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Women are doubly vulnerable to malnutrition, because of their high nutritional requirements for
pregnancy and lactation and also because of gender inequalities in poverty. Undernutrition and
overnutrition coexist in developing countries undergoing rapid nutrition transition, and women
are susceptible to this double burden of “dysnutrition,” often cumulating stunting or micronu-
trient malnutrition with obesity or other nutrition-related chronic diseases. The purpose of the
present paper is to describe the adverse impact of income and gender inequities on women’s
nutritional health, and the dramatic consequences, not only for women themselves, but for chil-
dren, families, and societies. Improving women’s resources, including health, nutrition, education,
and decisional power, is critical for equity and for the health of children and adults of future
generations, since poor fetal and infancy nutrition is another risk factor for chronic diseases,
in particular abdominal obesity, type 2 diabetes, hypertension, and cardiovascular disease. Ad-
dressing malnutrition and nutrition-related chronic diseases simultaneously is a challenge facing
developing countries, and examples of promising initiatives are provided. Focusing on women
along the lifecycle, according to the continuum of care approach, is essential to achieving the
Millennium Development Goals and to breaking the intergenerational cycle of poverty, malnutri-
tion, and ill-health.
Key words: maternal nutrition; poverty; double burden of malnutrition; gender inequalities
services, and it is often characterized by lack of free- then particularly in cities), and they can no longer be
dom, education, and opportunities, in addition to lack considered diseases of affluence.7 Additionally, there is
of income and inequalities.2 Maternal health dispari- mounting evidence that the two forms of malnutrition
ties are primarily evidenced in wide differences in ma- are synergistic. According to the theory of the early ori-
ternal and neonatal death rates. Nearly all maternal gins of chronic diseases,8 nutritional insults in utero or
and newborn deaths occur in DCs where women have during infancy permanently change the body’s struc-
inadequate access to health care.3 “Time poverty” has ture, function, and metabolism in such a way that the
been used to describe the situation of African women risk of chronic diseases, including diabetes and CVD
whose production and domestic (unpaid) work leaves is increased in later life. Therefore, early malnutrition
little time for leisure or even for child care or for partic- exacerbates the health risks associated with the nutri-
ipating in development activities.4 Time poverty rep- tion transition. Prevention of NRCDs is now a public
resents a critical dimension of women’s poverty. Work health priority worldwide, and the World Health As-
burdens are gender-differentiated, and this may even sembly adopted in 2004 the WHO Global Strategy on
be exacerbated in contexts of HIV/AIDS.4 In Benin, Diet, Physical Activity, and Health.9
we found, in rural as well as urban households, that
women engaged in less demanding physical activities,
but worked much longer hours than men, to such an The Vulnerability of Women
extent that no leisure time was left.5 to Both Forms of Dysnutrition
Hunger and overall undernutrition are usually con-
sidered synonymous. However, a more insidious form Preschool children are one of the two groups
of malnutrition, that of “hidden hunger,” consists most vulnerable to malnutrition. The second group
of specific micronutrient deficiencies, such as iron, is women and girls, who are also disproportionately af-
iodine, and vitamin A deficiency disorders, to mention fected by nutritional disorders associated with hunger
only the most prevalent. Micronutrient malnutrition is or undernutrition and micronutrient deficiencies, but
widespread and the consequences are life threatening also affected by nutrition-related chronic conditions,
for women and children. such as obesity and diabetes. Yet women are more
Another form of malnutrition that is now spreading resilient physiologically than men. Given similar eco-
in DCs is related to obesity and other chronic diseases. nomic and health resources, they tend to live longer
It is often regarded as the opposite of undernutrition than men, although inequalities and discrimination
and is sometimes referred to as “overnutrition.” How- may blunt this advantage. The most striking excep-
ever, “overnutrition” is somewhat a misnomer because tions are in Qatar, Pakistan, Maldives, and Bangladesh,
while obesity, for instance, is the result of energy in- where average healthy life expectancy is at least
take in excess of requirements, it may also overlap with 2.5 years higher in men than women.10
dietary inadequacies in micronutrients and fiber. We Women are doubly vulnerable to undernutrition or
