suggested solutions were largely dependent on health 18% of the global burden of disease if it were to
facilities and systems (2). In many of the countries most be eliminated.
affected these systems appear to be on the verge of So, what are the nutrition-related problems of pre-
collapse (12). Associated shortages of qualified staff school children mentioned in the title? As noted above,
are due to a severe ‘‘brain drain’’ to affluent countries undernutrition is a contributing factor to mortality from
(13), a high turnover and difficulty in training (14), as infectious disease in more than half of all under-age
well as an infrastructure suffering from a lack of invest- 5 deaths. Other nutrition-related problems that have been
ment in countries where poor health care is the norm. shown to have an impact on growth, development and
Donors have not been investing in health systems, learning may be divided into 4 categories, further demon-
although this may be changing (15). strating the need for a life cycle approach. As seen in
This article outlines the current burden of health and Table 1 factors act across the maternal and antenatal
disease globally, especially as related to nutrition, with an period, the infant and young child, at school, and the
emphasis on poorer countries. It then looks at the home environment.
relationships between nutrition, ill-health and education, For children under 5, undernutrition is caused directly
examines policies directed at all 3 and finally suggests by the interaction between a lack of nutritious food, the
some solutions to nutrition-related health problems of prevalence of common childhood illnesses such as diar-
preschool children, with an emphasis on education and rhoea and respiratory infections, and the impaired ability
nutrition policies. The underlying contention of the of caregivers to nurture their children because of resource
article is that the impacts of nutrition are bidirectional or knowledge constraints. Eight of the 15 major risk
in terms of education (ie, improved education leads to factors of disease identified globally are nutrition-
improved nutrition and improved nutrition leads to better related: underweight, iron deficiency, vitamin A
educational attainments). In turn, both of these lead to deficiency, zinc deficiency, high blood pressure, high
improved health and economic development. The title of cholesterol, high body mass index (overweight and
the article implies a biomedical model of identifying obesity), and low fruit and vegetable intake (17). Child
nutrition-related health problems of preschool children,
and then addressing them one-by-one. However, we
believe that a broader approach is required for a sustain-
TABLE 1. Life cycle factors affecting nutritional and
able and equitable improvement in both nutrition and educational outcomes
education. To understand what the determinants of pre-
school nutrition are and to address these factors, it is Categories Nutrition Education
necessary to also examine the health and nutrition of
Maternal and Iodine deficiency Mother’s education
older children and adults, especially women. The article antenatal Iron deficiency and Mother’s health
therefore addresses programs that improve child, adoles- other anaemias
cent and adult health and nutrition, and those including Undernutrition of Women’s status
education that intervene at key stages of the life cycle, at mother
Lack of adequate Poverty
critical ‘‘windows of vulnerability,’’ and that must be weight gain during
applied and supported at several levels of policy devel- pregnancy
opment and application (16). Infant and Not breast-feeding Hunger and
young child Iodine deficiency attention and
Iron deficiency and learning problems
CURRENT BURDEN OF ILL HEALTH AND other anaemias Play and lack of
DISEASE, WITH AN EMPHASIS ON NUTRITION Undernutrition and stimulation
inappropriate Educational level
Nearly two thirds of deaths in the 42 countries occur in complementary of parents
just 19 countries where the predominant causes are feeding
School Hunger (eg, lack of Poor facilities
pneumonia, diarrhoea, and neonatal disorders (2). A environment breakfast) Lack of stimulation
World Health Organization (WHO) estimation in 2002 Poor water and Gender bias
gave 15% as that part of the global burden of disease sanitation
that can be attributed to the joint effects of childhood and Helminths
maternal underweight and micronutrient malnutrition Home Poverty and food Educational status
environment insecurity of mother (and less
(17). A later estimation of the portion of global burden Lack of stimulation so of father)
that would be removed by eliminating malnutrition is Intrahousehold Lack of education
32% (18). Because this was based on the effects of distribution information
malnutrition on mortality and morbidity from infectious Gender discrimination Lack of support/
appropriate home
disease only, it is still a conservative figure, despite being environment for study
higher than previous estimates, mainly through including

S56 DARNTON-HILL ET AL.
malnutrition is increasingly recognized to be largely more severe infections, physical and cognitive disabil-
determined during the period of foetal and infant growth, ities, and the premature death of nearly 6 million children
when maternal nutrition has its strongest influence. In each year from the underlying causes of undernutrition
policy terms, it is therefore necessary to recognize that (2). Alarmingly, the main killers of children in 1980 were
women make up the majority of the world’s poor (19) the same as they are today (22).
and, in many situations, are particularly disadvantaged in Undernutrition remains a formidable global develop-
terms of nutrition and health (20). ment challenge because it is both a cause and a mani-
The UNICEF schematic provides a framework show- festation of poverty. Malnutrition is used here to address
ing direct causes of undernutrition: food security, care, both the prevailing chronic epidemic of undernutrition
health systems and environment (Fig. 1) (9). It then reflected in underweight and stunting in children and the
depicts that distal forces such as the political environment emergence of overweight and obesity; both affect the
are every bit as important. This is particularly true of the more disadvantaged people in most populations. World-
chronic nature of the nutrition problem. When siblings in wide, more than 180 million children under age
poor families are close in age, they compete for these 5—nearly 1 in 3—are stunted or low height for age.
constrained resources as well as for maternal care, further Stunting, along with underweight, is implicated in
increasing the likelihood of malnutrition in this high- more than half of all child deaths and is a major con-
risk group (21). In 2005, despite apparently abundant tributor to ill health and cognitive underdevelopment in
global food supplies, at least 120 million children under children (23). About 1 billion adults in developing
5 suffered various forms of malnutrition. The devastating countries are underweight, and an estimated 1.6 billion
results included underweight children, stunted growth, are anaemic, contributing to lower resistance to infection,
Manifestations
Malnutrition and Death
Inadequate Dietary Disease* Immediate Causes

Intake
Insufficient Inadequate Insufficient Health

Household Food Maternal & Child Services & Unhealthy Underlying Causes
Security Care Environment
Formal and Non-

Formal
Institutions
Basic Causes
Political and Ideological Superstructure
Economic Structure
Potential
Resources

FIG. 1. Causes of malnutrition (undernutrition and overnutrition) and death (9). Resulting in malabsorption, bacterial overgrowth and
nutrient loss in the gut.

impaired work capacity, and reduced economic pro- improvements in women’s education were associated
ductivity (24). In addition, foetal malnutrition threatens with the reduction of malnourished children by 50%
survival, growth, and development in childhood (6) and between 1970 and 1995. Many studies on women’s status
increases the risk of chronic diseases later in life (31,41). and childhood nutritional status have demonstrated that a
woman’s status has an impact on the nutritional status of
RELATIONSHIPS BETWEEN NUTRITION AND her child (37). Because women with higher status
EDUCATION (relative to men) have better nutritional status them-
selves, they are better cared for and provide higher-
The first years of life, including foetal life, are the most quality care to their children (38). Across countries,
important periods in terms of mental, physical, and relative resources controlled by women tend to increase
emotional development. It is during these critical win- the share spent on education (39). Educated girls and
dows of time that most of the basic human capital is women have fewer children, seek medical attention
formed. It is also the time, between 6 and 24 mo of age, sooner for themselves and their children and provide
that most growth failure occurs (25). Periods of increased better care and nutrition for their children (40). Education
risk are found particularly at 3 to 6 mo and 9 to 18 mo of poor girls and young women also helps reduce child
(26,27). Problems in the 3- to 6-mo period are related to and maternal mortality, enhances economic productivity,
nonexclusive breast-feeding or not breast-feeding at all, improves health and nutrition and protects girls from
and a too-early introduction of complementary foods and abuse, exploitation and exposure to HIV (35).
solids. Much of the risk at 9 to 18 mo is related to
inadequacy of nutrients in complementary feeding, ces-
sation of breast-feeding, and increases in diarrhoeal NUTRITION AND EDUCATION PROGRAMS
disease associated with exposure to pathogens in foods. Programs addressing both nutrition/health and cogni-
Stunting is associated with many negative outcomes, tive and physical development (and hence readiness for
including increases in morbidity and mortality, lower schooling) that have been evaluated and shown to have
achievements in school, reduced labour capacity and smal- had some impact are briefly considered for both devel-
ler adult stature (28), and in later life increased risk of oped and developing countries in the following.
chronic diseases such as diabetes, hypertension and heart
disease (31,41). The ability of the older child who was
formerly malnourished to learn, communicate, analyze and Early Childhood Programs in Developed Countries
socialize effectively and adapt to new environments is
profoundly affected by early nutritional status. Poor pre- Until recently it would have been considered some-
natal, infant, and child nutrition impedes behavioural and what unusual for programmes aimed at infants and
cognitive development, potential work productivity and preschoolers from developing and industrialized
reproductive health (29). Early intellectual damage due to countries to be discussed in 1 paper. As noted from a
anaemia, iodine deficiency, and chronic undernutrition in WHO/FAO (Food and Agriculture Organization) report
the infant and young child can only partially be reversed in (41), increasingly problems of undernutrition, chronic
later life (30). The damage to cognitive development and diseases and food insecurity exist in all countries world-
attained schooling among these children is likely to be long wide; in some of the poorer countries of the world, food
lasting. Early undernutrition also contributes to increased insecurity and obesity are observed in the same house-
risk for chronic disease in adulthood (31,41). Women who holds (42). Countries in Europe, particularly in eastern
were stunted as young girls can be subject to increased and northern Europe have long perceived a government’s
obstetric risk later in life and are more likely to have low obligation to ensure adequate nutrition for all children
birth weight babies. through the education system (eg, the ‘‘Oslo lunch’’). In
Identifying the constraints to achieving gender parity Australia and the United Kingdom, primary school-
in education, it is notable that mother’s education is a key children in the 1950s received one third of a pint of milk
determinant (ie, children whose mothers had no edu- every school day. The United States had a more targeted
cation are more than twice as likely to be out of school). approach based on socioeconomic need. Other countries
Other factors include poverty and geographic location. such as Chile started with programmes for all children,
The impact of inadequate nutrition and hunger on the which were highly successful in a country that was poor
ability to learn and concentrate has been conclusively at that time (43). Although it is recognized that obesity is
shown (32–34). School enrollment, attendance, pro- now more of a problem than undernutrition, it is politi-
gression and learning capacity both improve with cally unacceptable to halt the programme (Uauy, personal
improved nutrition of the preschool- and school-age child communication), and which probably should not happen
(32,35). because it is more important to alter the kinds of
Smith and Haddad (36) have convincingly demon- foods being supplied to disadvantaged children. Here
strated that in the 63 developing countries they studied, we briefly describe 2 major, US-based programs as