therefore suggest the term “dysnutrition” to encom- micronutrient deficiencies, owing to their high nutri-
pass the whole range of nutritional problems: mal- tional requirements for pregnancy and lactation, and
nutrition, which comprises undernutrition and spe- also because of gender inequalities in poverty. In some
cific micronutrient deficiencies, and nutrition-related but not all poor regions, gender discrimination in food
chronic diseases (NRCDs) including disorders of over- allocation may also contribute to women’s nutritional
nutrition and dietary imbalances.6 While malnutrition vulnerability. In Vietnam, for example, based on two
(undernutrition and micronutrient deficiencies) is tra- sets of household surveys 5 years apart, men reaped
ditionally considered a problem of the poor, NRCDs proportionally more nutritional benefit from economic
are seen as problems of the affluent, and this is one of development than women, as reflected in food access
the reasons NRCDs have been neglected in DCs up and body weight data.11 This sort of discrimination was
to recently. While hunger (or food insecurity) typifies also observed in Guatemala when comparing dietary
poverty, obesity may also be associated with poverty. intake of boys and girls.12 Malnutrition usually evokes
Indeed, except in extreme poverty, food insecurity of- the specter of severely wasted children and adults,
ten translates into energy-sufficient and even excessive, but it is not necessarily visible. Moderate malnutri-
but poor quality, diets. Obesity of poverty is observed in tion, with stunted growth, is also responsible for excess
industrialized countries, as well as in DCs undergoing mortality in children,13 not only the clinical and severe
the nutrition transition. Obesity and other NRCDs, forms of kwashiorkor and marasmus. It is estimated
such as diabetes and cardiovascular disease (CVD) are that malnutrition is involved in 50% of child deaths in
on the rise in DCs, even in low-income countries (but DCs, according to WHO. In women of reproductive
174 Annals of the New York Academy of Sciences
age, malnutrition is a major contributor to maternal risk factors (obesity, insulin resistance, high blood pres-
mortality, and it is evidenced by stunting, chronic en- sure, dyslipidemia) in DCs, including sub-Saharan
ergy deficiency (CED), and micronutrient malnutri- Africa.21,22 Urbanization is one determinant of the nu-
tion. Maternal malnutrition is a major determinant of trition transition and the resulting upsurge of chronic
low birth weight in DCs. According to Harvey, iron diseases, such as abdominal obesity, type 2 diabetes,
deficiency anemia is responsible for 22% of maternal hypertension, dyslipidemia, and CVD. The interac-
deaths and 24% of neonatal deaths.14 tion of adaptation, modernization, and stress is at play
Women are also more vulnerable than men to in the disease changes that accompany urbanization.23
obesity and other NRCDs, which have not replaced DCs may be particularly vulnerable to nutrition tran-
malnutrition-related diseases in DCs, resulting in the sition because of recent or concurrent undernutrition,
double burden of dysnutrition, primarily in southern as it may compound the chronic disease risk associ-
Asia and sub-Saharan Africa. This double burden is ated with higher-fat diets, lack of physical activity, and
now observed in low- and middle-income DCs. It is other lifestyle patterns, such as tobacco smoking. In
partly the result of the rapid nutrition transition char- other words, as is so well put by Adair and Prentice,
acterized by major shifts of populations’ eating patterns prenatal factors contribute to a phenotype that may
and lifestyles.15 Fueled by globalization, urbanization, be more sensitive to lifestyle factors associated with the
technological evolution, and income changes, the nu- development of obesity and the chronic diseases.24
trition transition involves progressive westernization Vorster and Kruger explored possible mechanisms
of diets, with increased consumption of energy-dense, to explain the known relationships among poverty, un-
highly processed foods and drinks,16,17 and a more dernutrition, and CVD in DCs.2 They postulated that
sedentary lifestyle owing to motorized transportation the link between poverty and CVD in South Africa
and mechanized work. could be explained by the high prevalence of un-
In a recent general press paper on world hunger, dernutrition in children aged 1–9 years (9% under-
Pinstrup-Anderson and Cheng describe the dual nu- weight, 23% stunting, 3% wasting), the high preva-
tritional problem of deficiencies and hunger in some lence of overweight in adults (54.5% in men and
households and obesity and related diseases in oth- 58.5% in women), and the negative changes in di-
ers.18 They remind that poverty is the main rea- ets (and lifestyles) when Africans urbanize, acculturate,
son that hunger and nutritional deficiencies persist. and adopt western patterns.
However, they do not refer to obesity associated with Among resource-poor populations, women may be
poverty. at greater risk of CVD, which is the single largest cause
of women’s deaths, accounting for one-third of the to-
tal worldwide.25 CVD risk factors are also increasing
Nutrition-related Chronic Disease in women of DCs and will contribute to more women’s
Risk Factors in Women than men’s deaths by 2040.25 Some risk factors play
of Developing Countries a greater role in women than men: high triglyceride
concentrations, low HDL-cholesterol, and diabetes. In
The burden of chronic diseases in DCs is much the THUSA (Transition and Health during Urban-
higher than usually perceived. In 2005, chronic ization in South Africa) study on CVD risk factors in
diseases—mainly CVDs, cancer, chronic respiratory South Africa, there were indications that while in men
diseases, and diabetes—were responsible for 50% of the CVD burden was heavier among the better-off, in
total disease burden in 23 countries which account women overweight/obesity (prevalence of 58.5%) and
for 80% of chronic disease mortality in DCs.19 WHO some other risk factors affected the rich and the poor.26
insisted on the need to address noncommunicable dis- Although there are more similarities than differ-
eases, a neglected problem in DCs.20 Women are at ences in CVD risk factor trends in developed and
a disadvantage: their age-standardized death rate for DCs according to a recent review,27 one risk factor
chronic diseases is 86% higher in DCs than in de- is particularly critical in DCs, and it is the risk as-
veloped countries, whereas in men, it is 54% higher sociated with poor early growth and nutrition.28 In-
in DCs compared to developed countries.19 Further- adequate growth and nutrition in utero is associated
more, these deaths occur at an earlier age in DCs com- with increased chronic disease risk, according to the
pared to high-income countries, depriving families and theory of the early origins of chronic diseases.8 Poor
societies of adults in their productive years. nutrition in infancy, which is still highly prevalent in
The nutrition transition fuels the increase of the DCs, also appears associated with later chronic dis-
metabolic syndrome, which is a clustering of CVD ease, although the evidence is less documented than in
Delisle: Poverty and Intergenerational Malnutrition 175
the case of intrauterine malnutrition. Several mecha- including in South Africa41 and Benin5 confirm that
nisms may explain the link between early life under- inactivity is related to women’s overweight/obesity.
nutrition and chronic diseases, including programmed
metabolic adaptation to an environment of scarcity
The Double Nutritional
in utero, by virtue of developmental plasticity.29 High
blood pressure is the chronic disease risk factor which
Burden in Women
has been the most consistently associated with poor
The shift toward obesity and related chronic dis-
early growth in several population and age groups.30
eases in DCs does not mean that malnutrition (under-
Insulin resistance, abdominal obesity, and CVD have
nutrition and micronutrient deficiencies) is no longer
also shown links with fetal malnutrition reflected in low
a problem. In actuality, both forms often coexist and
birth weight.31
characterize the double burden of dysnutrition. The
Hypertension is widespread in DCs, particularly in
double nutritional burden weighs heavily on already
sub-Saharan Africa.32–34 Its prevalence is not consis-
inadequate and overextended health budgets of DCs.19
tently higher in urban or better-off settings, which
The double burden is also deleterious for societies and
our studies in Benin confirmed (unpublished data). In
families. It may be observed at the individual level, and
poor Nordeste, Brazil, hypertension was more preva-
especially among women. The double burden is also
lent among women than men (38.5% versus 18.4%,
observed within households, and it is usually reflected
respectively).35 Some studies suggest that illiterate and
in the coexistence of maternal overweight/obesity and
underweight women are at greater risk of being hy-
child chronic or acute malnutrition. Its increasing
pertensive than educated or normal weight women,
prevalence at the household, community, or country
although overweight/obese women are also at higher
level is typical of rapidly transitioning countries, and
risk compared with normal weight women.36 Low
is becoming a major public health concern. It may
socio-economic status (SES) was a significant risk fac-
take the form of overlapping stunting or micronutrient
tor for high blood pressure in both adolescent males
malnutrition and obesity, as well as underweight in part
and females in Congo.37 A U-curve may be postulated
of the population and overweight and obesity-related
for the association of nutritional or economic status
comorbidities in the other.
with the risk of hypertension.