illustrative of 1 possible approach taken by an and together are a comprehensive child development
affluent country. program that aims to prepare children for success in
The Special Supplemental Nutrition Program for school by providing education, health, nutrition and
Women, Infants and Children (WIC) is the largest supple- social services components for children and their
mental nutrition program in the industrialized world families. In addition to educational activities, Head Start
serving 7.5 million participants annually. WIC partici- provides meals and snacks, which provide at least one
pants are from low-income families, and the program third of nutrition requirements. Children who arrive at
targets pregnant, breast-feeding and nonbreast-feeding Head Start without breakfast are given a morning meal.
postpartum women, and infants and children up to their Infants and toddlers are given foods that are appropriate
fifth birthday. It provides supplemental foods, nutrition to their developmental needs. In 2000 Head Start served
education and serves as an adjunct to health care. Preg- 857,664 children through 2060 agencies throughout the
nant women and preschool-age children receive 900 United States. The Head Start program has an ongoing
supplemental kilocalories per day from a food package monitoring system. The latest findings from 2004–2005
including milk and/or cheese, eggs, cereal, juice and (47) indicate:
peanut butter. Breast-feeding mothers are given a some-
Head Start preschoolers were twice as likely as
what larger package of supplemental food. Nonbreast-fed
infants receive iron-fortified formula and iron-fortified non–Head Start preschoolers to use center-based
cereal. WIC is operated by the US Department of care in 2003.
The largest impact on cognitive development of
Agriculture (USDA) at the national level through local
health centres and local health authorities at the children is in prereading skills. In a comparison of
community level. 3 and 4 y olds in Head Start to the lower risk cohort
The WIC program began in 1972 as a 2-year pilot of all 3 and 4 y olds in the United States, researchers
project serving 100,000 people with a total budget of found that Head Start participation of 1 y cut the
US$20 million. In 2004, WIC served 7.5 million people gap in cognitive skill levels to half of what would be
with an annual budget of US$5.235 billion in fiscal year expected without the program.
Among the 3-y-old age group, the frequency and
2005. Despite the exponential growth in the funding and
participation in WIC, the program initially had a stormy severity of behaviour problems reported by parents
history. In 1972 the USDA attempted to block the release were lower for children in the Head Start group
of funds designated for WIC. A major argument against compared with children in the non–Head
the creation of WIC was that evaluations of supplemental Start group.
For both 3 and 4 year olds in Head Start, dental
food programs in poor countries around the world had
failed to demonstrate significant improvements in neo- health was better than for non–Head Start children
natal outcome or preschool nutritional status (44). of a similar age.
Indeed, a later seminal report by Beaton and Ghassemi
(45) of more than 200 supplementation schemes world- The nutritional profile of the at-risk WIC population
wide concluded that the programs were expensive for the has changed from 1972 to the present day. Similar to the
benefit produced. Some policy makers therefore argued experience in Chile, problems of overweight and obesity
that the WIC program was unlikely to be effective in a are more common in the preschool population than
country as wealthy as the United States. Ultimately the underweight, low energy intake and nutritional
USDA was sued, lost the case and the WIC program deficiencies. Research is under way to identify new
was implemented. approaches combining WIC services to prevent over-
From the mid-1970s to the mid-1980s a series of weight and obesity (46,48). The challenge will be that
evaluations of the WIC program were conducted. healthier, lower energy (calorie) foods tend to be more
Although each of the studies had different strengths expensive per unit of dietary energy and if fresh, logistics
and weaknesses, taken together they collectively and availability are often constrained in poor populations
indicated that WIC participation is associated with sig- (46). Nevertheless, the evaluations have demonstrated the
nificant improvements in neonatal outcomes, haemato- synergistic effects of such food-based interventions in
logical status, dietary intake and nutritional status. This improving cognitive skill levels while having a positive
body of evidence also concluded that the positive effects impact on health, nutritional and behaviour problems.
were most dramatic in the higher-risk individuals; thus
the effects of WIC on birth weight and increased gesta- Early Childhood Development Programs in
tional age were most pronounced in teenage, under- Developing Countries
weight, and unmarried females, particularly those who
smoked tobacco products. Much of the work in developing and transitional
Head Start (3–5 y olds) and Early Head Start (<3 y economy countries has been relatively small-scale
old) serve the same target low-income population as WIC research or pilot studies. Chile and several centrally