The prevalence of overweight and obesity is much Double Burden of Malnutrition
higher among women than men in most DCs. In low- at the Country Level
income countries, the risk of obesity (and comorbidi- Women are more exposed than men to the double
ties) is higher in more affluent groups, but the burden burden. In Brazil, for instance, there were roughly two
shifts to poorer groups as GNP rises; the shifting point cases of underweight for one case of obesity in 1975; the
is the middle national income, according to the World ratio was reversed in 1997.38 Low-income women were
Bank grouping of countries based on per capita in- more susceptible to both underweight and obesity. The
come.38 Obesity is increasing rapidly under the in- combined prevalence, considered by the authors as a
fluence of urbanization and westernization of diets, proxy for the total burden of nutritional diseases, was
lifestyles, and culture. Cultural factors may also con- significantly higher in low-income than high-income
tribute to the higher prevalence of overweight or obe- women in both surveys: 22% versus 17% in 1975, and
sity in women compared to men. In several African 22% versus 15% in 1997, respectively.
countries, the ideal of beauty is not leanness, in contrast The double burden of dysnutrition is currently most
with western countries, but rather overweight, which is problematic in middle-income DCs of Latin Amer-
also a social status symbol.39,40 The gender difference ica and North and South Africa. While CED or
occurs already at adolescence. In semi-urban areas of underweight (BMI < 18.5 kg/m2 ) remains the major
Congo (Kinshasa), the prevalence of overweight and nutritional problem among women of low-income
obesity was 68.5% in female school adolescents, versus countries, the double burden of underweight and
24% in male adolescents.37 overweight/obesity (BMI ≥ 25 kg/m2 ) is emerging in
Physical inactivity as a CVD risk factor in DCs is South Asia and sub-Saharan Africa. In Bangladesh,
of concern: 60–85% of the population of developed for instance, in nationally representative samples of
countries or DCs do not undertake sufficient physi- women of reproductive age, the prevalence of CED
cal activity to gain health benefits.25 Lack of physical between 2000 and 2004 was 38.8% among rural and
activity is more of a problem in women in several set- 29.7% among urban poor women, while 4.1% and
tings, and particularly so among adolescent girls and 9.1%, respectively, were overweight or obese. It has
low SES women. Studies in sub-Saharan countries, been suggested to lower the BMI cutoffs of overweight
176 Annals of the New York Academy of Sciences
TABLE 1. Nutritional status of women aged 25–60 years in three sites in Benin (West Africa)
Large city Medium-size city Semi-rural outskirts
(Cotonou) N = 100 (Ouidah) N = 85 (Ouidah) N = 85
and obesity in Asian populations because of evidence Egypt, Mexico), is characterized by a low prevalence of
of emerging CVD factors and diabetes below the stan- undernutrition, but the overlap of stunting and over-
dard overweight cut-point of 25 kg/m2 , possibly be- weight/obesity in children, while in adults obesity is
cause of a proportionally higher percentage of body high or rapidly increasing, with increasing diabetes
fat for any BMI in Asians compared to Caucasians.42 and coronary heart disease rates as correlates.
In Bangladeshi women, an additional 9.6% of ru- In Benin (West Africa), our on-going studies on the
ral and 18.9% of urban poor women were consid- nutrition transition and cardiometabolic risk factors in
ered at risk of overweight, with a BMI at or above adults of urban and semi-rural areas show that un-
23 kg/m2 .43 Although in urban poor areas, the com- derweight is as prevalent in semirural women as over-
paratively wealthier group had a higher prevalence of weight/obesity is among city women (see TABLE 1).
overweight/obesity (12.2%), the rate was 8.4% among Income and gender inequalities appear to have ad-
the poorest women. Over the 5-year period, CED de- ditive or compound effects. In India, for instance, it was
clined and overweight/obesity increased in both set- found that state income inequality increased the like-
tings, but the increasing trend of high BMI was more lihood of both undernutrition and overweight among
marked in rural than urban women. In The Gambia, women, that is, of the double nutritional burden, even
data collected a decade ago showed that the preva- after adjusting for several individual and state-level co-
lence of CED was 18% and affected all social strata, variates.46 For one standard deviation increment in
whereas obesity was primarily a problem of urban income inequality measured by the Gini coefficient,
women, with one-third affected beyond the age of 35 the odds ratio of being underweight increased by 19%
years.44 (P = 0.02) while the odds ratio of being obese increased
In resource-poor countries, a still-predominant fea- by 21% (P < 0.001). The adverse effect of state income
ture of the double burden is that undernutrition inequality is also observed for overweight. The contex-
tends to cluster among the impoverished and over- tual inequality appears to exacerbate the known im-
weight/obesity among the more affluent. This is typi- pact of individual SES as low SES women experience
cal of the early stages of the nutrition transition. How- the greatest risk of underweight whereas the high SES
ever, the situation is rapidly evolving, and overnutrition ones are exposed to higher obesity risk. The authors
coexists increasingly with undernutrition even among suggested that, in regions in economic transition and
the poor. growth, focusing on reducing economic inequalities is
The Food and Agriculture Organization of the likely to address the dual burden.
United Nations, on the basis of case studies in six DCs,
proposed a typology of countries with respect to the Double Nutritional Burden Households
double burden of malnutrition.45 Three country types The phenomenon of coexistence of child undernu-
are delineated, corresponding to advancing stages of trition and maternal overweight/obesity in the same
the nutrition transition. The first group includes India households has been described in several DC set-
and the Philippines. These countries are still in the tings, including South Africa, China, Brazil, Haiti, and
early transition stages, with persistent undernutrition Benin.47,48 Comparing Russia, China, and Brazil, the
and micronutrient deficiencies in children and adults, prevalence of the double burden among households
and only emerging problems of obesity, diabetes, and was very similar: 8% in Russia and China, and 11%
high blood pressure in urban areas. The second type in Brazil, based on national surveys.48 In a poor rural
is illustrated by South Africa, where child stunting and community of Malaysia, 15.7% of mother/child pairs
micronutrient malnutrition are still widespread, but showed the double burden,49 which is quite similar to
overweight/obesity is more a problem than undernu- what we observed in a shanty town of Port-au-Prince,
trition in adults. The third type, corresponding to a still Haiti (14%) and in poor neighborhoods of Cotonou,
more advanced stage of the nutrition transition (China, Benin (16%).50,51
Delisle: Poverty and Intergenerational Malnutrition 177
OR (95% CI)
Double burden households (n = 24)
nutrition transition.52 It suggests that similar circum-
(n = 29)
trate the differential rate of change of the prenatal and
postnatal environment.29 The prenatal environment is
0.009
0.049
0.009
0.10
0.92
0.06
determined by maternal size, body composition, and
P
metabolism, which is partly determined in turn by the
mother’s own growth in utero and during infancy and
1.38
0.62
1.67
−2.87
−1.77
−1.98
childhood. In the nutrition transition context, small
β
mothers have small babies because of maternal size
TABLE 2. Predictors of the concurrent presence of malnutrition in at least one child and maternal overweight51
constraints, and then the children grow rapidly owing
to more favorable factors in the postnatal environment.
a
4.45 (0.81; 24.54)
(n = 30)
obesity and child stunting were present in 6% of pairs.
The odds of having a stunted child were twice as great
0.087
0.046
0.050
0.68
0.21
0.32
P
in mothers with a waist-hip ratio (WHR) around 1,
compared with those with a WHR of 0.65.54
In Benin, we found that “double burden” house-
0.32
0.77
1.49
−2.05
−1.58
−0.72
holds had a higher SES than households with a mal-
β
0.003
0.37
0.11
0.60
0.38
P
The association between stunting in infancy and evidence is still limited and research in this area is
obesity later on in life has been reported in several stud- direly needed, but micronutrients in short supply in
ies conducted in nutrition-transitioning countries.56 several DCs, including folate and antioxidants, such as
And stunting in infancy is already present at birth in iron, zinc, vitamin C, and carotenoids, may contribute
many cases, as a result of maternal constraint or poor to CVD (and certain types of cancer). Zinc deficiency
nutrition. The mechanism is not yet elucidated, but it is widespread in DCs. It could contribute to oxida-
has been proposed that defective fat oxidation, as ob- tive stress and to the development and progression of
served in stunted children in Brazil, may be a culprit.57 diabetes as well, by virtue of its antioxidant proper-
In Egypt, the odds of being overweight/obese were ties and also because of the metabolic links between
80.8% higher in women of reproductive age who were zinc and insulin in the pancreas.61 Analysis of cross-
possibly deficient in micronutrients based on per capita sectional data from Egypt, Mexico, and Peru revealed
supply of vitamin A, iron, and zinc in the house- that overweight women did not necessarily meet their
hold.58 This study concludes that the overlap between iron requirements. The prevalence of overweight was
micronutrient inadequacies and obesity is not given above 50% in all three countries, reaching 77% in
enough attention by policy makers and researchers as Egypt. While the odds of anemia were lower in over-
well, and one of the implications is that food subsidies weight/obese women in Egypt and Peru, there was no
aggravate the obesity problem as these target energy- difference among BMI groups in Mexican women.