planned economies have been among exceptions to this loan from the International Development Association, the
but have been, again except for Chile, relatively under- concessionary lending affiliate of the World Bank (52).
evaluated and rarely bought to scale (43,48). A review by The project covered a population of 15.6 million in
WHO demonstrated the potential of combining interven- 59 thanas (a locality with a population of 200,000–
tions that enhance early childhood development and 450,000). The project was designed on the assumption that
those that improve child health and nutrition into an poor caring practices are an important cause of malnu-
integrated model of care. WHO was able to conclude trition and that a change in caring practices will lead to a
this by reviewing a series of efficacy studies as well as decrease in malnutrition. Key objectives were to be
scaled-up effectiveness interventions (34). The effective- achieved through education: to improve the capacity of
ness studies included Integrated Child Development individuals, household, communities and national institu-
Services from India, Head Start from the United States, tions to prevent and alleviate malnutrition. Supplementary
Homes of Well-being from Colombia and others from food was given to children with severe malnutrition or with
Brazil, Indonesia, Peru and Thailand (34). growth failure (53). The basic model of the project was
One of the few longer-term studies of effect of protein borrowed from the Tamil Nadu Integrated Nutrition Pro-
and/or energy supplementation occurred in 4 rural villages ject, a large-scale nutrition intervention project in India
in Guatemala. A longitudinal study (1969–1977) of chil- started in 1980 with a US$32 million credit from the
dren ages birth to 7 y old was followed by a cross-sectional International Development Association. The project
study when the same children were 11 to 24 y (1988–1989) aimed to reduce severe and moderate malnutrition among
(49). In the follow-up cross-sectional study there was a children under 4 y old by half, infant mortality and vitamin
particular interest in children whose mother had received A deficiency, and anaemia in pregnant and nursing women.
the protein/energy supplement prenatally and then during The project reduced severe malnutrition among children
the first 2 y of life. Supplementation of children was found 6 mo to 5 y old by half, but with limited impact on moderate
to have long-term nutritional and cognitive effects. In the malnutrition and anaemia, and a large number of those who
initial study, supplementation was associated with signifi- graduated from feeding centres relapsed. The second
cantly increased birth weights, lower infant mortality and Tamil Nadu Nutrition Project began in 1991 to address
improved growth rates for children up to 3 y of age in these problems. A key change was the addition of pre-
children receiving the protein/energy supplement (49); the school education to the program. The idea was to provide
follow-up study found long-term effects persisted, includ- nutrition, health and preschool services to young children
ing greater height, particularly in females, and improved under 1 roof. A strategic change was the focus on expectant
work capacity in males. In addition, long-term effects on mothers, who would receive a full range of antenatal
cognition persisted. Adolescents who had been given the services, including iron and food supplements, instead
protein/energy supplement in early life scored signifi- of only those who showed faltering growth. The project
cantly higher on tests of knowledge, numeracy, reading design stressed beneficiary participation through groups
and vocabulary than teenagers receiving the lower-energy for women and adolescent girls and special community
supplement. The authors, from a rigorous analysis of the organisations (54).
data, concluded, ‘‘nutritional differences provide the stron- In Africa a large nutrition programme was initiated in
gest explanation for the test performance differences 1982 in the Iringa region of Tanzania with the assistance
observed in the follow-up’’ (50). of UNICEF and WHO and has since been partly repli-
The best achievable results of an integrated health and cated in many other African countries. The scheme
nutrition programme probably come out of the Narang- addressed food production, infant physical growth
wal study in India (51). Health care plus nutrition monitoring and health-related activities. Communities
supplementation of high-risk women and their children and villages in the Iringa region set up their own day
resulted in a significant decrease in neonatal and infant care centres, with the villagers paying from their own
mortality and decreased infant morbidity. There was also resources for up to 70% of the wages of the day care
an increased weight and height in participating children. attendants. In 4 y the prevalence of moderate under-
Worth noting is that this was a well-controlled research nutrition dropped from 50% to 37% and that of severe
study and thus may be the upper limit of effects that undernutrition from 6% to 2%. Attendance at the weigh-
would be expected from an integrated health and ing clinics rose from 25% to 80% (55,56).
nutrition program. The WHO review of interventions for physical growth
The Bangladesh Integrated Nutrition Project (BINP), and psychological development (34), since confirmed by
implemented by the government of Bangladesh, Ministry other evaluations, was able to demonstrate from such
of Health and Family Welfare, between 1996 and 2002 had large-scale programs the following:
the aim of reducing the prevalence of severe underweight
by 40% and moderate underweight by 25% in young Nutritional interventions significantly improve
children in the project areas (52). It was largely funded physical growth in poor and malnourished popu-
by the Bangladesh government through a US$59.8 million lations.

Combined interventions to improve both physical funding is related to the achievement of goals, such as
growth and psychological development have an reduction of undernutrition prevalence and expansion of
even greater impact in disadvantaged populations at prevention of anaemia, and to outcomes such as
risk for malnutrition. improved growth and development.
Full-scale programs that include both nutrition and Adequate and targeted human and financial resources
psychological components have been implemented are required (16,59), as well as improved ways to track
throughout the world. such investments. As noted by the Commission on
The effects of such combined programs are often Macroeconomics and Health, a substantial proportion
greatest for children <3 y old and those who are of the required funds for programs aimed at improving
most malnourished (eg, in Jamaica) (32), and these health and national development by addressing nutrition
findings have obvious conclusions for policy. and education, amongst other inputs, could be largely
mobilised from within the countries themselves; for a set
It is important to define what the large-scale interven- of essential interventions costing $34/person/y and for all
tions require to be achieved at a minimum to be seen as age groups, even the least-developed countries could
successful. Purely in terms of growth, several critical raise $15/y by 2007, leaving $19 to come from inter-
studies have questioned the total success of the Tamil national assistance (59). As also noted by the Bellagio
Nadu project and Bangladesh Integrated Nutrition Pro- Child Survival Study Group in 2003, human resources are
ject because evaluations (internal and external) were not at least as important as financial resources, especially at
able to demonstrate significant improvement in nutri- the country and community levels.
tional status due to the interventions’ inputs. There were There are 4 levels of policy that will have positive
however, many other gains documented, particularly in effects on nutrition and education outcomes and the
terms of nutrition knowledge and practices of caregivers, resultant additional and larger national impacts of such
antenatal care and immunisation coverage (53). Specific outcomes. As WHO has demonstrated, policies that
components such as child growth monitoring, strength- promote integrated programs addressing nutrition and
ening the health infrastructure, health education, and early childhood development have a synergistic outcome
women’s activities have had variable success. As in other (34). These levels could be grouped as family/community
nutrition success stories, government and community (micro); district/health systems (meso); national policies
commitment are essential. Longer sustainability has been (macro); and global (or mega) (Fig. 1, Table 2).
more difficult to ensure. The high levels of inputs
required of the donor community can lead to failure Family/Community
when these cease, and thus larger antipoverty efforts
are also essential. Environmental factors such as a Family/community would correspond in Figure 1 to
tradition of local participation, supported by national inadequate dietary intake and disease, as well as part of
policies that can improve basic equity, literacy, local the underlying causes such as insufficient household food
governance and engagement are crucial for the success security and inadequate mother and child care. It has been
of such programs. demonstrated that an estimated 66% of the >10 million
deaths among children under 5 y could have been pre-
SOLUTIONS vented by interventions that are available today and are
feasible for implementation in low-income countries at
If the reality were as simple as the title of this article, high levels of population coverage (2). Breast-feeding
the solutions would not be still being discussed here. and oral rehydration therapy alone are estimated to be
What we have done is to take an evidence-based able to prevent 13% to 15% of all under-age 5 deaths,
approach on what may work. Some factors are clear: respectively. Complementary feeding could reduce 6% of
interventions need to be supported through all levels of all under-age 5 deaths, zinc to reduce diarrhoea and
policy and administration, integrated, properly financed pneumonia deaths by 5% and vitamin A could reduce
and sustained. Successful examples, such as Chile (43) 2% of all under-age 5 deaths (60). Hence, among children
and other evaluations have shown various positive living in the 42 countries with 90% of child deaths, this
impacts (29,34,56–58). It is often the case that solutions group of effective nutrition interventions could save
are proposed that take a problem analysis and then make about 2.4 million children each year (25% of all deaths).
a link with a needs assessment. The loose relationship The key long-term nutrition improvement lies in
between the 2 analyses results in a long list of program family and community action to prevent and treat under-
and policy options. A more challenging task is to match nutrition. This requires harnessing the resources of gov-
the problem with the needs and then prioritise actions. It ernments, civil society, and the private sector to empower
is important to be able to assist policymakers and pro- individuals, families, and communities with knowledge
grammers to respond to the problem analysis by devel- and to support them with services, including universal
oping models that show how the amount and allocation of access to reproductive health services. It also requires

TABLE 2. Matrix of possible nutrition intervention recommendations by the 3 levels of causation in Figure 1
Underlying causes (district and
Immediate causes (family/community) national systems) Basic causes (institutional/political/global)
Problem Recommended action Problem Recommended action Problem Recommended action
Inadequate " dietary quality Insufficient Home gardening Formal and " women’s status
dietary intake " household food security household Biofortification informal " women’s education
food security Agricultural/horticultural institutions
extension
Availability Home gardens Improved market and Political and # inequities and
Improved intra-household transport systems ideological discrimination
distribution Improved intrahousehold superstructure # inequities in global
Home-based fortification distribution trade structure (eg, by
Biofortification reducing agricultural
Accessibility Home gardens Inadequate Female education subsidies in wealthy
Microcredit maternal and Nutrition education countries)
Nutrition education child care Breast-feeding promotion # poor governance and
(especially females) Baby-friendly Hospital Initiative corruption
Targeted food subsidies Adequate complementary Facilitative legislation
feeding for fortification
Fortified complementary
foods
High levels of disease
Prevention Child survival interventions Insufficient Strengthen health services Economic # inequities and
such as micronutrients health services by increased national structure income disparities
Antenatal care Breast- allocations (and donor " global investment
feeding Appropriate support where appropriate) in agricultural/
complementary feeding Free access for very poor horticultural research
people and development
Global measures (eg, to # inequitable impact of
restrict recruitment) globalisation on very
Career structures for poor people (eg, by
nutritionists explicitly pro-poor
policies
Ensure appropriate
private sector
involvement
(eg, fortification
Therapeutic Child survival interventions, Unhealthy Water and sanitation
including neonatal actions environments measures Reduction
such as early initiation of of discrimination and
breast-feeding marginalisation
A more detailed discussion of intervention options can be found in publications from, eg, the United Nations (eg, FAO, UNICEF, WHO), projects of
government bilateral agencies (eg, A2Z, FANTA, the Micronutrient Initiative) and international nongovernmental organisations (eg, HKI, Save the
Children) (1,5–7,9,11,14–16,25,27,32,36,38,41,43,44,46,72).
much greater emphasis on enhancing nutrition knowl- first 6 mo. Increasing women’s income and control over
edge at the household level. This means increasing family assets is critical. Focusing on disadvantaged
people’s access to both formal and informal sources of groups and ensuring opportunities for girls’ education
nutrition education and information. It also means stan- will make a difference, as will efforts to address inequity
dardising messages based on best practices, tailoring the in gender roles and women’s entitlements.
communication method to local cultural norms, investing
in the measurement of impacts, and systematising the District/Health Systems
use of information across all aspects of nutrition
programming. Micronutrient deficiencies can be Policies and programs are needed that address the scal-
addressed through supplementation, home fortification ing-up of known positive household behaviours, including
and other food-based interventions. Public action feeding practices, especially exclusive breast-feeding and
should include strong community initiatives to support appropriate complementary feeding (27), but also adequate
breast-feeding. The HIV/AIDS pandemic has illustrated micronutrient intake and appropriate intrahousehold food
that in resource-limited settings, exclusive breast-feeding distribution, and health-seeking behaviours and knowl-
by HIV-infected mothers may be lifesaving if done for the edge. Insufficient household food security and mother