dense foods, which become important for the poor.
In a study of 315 families of an urban slum area
in Nordeste, Brazil, it was found that high blood pres- The Insidious Impact
sure was significantly more prevalent among stunted of Maternal Dysnutrition on the Health
adults compared to normal-height adults, particularly of Whole Societies
in women.35 Short stature, an epidemiological indi-
cator of chronic malnutrition in early life, was more Gill et al. reviewed the evidence linking maternal
strongly associated with high blood pressure in women health with development and proposed an interesting
than men. The odds ratio for hypertension in stunted framework on the key links at the individual, fam-
women compared to nonstunted ones was 1.98 (95% ily, and society level.63 Women are mothers and in-
CI [Confidence Interval] 1.22–2.96). The negative as- dividuals; they are also family members and citizens.
sociation of stature with hypertension, as well as with This framework is useful to better comprehend how
obesity, was observed in women, but not in men. In- women’s health, and notably their nutritional status,
deed short stature was the single most important risk impacts all those levels, and in the present and future
factor for hypertension in women. In the Congo, it generations. Women’s health is connected with their
was observed that in male adolescents but not in female own status, their education, employment, and deci-
adolescents, chronic malnutrition as well as obesity was sional power. Their status is conducive to better health,
a risk factor for high blood pressure.37 and conversely, their health contributes to their status
A small case–control study conducted in Mexico and condition. It is primarily as mothers that women
showed that men who had suffered malnutrition in have been the focus of health efforts. Maternal health
their early years were more prone to insulin resistance affects women’s survival and the health and survival of
when they developed abdominal obesity, suggesting their children. Nutrition is critical for maternal health
that obesity may have more adverse effects in individ- and for reducing maternal mortality in DCs. For in-
uals who were exposed to early malnutrition.59 This stance, as already mentioned, iron deficiency anemia
study was only conducted in men, but several other reportedly accounts for 22% of maternal deaths and
reports linked low birth weight with increased insulin for 24% of neonatal deaths.14 Indeed, interventions to
resistance in men and women, including a study on improve maternal diets and to promote breastfeeding
600 men and women aged 45 years in China.60 are relevant everywhere.
Probably the most prevalent phenotype of double Women’s status, health, and nutrition also impact
dysnutrition is the simultaneous presence of micronu- families’ income, welfare, and well-being, and it has
trient malnutrition and overweight/obesity, as “transi- been shown in several settings that maternal income,
tional” diets are typically energy dense but micronutri- more than that men’s income, is directly reflected in
ent poor. This situation is of concern not only because better nutrition and health of children.64 That poor
of the adverse health outcomes of both forms of dys- maternal health and nutrition perpetuates the cycle of
nutrition, but also because micronutrient deficiencies ill-health and malnutrition across generations is further
may actually contribute to chronic diseases.61,62 The described below. Although more research is required
Delisle: Poverty and Intergenerational Malnutrition 179
ignored or seriously neglected in policies for health, ity and empowerment of women; reduction of child
education, gender equality, or poverty reduction, par- mortality; and improvement of maternal and repro-
ticularly in sub-Saharan Africa, considering that it is ductive health. The project views nutrition as a cross-
the worst region in the world as regards child and ma- cutting issue, interconnected with gender, and involv-
ternal malnutrition and mortality rates. In the Com- ing several development sectors and players. The NGI
mission for Africa report, for instance, Chopra and strives to find suitable approaches to addressing malnu-
Darnton-Hill criticize the fact that the chapter on ed- trition throughout the lifecycle as a means of improving
ucation and health devotes less than half a page to gender equality, along with enhancing institutional ca-
nutrition, and only to address parasite control and mi- pacity for gender analysis, nutrition programming, and
cronutrient support.71 Similarly, it was a surprise to us advocacy.