and child care are reflected at this level, because although In Thailand, where nutrition has improved remarkably,
they have the most impact at the household level, the causes women enjoy high literacy, high participation in the
are usually beyond the control of the household. labour force, and a strong place in social and house-
Starting life as a low birth weight baby leads to poor hold-level decision making. Within India, women have
child nutritional status and is directly related to the similarly better relative status in Kerala as compared to
mother’s health before and during pregnancy. Expanding other states and the state has better health, social and
access to reproductive and antenatal health care and nutrition indicators and, not coincidently, the highest
ensuring adequate nutrition has been conclusively levels of female education (67). There are other
demonstrated to greatly enhance the health of mothers examples: Chile, Costa Rica, Cuba, Sri Lanka (and
and their children (61). Improvement of nutrition edu- others), where even at relatively low per capita income,
cation delivered through health services has been shown health indicators remain far better than in other countries
to decrease the prevalence of stunted growth in childhood with higher per capita incomes (15,68). Conversely, in
in areas where access to food is not a limiting factor (14). settings that experience little nutrition improvement
Conversely, food distribution serves as a strong incentive despite economic growth, social discrimination against
to use health care services (62). women is common (67). In Pakistan, for example, wide-
Efforts to increase educating women and girls are spread discrimination against girls and women is high
essential. The provision of food to children at school is and child malnutrition rates are among the highest in the
only the basic element of a school feeding program world, as is the proportion of low birth weight infants, at
and will have only a relatively minor impact on 25% (67).
nutritional status at that age. However, food for Poverty-oriented approaches are much more likely to
schoolchildren represents a contribution of food and be accepted in environments characterised by a strong
nutrients as well as an income transfer for the family commitment to equity among policymakers and pro-
and often additional resources for the school and gramme managers. Developing and maintaining such a
community. The primary objective of a snack or meal commitment to equity is more probable if policymakers,
is to alleviate short-term hunger (63,64). Meals provided programme managers, and communities feel that they are
early in the day to alleviate hunger will result in children being involved in policy formulation. Several types of
being more attentive and to children being enrolled for monitoring and reporting can provide useful information
longer periods (32). Nevertheless, it is critical for a school for policymaking: the simple measurement of health
to provide a minimum standard of educational quality for a status and programme use disaggregated by socioeco-
snack or meal to be effective. Although school meals have nomic status, gender, or ethnic group; another is the
been shown to improve enrollment and attendance establishment and monitoring of health objectives in
(50,65,66), food alone is insufficient to bring about terms of health status or service use among disadvan-
changes in educational outcomes. It is the combination taged groups. Food distribution often does not have
of well-motivated and well-trained teachers, appropriate clearly stated objectives, lacking specificity and clear
curricula, support and related materials, and infrastructure time frames (62). Nevertheless, a subsequent review of
together with good nutrition and health care (eg, deworm- food supplementation programs by Ghassemi a decade
ing, micronutrients) that translates into improved perform- after his earlier review (45) was much more optimistic.
ance (63,64). He considered food supplementation to be a further type
of intervention, especially as an income distribution
device, and for improving nutritional outcomes in the
National Policies and Actions poorest people. The establishment of monitoring mech-
anisms to track progress among the targeted groups
Few of the above interventions will be effective in a reinforces their effectiveness (69). Equity must be a
nonsupportive environment. The supportive environment priority in the design of interventions and delivery strat-
must be provided by functioning national governments or egies, including accountability at national and inter-
sometimes subnational or even district governance. The national levels (69). The first goal of the Millennium
importance of supporting action at community and dis- Development Goals (MDGs), poverty and hunger
trict levels can be demonstrated by the changes in iodine reduction, should be brought together with the other
sufficiency when, for example, national legislation or goals, producing synergistic effects on under-age 5 y
regulations on the appropriate iodisation of salt are not child survival and development through mechanisms
enforced or are rescinded, as happened in India (which already proven (16).
has wisely reimposed a national mandate that all salt
should be iodized; Schultink, personal communication, Global
2005). Both formal (government) and informal (non-
governmental) institutions are essential, as is a function- The importance of both nutrition and education to a
ing and responsible private sector. nation’s development has been acknowledged in the

importance given to these 2 sectors by the Millennium challenge, which is now being heard, for example, at the G8
Declaration and the MDGs: 8 goals accepted by virtually Summit and at the UN High Level Plenary in New York, is
all nations, affluent and least developed (40). Political, whether resources and commitment will be sufficient.
ideological and economic structures are seen as the most Of the measurable health goals, the world is further
basic causes, and the causality is likely to be stronger from achieving the one for child mortality—a two-thirds
with increasing globalisation. It is contended that by reduction by 2015—than any other (72). Universal edu-
extending the coverage of crucial health services, includ- cation may seem a relatively straightforward goal, but it
ing specific interventions, to the world’s poor, millions of has proven as difficult as any to achieve. So many
lives each year would be saved, poverty reduced and countries around the world that will fall far short of
economic development accelerated, and all of these the MDGs in the remaining 9 y to 2015 points to an
results would help promote global security (59). Inter- urgent need to change course (73).
national goals are 1 mechanism at this level; the MDG’s In conclusion, the reasoning and evidence above
are partly an expression of humanitarian concern, but suggests the following:
they are also an investment in the well-being of the rich
countries as well as the poor (59). Malnutrition and To accelerate economic development, it is necess-
disease breeds instability in poor countries, with ary to improve health, nutrition, education and
rebounds to the security of rich countries. A high infant gender parity.
mortality rate was found to be 1 of the main predictors of To improve each one of these will have a positive
subsequent state collapse in a study of state failure during impact on the others, and conversely, not addres-
the period 1960 to 1994 (59). International agreements sing one will impede progress in another: con-
and trade and other global agreements and laws can have sequently programs need to be integrated.
both positive and negative effects on education and Equity is both a right and an obligation, but it will
nutrition at the community level. At present, the evidence also accelerate the development process. To ensure
suggests (at least in sub-Saharan Africa) that the impact equity, governments must take an active role.
of these international trade laws have been largely nega- Reliance on market forces alone is not appropriate
tive for the poor (10). Others have also argued that 1 of when there are extremely poor populations and
the negative impacts of globalisation has been a sub- weak infrastructures for health, education and other
stantial reduction of public spending, particularly in the systems. Consequently, both government and
areas of education and health care (70). global commitment are essential.
For improved outcomes in the under–age 5 y age
CONCLUSIONS group, there is a need to address life stages outside
of this period, particularly maternal and antenatal
In terms of possible solutions, 4 levels have been dis- health, nutrition and education; thus antenatal
cussed: (1) microlevel changes at community and house- programmes are essential, as is breast-feeding
hold levels, especially in terms of gender equity and promotion and appropriate complementary feeding.
nutrition education and scaling-up of proven child survival Accelerating programmes aimed at adolescents
interventions; (2) known and proven interventions at a seems logical based on the available evidence, but
district level, such as strengthening health systems and further assessment of their impact is needed.
making them more effective and accessible; (3) national, Improvement of community involvement continues
such as pro-poor development and economic policies, to be invoked, but is still infrequently done
policies towards parity in education and improved acces- adequately; the same could be said of upfront
sible health systems; and (4) global policy and the reduction planning for monitoring and evaluation.
of inequities (Table 2). To implement these proven inter- Biomedical or vertical models to address nutrition-
ventions, there is a need to prioritise choices for interven- related health problems are insufficient, although
tions, apply them based on negotiated actions with the effective nutrition education and other nutrition
affected communities and individuals; and support them by interventions can be delivered successfully through
appropriate policies and programmes. There is at this point health services.
no need to reinvent wheels. Differential rates of improve- Structural and political changes are also needed to
ment in stunting were recently reported to be due to support interventions, as are adequate and consist-
improved immunisation rates, improved water and sani- ent family, community and donor support.
tation and improved female literacy rate, as well as Although apparently not cheap, interventions such
economic and agricultural variables, none of which is a as those outlined above are cost-effective, especi-
surprise (71). Achieving the MDGs would address the ally when contributions to national economic
nutrition-related concerns and educational needs (eg, cog- development are assessed properly.
nitive development, forming social skills and preparedness The achievement of the MDGs remains an
for schooling) of under-age 5 y old children (16). The appropriate overarching policy goal to provide

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Priorities in Nutritional Rehabilitation

Stanley Zlotkin
Division of GI Hepatology/Nutrition, Department of Pediatrics, Hospital for Sick Children,
University of Toronto, Toronto, Ontario, Canada
ABSTRACT
This review examines nutritional rehabilitation and stresses nutri- childhood. JPGN 43:S66–S71, 2006. Key Words: Nutrition—
tion prophylaxis or prevention because for school-age children, Rehabilitation—Global risk factors—Malnutrition—Obesity—
health promotion and disease prevention are the keys to a healthy Iron deficiency anaemia. # 2006 Lippincott Williams & Wilkins
INTRODUCTION UNDERWEIGHT
Although the focus of this article is nutritional reha- All ages are at risk, but underweight is most prevalent
bilitation, ‘‘rehabilitation’’ suggests that the insult has among children under 5 years of age, and the World
already occurred and that an intervention is needed to Health Organization (WHO) estimates that globally
ameliorate the problem. This review stresses nutrition 27% of children in this age group are underweight.
prophylaxis or prevention because these are the keys to a It is estimated that underweight was associated with 3.4
healthy childhood. million deaths in 2000, including about 1.8 million in
Research on children in the preschool age range is Africa and 1.2 million in countries in Asia. Underweight
limited, therefore, this article identifies the most import- is considered to exist as a contributing factor in 60% of all
ant contributors to morbidity in preschool children. The child deaths in developing countries (1). Excluding North
10 leading risk factors globally in terms of burden of America and western Europe, there is a strong gradient of
disease they cause are shown in Table 1 (1). Together, increasing child underweight with increasing absolute
these factors account for more than one third of all deaths poverty (see Fig. 1). The strength of the association varies
worldwide. Of these 10 causes, 5 have direct relevance to little across regions. People living on <$1/d generally are
preschool-age children, and 3 of the 5 are nutrition at 2- to 3-fold higher relative risk compared with people
related. Clearly, nutrition has a huge bearing on the living on >$2/d. Clearly, poverty or the eradication of
health of preschool-age children. The 3 nutrition-related poverty will have a huge impact on underweight in
causes include underweight, obesity and iron deficiency. children.
This review focuses on these 3 conditions, on what the The etiology of underweight and growth deficits has
literature has to say about nutritional rehabilitation and been widely studied. Underweight and growth deficits
prevention and what has been dubbed the ‘‘nutrition are linked to impairment in terms of physical work
paradox’’ (2,3). This paradox is described as having capacity, cognitive skills and increased risk of morbidity
underweight, obesity and micronutrient deficiencies in and mortality. Thus, as reflected in the WHO documen-
the same country, even in the same household at the same tation, these 2 factors are important. Underweight in
time. preschool-age children is a combination of low birth
weight, inadequate quantity and quality of complemen-
Address correspondence and reprint requests to Dr Stanley Zlotkin,
tary foods, limited breast-feeding and limited variety of
555 University Avenue, University of Toronto, Toronto, ON, M5G 1X8 appropriate postweaning foods. Combined with these
Canada (e-mail: stanley.zlotkin@sickkids.ca). nutritional causes of underweight are environmental
The research on ‘‘Sprinkles’’ was generously supported by grants conditions that predispose to poor child care practices
from the US Agency for International Development OMNI Research and recurring infections. A lack of sanitary conditions,
Program through the Human Nutrition Institute of the International Life
Sciences Institute Research Foundation, the Canadian Institutes of
especially clean drinking water and refrigeration, exist as
Health Research, HealthCanada, the International Atomic Energy the cause of recurrent enteric infections, which lead to
Agency, and the H.J. Heinz Company Foundation. anorexia and chronic poor food intake.
S66
PRIORITIES IN NUTRITIONAL REHABILITATION S67
TABLE 1. 10 leading global risk factors between the 1960s and 1980s suggest that environmental
constraints affected growth in the past. Growth and
Factors impact health of
preschool children? development surveys of children under 7 years of age
in China reported a marked increase in both weight and
Underweight Yes length of infants from 1975 to 1985. This improved
Unsafe sex No growth was possibly the result of the better economy
High blood pressure No
Tobacco consumption No
and food availability. During the same time period, a
Alcohol consumption No similar change was observed in 2- to 18-year-old Hong
Unsafe drinking water, poor Yes Kong children and adolescents. It is interesting to note
sanitation and poor hygiene that as early as the mid-1980s there was a tendency for
Iron deficiency Yes Hong Kong Chinese children to be overweight.
Indoor smoke from solid fuels Yes
High cholesterol No The second example is the migration of Mayan refu-
Obesity Yes gees from Guatemala to the United States (4). Guatema-
lan Mayans illustrate the ‘‘genetics versus environment’’
argument because at one point in history, they were
Although it has been argued that there is a genetic considered a ‘‘pygmy’’ people of the Americas. They
component to the poor growth of preschool-age children are, in fact, not pygmies. Comparing the height of Mayan
in the developing world, several lines of evidence suggest children in their home villages versus those who moved
that environment, including the social, political and to 2 cities in the United States, they are taller, heavier and
economic environment, and not genetics explains growth carry more fat and muscle mass than Mayan children
faltering and underweight. Indeed, the consensus of living in Guatemala. Within the same generation, Mayan
research is that physical growth and development are children ages 4 to 14 years old growing up in the United
sensitive indicators of the quality of the social, political States average 5.5 cm taller than their age-peers living in
and economic environment (4). For example, changes in Guatemala. It is believed that the short stature of a
birth weight and growth of children who emigrate to the population is a proxy for an ecology for human devel-
developed world tend to support the role of environment. opment that results in nutritional deficiency, excessive
Ramakrishnan and Yip have documented that the mean energy expenditure and poor health. Migration, in many
birth weight of Chinese infants born in China are lower cases, breaks the cycle of poverty into which Guatemalan
than Chinese infants born in the United States (5). Mayans are born. The political economy of Guatemala in
Chinese infants born in industrialized countries do not the mid-1990s created an ecology for human develop-
show the typical growth faltering seen at 4 to 6 months of ment that deprived most Guatemalan Mayans of suffi-
age. Wheeler and Swee (6) studied Chinese infants living cient food, health care, drinking water, education and
in London in the 1980s. The families provided traditional other basic needs. At the same time, the political
Chinese foods as well as popular English foods to their economy of the United States offered economic, nutri-
children. These children grew at a similar rate to their tional, educational and public health benefits unavailable
UK counterparts for the first 2 to 3 years of life. Secular to most Guatemalan Mayans.
growth changes also reflect the role of environment in The sample in Florida and California described by
determining growth potential. Secular changes in growth Bogin and Loucky (4) is, on average, taller than any
in Chinese children in both China and Hong Kong sample of Guatemalan Mayans and taller than many
FIG. 1. Prevalence of moderate underweight in children by average daily household income by subregion.