not to see a single mention of nutrition, diet, dietary Several risk factors and opportunities for preven-
education, or even food (except for food availability) tion are similar for chronic diseases, such as cancer,
in a whole paper on the management of diabetes in CVD, and diabetes. Additionally, the same behavioral
sub-Saharan Africa,72 given that healthy eating is the risk factors are observed in developed countries and
cornerstone of treatment as well as prevention of type 2 DCs.33,34 However, programs to prevent obesity and
diabetes. Much advocacy effort is needed for nutrition related chronic diseases are rather new in several DCs.
to be mainstreamed, and particularly so for addressing A wide range of such programs was described in a sum-
chronic diseases connected with the nutrition transi- mary paper77 and encompassed worksite, community-
tion in resource-poor DCs. based school, and national programs to improve diet
Nonetheless, there are encouraging policies and and increase physical activity in 14 DCs. The tem-
strategies as regards gender equality, women’s health plate presented by van der Sande and colleagues for
and nutrition, and empowerment. Women’s educa- the prevention and control of CVD in sub-Saharan
tion is empowering,73 and it may bring about major Africa is still highly relevant.78 As suggested in this pa-
improvements in maternal and child nutrition.74 Ad- per, a comprehensive program will be more acceptable
ditionally, women’s empowerment is one of the most and effective if it combines prevention and treatment.
effective ways of cutting down birth rates.65 Mater- As noted for South Africa, the poor, however, may
nal malnutrition is responsible for excess maternal and have limited knowledge on, or interest in, primary
neonatal mortality; improvements in women’s nutri- prevention of CVD behavioral risk factors, as meet-
tion will decrease mortality, while increasing the nu- ing their basic needs takes up all their attention and
tritional status of surviving children. Additionally, im- energy.2 Furthermore, the poor have limited access
proved maternal nutrition will contribute to enhancing to secondary prevention. They are therefore at high
the economic productivity of women and decreasing in risk and should be targeted, but promoting healthy
their progeny the chronic disease risk associated with lifestyles, including an adequate but prudent diet, may
poor nutrition in early life. As stated in a UNICEF re- not be enough inasmuch as limited access to resources
port on the state of children, gender equality is central is a major constraint to healthful behaviors. Means of
to realizing the MDGs.75 More gender equality will increasing access to resources are therefore needed,
empower women to overcome poverty and will assist and particularly so among women, who are dispropor-
their children, families, communities, and countries as tionately poor and disproportionately affected in their
well. Improving nutrition, particularly that of women, own health and that of their children by poverty. Means
is also considered key to meeting the MDGs.14 Based of coupling nutritional improvement with women’s in-
on the premise that investing in nutrition and gender come generation should be sought and exploited as
is an investment in MDGs with a high return, the In- much as possible. This was the concept behind the red
ternational Center for Research on Women and its palm oil development project in Burkina Faso, with
partners successfully implemented the Nutrition Gen- the dual objective of improving vitamin A nutrition
der Initiative in Ghana, India, and Bangladesh be- of mothers and children and of generating income for
tween 2002 and 2005.76 The goal of the Nutrition and women extracting and retailing the oil.79
Gender Initiative (NGI) is to add nutrition and gender The overlap of malnutrition and NRCDs in the
objectives and actions into development programs and same population groups is a challenging issue to health
thereby contribute to achieving the following MDGs, bodies. Creative initiatives are direly needed. Govern-
through action research, communication, and advo- ments have to be involved in the prevention and con-
cacy: eradication of poverty and hunger; achievement trol of chronic diseases, were it only to help individu-
of universal primary education; reaching gender equal- als to make informed choices regarding risk behaviors
Delisle: Poverty and Intergenerational Malnutrition 181
through fostering the generation of relevant informa- Preventing all forms of dysnutrition among women
tion, and making this information widely available and is key, and measures should start early. The school
understood.19 Addressing obesity and chronic diseases setting, for instance, is particularly appropriate for pre-
simultaneously is not simple. It even creates a “cul- ventive actions.85,86 A recent WHO initiative intended
tural shock” among decision makers,80 as policies and to fight the double burden of malnutrition in schools,
programs have been focusing on food insecurity, un- the “Nutrition-friendly School Initiative,” is being pro-
dernutrition, and micronutrient deficiencies. Vorster moted and tested. As suggested by some,39 young gen-
and Kruger plead for an integrated, transdisciplinary, erations in emerging countries are likely to be respon-
and multisectoral approach to break the vicious cy- sive to messages for the prevention of obesity, much
cle of poverty and undernutrition for the long-term like in western countries, because of their exposure to
prevention of CVD.2 Governments must feel the pres- global media.