S68 ZLOTKIN
samples of low-socioeconomic-status Ladinos of Guate- Nutritional transition may be defined as a country in

mala. However, this American sample of the children of the midst of changes in diet, changes in food availability
refugees is still significantly shorter in stature than the and changes in lifestyle. These transitions typically occur
other ethnic groups in the towns in which they live. These in countries experiencing socioeconomic and demo-
results suggest that human phenotypes change at different graphic changes. Examples of these countries include
rates for different traits. The present generation of Mayan Kyrgyzstan, Indonesia, Russia, Brazil and China. In such
refugee children is likely to be in the first stage of a countries, as many as 60% of households with an under-
process of increasing stature from generation to gener- weight family member also have an overweight one, a
ation. Classic examples of this secular trend in growth situation that has been dubbed the ‘‘dual-burden house-
of migrant children and more recent follow-up studies of hold’’ (3). According to WHO statistics, among middle-
these same populations show that over time the height of income countries (ie, those with a per capita gross
each generation of the children of migrants continues to national product [GNP] of $3000/y), overweight ranks
increase until it converges on that of the host population. fifth among the top 10 causes of disease burden, right
Perhaps the best example of this phenomenon comes below underweight (1). This is the same position held by
from Mexican immigrants to the United States who have overweight as a cause of disease burden in the developed
become taller on average, with each generation, since the world.
1930s. The most recent generation of US-born Mexican Traditionally, obesity has been linked with affluence
Americans under 12 y old has mean heights that are equal and abundance, whereas undernutrition has been linked
to the National Center for Health Statistics references (7). with poverty. As Caballero has suggested (2), it was
Much of the existing research on the factors influen- anticipated that as developing countries improved their
cing plasticity in human phenotypes focuses on the economic status and their GNP, undernutrition would
physical environment, for instance, the hypoxia of high improve and obesity would become worse, especially
altitude, the cold and heat of extremes in latitudes or the among members of the upper socioeconomic classes. The
nutritional stress experiences in traditional agricultural relationship between the economic status of a country
communities. Often, little can be done to alter the and the prevalence of obesity is not straightforward,
physical environment and variation in human physical however.
and behavioural phenotypes is ascribed to inevitable
accommodations to them. However, all people live within HEALTHY RISK FACTOR TRANSITION
social, economic and political environments that also
have powerful effects on human phenotypes. It is the The nutritional transition encompasses changes in a
author’s hope that much can be done to change the social, range of risk factors and diseases. Traditionally, the
economic and political environment to influence growth dietary energy intake of the poorest people in a country
and undernutrition through peaceful change. may be limited by their inability to purchase enough food
and the high energy demands of manual labour and daily
OBESITY survival activities. It is difficult for this group to achieve
a net positive energy balance and therefore to gain
In his preamble to the 2002 WHO World Health weight. In more urbanized developing countries with a
Report, Dr Gro Harlem Brundtland stated, ‘‘Two of higher GNP, widespread access to television and mech-
the most striking findings in this report are to be found anisation would favour sedentary activities and reduced
almost side by side. One is that in poor countries today daily energy expenditure. At the same time, as a country
there are 170 million underweight children, over three develops and more people buy processed food rather than
million of whom will die this year as a result (1). The growing and buying raw ingredients, an increasing pro-
other is that there are more than one billion adults portion of energy tends to be drawn from sugars added to
worldwide who are overweight and at least 300 million manufactured food and from relatively cheap oils. Along-
who are clinically obese. Among these, about half a side the change in diet, changes in food production and
million people in North America and Western Europe the mechanics of work and leisure result in a decrease in
combined will have died this year from obesity-related physical exercise. Thus, the consequent epidemic of diet-
diseases. Could the contrast between the haves and the related noncommunicable diseases, including obesity,
have-nots ever be more starkly illustrated?’’ It has diabetes, hypertension and cardiovascular disease coex-
recently been suggested by Dr Benjamin Caballero that ists with residual undernutrition, especially micronutrient
the combination of underweight in children and over- undernutrition, and is projected to increase rapidly. For
weight in adults occurs at the same time in the same example, in India and China a shift in diet towards higher
household in developing countries. He called this a fat and lower carbohydrate is resulting in rapid increases
nutritional paradox (2). in overweight among all adults in China and mainly
The nutritional paradox is most frequently found in among urban residents and high-income rural residents
developing countries undergoing economic transition. in India. Countries that have completed the transition to

overnutrition are experiencing a continual increase of comparable nationally representative dietary surveys
in levels of obesity, as high-fat, high-energy and low- (eg, the National Nutrition Survey).
exercise lifestyles permeate their society. However, The study addresses the question of why the fat intake
such a transition may not be inevitable, and a key in the Republic of Korea is low. The authors suggest
challenge for policymakers is to generate a healthier 3 possible answers: (1) rice is still the staple food in
transition. Korea, so carbohydrate intake remains high; (2) cooking
It is somewhat self-evident that improvement in per styles use small amounts of fat because traditional
capita GNP in countries in economic transition does not Korean cuisine adds small amounts of sesame oil to
benefit all citizens equally. However, children under age vegetables after they have been boiled or steamed, as
5 y are particularly at risk in this time of transition. For opposed to Chinese cooking in which foods are stir fried
example, data from The World Bank show that the rates in oil (with stir frying, there is a tendency to use more
of poverty and underweight have actually increased oil as the availability of oil increases); (3) there has been
among children under 5 y of age in urban areas of a strong, sustained national movement to retain the
countries in socioeconomic transition. The reasons are traditional Korean diet and cooking methods. Mass
not as esoteric as may be imagined. For example, families media campaigns promote local foods, emphasizing their
that move from rural to urban areas usually lose the higher quality and the need to support local farmers. A
ability to grow their own food, lose their contact with unique training programme is offered by the Rural
extended family and become dependent for their food on Development Administration. Since the 1980s, the Rural
a cash market. It is also more likely that women who Living Science Institute has trained thousands of exten-
move to the city will join the labour force and therefore sion workers to provide monthly demonstrations of cook-
become less available to feed their children frequently or ing methods for traditional Korean foods such as rice,
prepare food at home, relying more heavily on nonfam- kimchi (a form of pickled and fermented Chinese
ily-based child care and inexpensive commercially pre- cabbage) and fermented soybean food. These sessions
pared foods for themselves and their families. Much of are open to the public in most districts in the country, and
this store-bought food is high in fat and energy but low the programme appears to reach a large audience.
in micronutrients such as iron and zinc. For example, on Although the combination of these 3 interventions may
a per-energy unit basis, a 5-y-old boy needs 5 times as explain the low fat intake, with the lowering of trade
much iron in his diet as an adult man. Cheap energy- barriers there is a trend to increasing obesity in young
dense, nutrient-poor foods may adversely affect the children, even in Korea.
growth and micronutrient status of the child but at
the same time may provide sufficient energy units for MICRONUTRIENT DEFICIENCIES
the adult to gain excessive weight.
The relationship between GNP per capita and dietary A major impact of the nutrition transition, as pre-
fat intake, expressed as a proportion of energy from fat, viously mentioned, is the ingestion of relatively large
was studied for 88 countries and recently updated to amounts of energy-dense but nutrient-dilute foods.
include 121 countries (X. Guo et al., unpublished obser- Because of the relatively high requirements for micro-
vation, 1999). Not surprisingly, there was a strong nutrients by preschool children, they are at highest risk
positive relationship between the 2, in other words, fat during the period of nutritional transition, but women of
intake was higher in richer countries. There is 1 example, reproductive age and pregnant women are also at high
however, that goes against this trend: the Republic of risk for micronutrient deficiencies. For example, rates of
Korea. Based on the regression equation between GNP iron deficiency and anaemia were higher in 2000 than
per capita and dietary fat intake and using statistics from they were in 1990. Thus, the control of micronutrient
1996, one could predict that the proportion of energy deficiencies is also high on the global priority list.
from fat in the Republic of Korea would be 35.5%. The We have done a reasonably good job in controlling
actual percentage of energy from fat was 16.7%. This low iodine and vitamin A deficiencies with iodised salt
level of fat intake may be part of the reason for the lower and vitamin A capsules; however, the international nutri-
level of obesity in the Republic of Korea as compared tion community has not yet solved the problem of iron
with many other Asian countries. There are not many deficiency.
examples of societies successfully dealing with their own Recent WHO/UNICEF estimates suggest that the
nutrition transition, but Korea is one example that is worth number of children with iron deficiency anaemia
highlighting. The study, entitled Nutrition Transition in is >750 million (8). Iron deficiency is the most common
the Republic of Korea, describes a unique nutrition tran- preventable nutritional problem despite continued global
sition that has occurred in the Republic of Korea, a country goals for its control. Historically, the problem of iron
that modernized earlier than most Asian countries. The deficiency anaemia in children largely disappeared in
analysis uses secondary data on economics, dietary intake, North America when foods fortified with iron and
anthropometry and causes of death, including a series other micronutrients became available. In this group,

S70 ZLOTKIN
the prevalence of iron deficiency anaemia has fallen from THE STRATEGY
21% in 1974 to 13% in 1994 (5). Although pockets of
infants and children remain at risk, generally the eradica- Our research group at the Hospital for Sick Children in
tion of iron deficiency in the West is recognized as a Toronto conceived of the strategy of home fortification
successful public health accomplishment. This solution with Sprinkles, single-dose sachets containing micronu-
has not worked in developing countries, where commer- trients in a powder form, which are easily sprinkled onto
cially purchased fortified foods are not available or are any foods prepared in the household. We hypothesized
not used. that this would be a successful method to deliver iron and
In the developing world, there are 3 major approaches other micronutrients to children at risk (11). The idea of
available to address iron deficiency: dietary diversifica- Sprinkles was formulated in 1996, when a group of
tion to include foods rich in absorbable iron, fortification consultants determined that the prevention of childhood
of staple food items including wheat and the provision of iron deficiency anaemia was a UNICEF priority, yet the
iron supplements. When dietary or fortification strategies available interventions including syrup and drops were
are not logistically or economically feasible, supplement- not effective (11).
ation of individuals and groups at risk is an alternative In Sprinkles, the iron provided as ferrous fumarate is
strategy. For the past 150 y or more, oral ferrous sulphate encapsulated within a thin lipid layer to prevent the iron
syrups have been the primary strategy to control iron from interacting with food. This means that there are
deficiency anaemia in infants and young children (9). minimal changes to the taste, colour or texture of the food
However, adherence to them is often limited due to a upon adding Sprinkles. Other micronutrients including
combination of their unpleasant metallic aftertaste, dark zinc, iodine, vitamins C, D and A, and folic acid may be
staining of the child’s teeth and abdominal discomfort added to Sprinkles sachets. Any homemade food can be
(10). Thus, despite the ongoing work of the UN Standing fortified with the single-dose sachets, hence the term
Subcommittee on Nutrition and others to solve the home fortification. Two formulations have been devel-
problem of poor adherence in infants and young children, oped, a nutritional anaemia formulation (Table 1) and a
all of the interventions to date have been universally complete micronutrient formulation (Table 2).
unsuccessful (8–10). Our program in Toronto, the Sprin- Over the past 5 y, we have completed 7 community-
kles Global Health Initiative, has come up with what we based trials in 4 different countries (12). The goal of these
believe to be 1 solution to the problem. studies was to test the efficacy of Sprinkles in diverse
TABLE 2. Dose and derivation of Sprinkles Complete Micronutrient Formulation for home fortification of complementary foods for
infants and young children, 6–24 mo old
6–11 mo 12–24 mo 6–24 mo

WHO IOM DRIy WHO IOM DRIy Lutter and Deweyz Upper limity Sprinkles
Vitamin A, mg RE 400 500§ 400 300 250 600 300

Vitamin C, mg 30 50§ 30 15 70–140 1000 30
Vitamin D, mg 5 5§ 5 5 1–2 25 5
Vitamin E, mg a-TE NA 5§ NA 6 NA 2000 6
Vitamin B1, mg 0.3 0.3§ 0.5 0.5 0.18 NA 0.5
Vitamin B2, mg 0.4 0.4§ 0.5 0.5 0.18 NA 0.5
Vitamin B6, mg 0.3 0.3§ 0.5 0.5 0.22 30 0.5
Vitamin B12, mg 0.5 0.5§ 0.9 0.9 0.26 NA 0.9
Folic acid, mg 80 80§ 160 150 41.5 300 160
Niacin, mg 1.5 4§ 6 6 3.3 10 6
Iron, mgô 9.3 11 5.8 7 7–11 40 12.5
Zinc mg# 4.1 3 4.1 3 4–5 5–7 5
Copper, mg NA 0.22§ NA 0.34 0.2–0.4 1 0.3
Iodine, mg NA 130§ 90 90 90 200 90

Recommended Nutrient Intake (RNI). Source: Joint FAO/WHO Expert Consultation. Vitamin and Mineral Requirements in Human Nutrition.
Geneva, Switzerland: World Health Organization; 2002.
y
Recommended Dietary Allowances (RDA). Source: Institute of Medicine (IOM). Dietary Reference Intakes (DRI). Washington, DC: National
Academies Press; 2000.
z
Recommended nutrient composition of complementary foods (per 50 g of food as daily ration) is based on a total intake of 1 RNI for all children
6–23 mo after accounting for the amounts already present in breast milk and complementary food.
§
Based on adequate intake (AI) estimates.
ô
Assuming medium bioavailability (10%).
#
Assuming moderate bioavailability (30%).

settings. When we pooled data from 2 of our studies that development of the Sprinkles initiative has recently been
compared Sprinkles to the reference standard, ferrous published (12).
sulphate drops, we had a total of 518 anaemic infants In summary, the present review has identified the top
(haemoglobin < 100 g/L) who were given 1 of 2 ferrous 3 risk factors in terms of burden of disease, affecting
sulphate doses providing 15 or 40 mg of elemental iron as preschool children. The impact of each factor on this
ferrous sulphate and 318 similar infants who received age group has been assessed, and at least 2 examples
1 of 4 doses of iron from Sprinkles providing 12.5, 20, 30 of successful approaches to rehabilitation have been
or 80 mg of elemental iron as microencapsulated ferrous suggested.
fumarate. This gave us >97% power (a ¼ 0.05) to detect
whether the mean difference in end of study haemo-
globuin concentrations between ferrous sulphate and
Sprinkles regimens was within 5 g/L (a range of equi- REFERENCES
valence). Using a random effects model for study and 1. The World Health Report 2002: Reducing Risks, Promoting
dose that adjusted for baseline haemoglobin, we found no Healthy Life. Geneva: World Health Organization; 2002.
significant difference between Sprinkles and drops. 2. Caballero B. A nutrition paradox: underweight and obesity in
We further examined this through quantile-quantile developing countries. N Engl J Med 2005;352:1514–6.
plots of haemoglobin concentrations at the end of the 3. Doak CM, Adair LS, Bentley M. The dual burden household and the
nutrition transition paradox. Int J Obes Relat Metab Disord 2005;
studies for Sprinkles and ferrous sulphate drops. The over- 29:129–36.
laid plots of haemoglobin concentrations of the Sprinkles 4. Bogon B, Loucky J. Plasticity, political economy and physical
and drops groups demonstrate that these 2 distributions growth status of Guatemala Maya children living in the United
overlapped at all quantiles. These plots clearly indicate States. Am J Phys Anthropol 1997;102:17–32.
5. Ramakrishnan U, Yip R. Experiences and challenges in industria-
that the haemoglobin response to the 2 different forms of lized countries: control of iron deficiency in industrialized coun-
iron were equivalent. Thus, we have concluded that tries. J Nutr 2002;132:820S–4S.
Sprinkles are as efficacious as the current reference 6. Wheeler E, Swee T. Trends in the growth of ethnic Chinese children
standard for the treatment of anaemia. Overall, 55% living in London. Ann Hum Biol 1983;10:441–8.
to 90% of the anaemic infants who were provided with 7. Martorell R, Mendoza FS, Castillo RO. Genetic and environemtnal
determinants of growth in Mexican-Americans. Pediatrics 1984;
Sprinkles were cured. 84:864–71.
Each stage in the evolution of the Sprinkles inter- 8. Delivering Essential Micronutrients: Iron. Available at: http://www.
vention has been evaluated in a controlled manner. We unicef.org/nutrition/index_iron.html. Accessed January 5, 2003.
determined that the use of encapsulated iron did not 9. Stoltzfus R. Defining iron-deficiency anemia in public health terms:
a time for reflection. J Nutr 2001;131:565S–7S.
appreciably change the taste or color of the food to which 10. Galloway R, McGuire J. Determinants of compliance with iron
it was added; we showed that the haemoglobin response supplements: supplies, side effects or psychology. Soc Sci Med
in anaemic infants was equivalent to the current standard 1994;39:381–90.
of practice; and we documented the acceptability of 11. Nestel P, Alnwick D (eds). Iron/Multi-micronutrient Supplements
Sprinkles among caregivers who used Sprinkles in their for Young Children. Summary and Conclusions of a Consultation
Held at UNICEF Copenhagen, Denmark, August 19-20, 1996.
homes. Finally, through various partnerships, we have Washington, DC: International Life Sciences Institute; 1997.
developed a successful model to scale up the intervention 12. Zlotkin S, Schauer C, Christofides A, et al. Micronutrient sprinkles
for countrywide use. A review of the progress and to control childhood anaemia. PLoS Med 2005;2:e188.

The Danone Institutes
Danone Institutes are not-for-profit organisations Organisation of training and education sessions
contributing to improving the quality of the diet and for professionals (eg, health care professionals,
therefore the health of all people. With this objective, journalists)
Danone Institutes promote evidence-based scientific Production of pedagogic material, leaflets, book-
knowledge in diet and nutrition and disseminate lets, television and radio programs, computer
relevant knowledge on diet and nutrition to pro- games for parents, pregnant women, children,
fessionals in fields such as health care, education and teenagers, and older adults
media as well as to the public.
Danone Institutes gather internationally renow- An international entity was created in 2004 to develop
ned scientists in diet and nutrition from independent international activities such as research support and
organisations (eg, universities, research centres) scientific conferences or publications, to enhance
who are committed to taking a multidisciplinary collaborations between Danone Institutes and/or their
approach combining medicine, biology and human members and to promote the sharing of experience
sciences. between Danone Institutes.
The programs offered by Danone Institutes may deal
ETHICS with any food or nutrient that could have an impact on
human health. They are generally focused on major
Danone Institutes are independent from the Danone public health nutrition issues.
Company. They define their own programs to be relevant
in their local environment.
ACTIVITIES
They have no commercial objective
Support for research: To date, Danone Institutes
They act freely and independently
They function on the basis of guidelines that have funded more than 700 research studies, which
guarantee a clear and democratic organisation accounted for more than s11 million.
Danone Institute publications never contain any Prizes and awards: More than 40 prizes and awards
commercial/advertising information have been attributed to outstanding professional
initiatives for more than s600,000.
Symposia, workshops and educational meetings:
HISTORY Since 1991, more than 140 events involving top-
level scientists have reached more than 30,000
The first Danone Institute was created in France in health professionals.
1991. Since then, an international network of 15 local Publications related to health and nutrition:
Danone Institutes has been developed in Belgium, Seventy-five publications and 6 newsletters present
Canada, China, Czech Republic, France, Germany, professionals with overviews of recent develop-
Israel, Italy, Japan, Mexico, Poland, Russia, Spain, ments, promote consensus and/or explore contro-
the United States and Turkey. Today, more than 200 versies about relevant issues.
renowned experts in diet and nutrition are involved in Education programs for the public: More than 70
this unique international network. In each country, the programs (eg, nutrition lectures, distribution of
local Danone Institute develops specific programs folders and brochures) geared towards the public
including the following: have been organised.
Research support through grants, credits, awards,
fellowships and scholarships SPECIAL FOCUS ON PERINATAL AND CHILD
Publication of research findings NUTRITION
Organisation of scientific conferences Proper nutrition during pregnancy and childhood is
Publication of newsletters and books for pro- increasingly understood to be a major determinant of
fessionals (eg, health care professionals, educators, growth, development and future health. Therefore, Danone
journalists) Institutes consider that encouraging good nutrition in
S72
THE DANONE INSTITUTES S73
pregnancy and childhood is the key to improving public and most recent practical knowledge on children’s
health. For this reason they dedicated a large part of their diets to pediatricians. This course, acknowledged
activities to perinatal and child nutrition. The most recent by the Italian Ministry of Health as part of the
programs include the following: program of Continuous Medical Education, is now
available online for individual training at www.
Support for research: (1) award of the 2005 Danone
istitutodanone.it. (2) The corpulence program devel-
International Prize for Nutrition (s120,000) to
oped by Danone Institute of France, encourages
David J.P. Barker (University of Southampton, health professionals to monitor the evolution of the
UK, and Oregon Health and Science University,
body mass index of children and open a dialogue
Portland) for his innovative research work on the
with parents on childhood obesity. This program, in
developmental origin of chronic adult disease
line with the national plan of the French Ministry of
leading to the so-called Barker’s hypothesis; (2)
Health, comprises a series of leaflets and posters for
partnership with the European Union Childhood
health professionals and parents.
Obesity program to test the possible relationship Educational programs for the public: (1) ‘‘Healthy
between the level of early protein intake and the
Diet, Healthy Growth’’, a television program
later risk of obesity; (3) award of several grants to
produced by Danone Institute of China, aims to
local research programs.
Organisation of scientific conferences: (1) at the educate mothers with children 6 to 16 y old about
what constitutes a healthy diet. Fifty-two episodes
local level: ‘‘Child Nutrition and Development’’
of 10 min each were shown on 5 national television
(Danone Institute France, 2005), ‘‘Early Nutrition
channels. (2) ‘‘Celebrating Healthy Eating,’’ a
and Later consequences’’ (Danone Institute China, nutritional education program developed by
2005); (2) at the international level: ‘‘Nutritional
Danone Institute US, specifically designed for
Solutions to Major Public Health Problems of
preschool children. The curriculum is distributed
Preschool Children’’ (Danone Institute Inter-
nationally to early child educators. Families can
national 2005 at the 18th International Congress
read about nutrition news, create recipes for
of Nutrition), ‘‘Novel Concepts in the Develop-
children, and learn about children’s books about
mental Origins of Adult Health and Disease’’
nutrition. Teachers have access to educational
(Danone Institute International 2006 at Experimen-
information, lesson plans and activities on different
tal Biology 2006), ‘‘Risks and Benefits of Rapid
food groups. Tools are now available online at
Early Growth’’ (Danone Institute International
www.celebratehealthyeating.org. (3) Computerised
2006 at Europediatrics 2006) nutrition games for children were recently devel-
Publications: ‘‘Early Nutrition and Later Con-
oped by Danone Institute of Czech Republic and
sequences: New Opportunities,’’ proceedings of a
Danone Institute of Poland for children ages 7 to 10
European Union–supported workshop organized at y and 6 to 9 y, respectively. Both games presenting
the 2nd World Congress of Pediatric Gastroenter-
dietary and nutritional information in a fun and
ology, Hepatology and Nutrition (Danone Institute
interactive way are intended to help children
International 2005)
Educational programs for professionals: (1) ‘‘The develop healthy eating habits and contribute to
preventing childhood obesity.
Course in Pediatric Nutrition,’’ created in 1998 by
Danone Institute of Italy. This annual 2-d course,
given by teachers of the pediatric clinic of the Readers are encouraged to read more information
University of Milan with the support of the Italian about the Danone Institutes and their activities at
Society of Pediatric Nutrition, provide extensive www.danoneinstitute.org.

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V O L U M E 4 3 ♦ S U P P L E M E N T 3 ♦ D E C E M B E R 2 0 0 6

JOURNAL OF PEDIATRIC GASTROENTEROLOGY AND NUTRITION

The Official Journal of

NUTRITIONAL SOLUTIONS TO MAJOR PUBLIC HEALTH

VOL. 43, SUPPL. 3, DECEMBER 2006 PAGES S1–S73

JOURNAL OF PEDIATRIC GASTROENTEROLOGY AND NUTRITION

The Official Journal of

Nutritional Solutions to Major Public Health Problems of

Publication of this supplement was supported by an unrestricted

The Official Journal of

Causes of Nutrition-related Public Health Problems of Preschool Children: Available Diet S8

Nutritional Deficiencies in Learning and Cognition S22

(continued on next page)

Successful Food-Based Programmes, Supplementation and Fortification S47

Priorities in Nutritional Rehabilitation S66

The Danone Institutes S72

Nutritional Solutions to Major Health Problems of Preschool

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

Nutritional Solutions to Major Health Problems of Preschool

INTRODUCTION A major challenge that still is unrecognised is the one

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

Causes of Nutrition-related Public Health Problems of Preschool

INTRODUCTION IMPORTANCE OF NUTRITIONAL DEPLETION

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

Effect of Infections and Environmental Factors on Growth and

INTRODUCTION global burden of malnutrition because a large pro-

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

Leucine 91y 62 101 124 82 29 80 89 1090 72 8

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

loss (220 mg/kg/d) (45,46) exceeds even that which is

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

Nutritional Deficiencies in Learning and Cognition

INTRODUCTION For example, depletion of the bioavailability of tyrosine

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

Prevention and Control of Obesity in Preschool Children:

INTRODUCTION NORMATIVE GROWTH STANDARDS FOR

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

2 10.5 85.5 14.4 5.7 1.6 N 1.8 2.1 U 2.0 2.1 U —

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J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

challenge of defining the optimal energy intakes and A Weight/age

NUTRITION PROGRAMS FOR YOUNG

To address food insecurity and protect vulnerable

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

Chile is often presented as a paradigm of the success of 0

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

AGE years AGE years

J Pediatr Gastroenterol Nutr, Vol. 43, Suppl. 3, December 2006

loss (220 mg/kg/d) (45,46) exceeds even that which is

2 10.5 85.5 14.4 5.7 1.6 N 1.8 2.1 U 2.0 2.1 U —