sure. Diabetes may be a key word, as the associated Maternal and child nutrition should not be di-
health costs are enormous, and health ministries are chotomized, however, because they are closely con-
well aware of them, more so than of the health risk nected. This is in line with the approach of the contin-
associated with obesity.81 Linking diabetes with child uum of care for maternal, newborn, and child health.87
obesity and with maternal risk may be a worthy strat- Nutrition ought to be integrated in the continuum of
egy. care, at adolescent, prepregnancy, neonatal, and child
Promoting diets that are adequate, well-balanced, care levels. For instance, adolescent and prepregnancy
and safe yet affordable and in line with cultural prac- nutrition is part of family and community care, and
tices and local food production appears as one of the folate and iron supplementation is integrated into re-
pillars of the prevention of the double burden of malnu- productive health care. It is argued in the same paper
trition,82 along with the promotion of physical activity. that if the eight proposed continuum of care pack-
The 2004 WHO global strategy on diet and physical ages were implemented to reach most families, the
activity focused on food, agriculture, and multisectoral lives of 2/3 of the 10 million babies and children
policies to promote healthy eating and physical activ- dying every year could be saved, and many of the
ity.9 Traditional diets, oftentimes more diversified and half-million maternal deaths could be averted, along
higher in fruits and vegetables, need to be rehabilitated, with many stillbirths. However, the dual burden of
and physical activity has to become socially desirable. malnutrition in women and the dramatic adverse ef-
Brazil offers an interesting example. A national food fects in the progeny is not explicitly considered in this
and nutrition policy was designed early in the new strategy.
century to continue to combat nutritional deficien- Surveillance, which provides appropriate informa-
cies, while also addressing the prevention of NRCDs.83 tion for advocating for policy and action tailored to
The policy is essentially to promote, protect, and address the double burden of dysnutrition, is required,
support healthy eating and lifestyle patterns through as recently emphasized.71 Sawaya and colleagues, in a
legislative measures, communication, and capacity review of the association between chronic undernutri-
building. tion and hypertension, also suggested that healthcare
As stressed by Eckhardt, the most important strat- practitioners working in low-income urban communi-
egy for reducing the double burden of micronutri- ties monitor blood pressure in order to detect and treat
ent malnutrition and overweight/obesity in nutrition- in timely fashion high blood pressure that tends to be
transitioning countries is to enhance diet quality associated with early life malnutrition.88
throughout the life cycle.61 For this purpose, develop- Research needs in the realm of the double bur-
ing dietary guidelines appears important. Food-based den of dysnutrition in DCs are pressing. Research
dietary guidelines should become available at the coun- priorities may include, in addition to epidemiological
try or regional level in order to take account of cultural and surveillance data on chronic disease risk factors
patterns. For those individuals already diagnosed with and the prevalence of the double burden, the links
diabetes, health professionals should devise location- between micronutrient malnutrition and chronic dis-
specific and tailor-made eating plans based on up-to- eases, the contribution of stress of life to chronic dis-
date international recommendations. For all of this to eases particularly in urban settings, changes in food
happen, the current paucity of well-trained nutrition- provisioning of urban and rural communities, and the
ists in several sub-Saharan regions urgently needs to relevance and effectiveness of location-specific dietary
be remedied. Indeed a 2005 report by WHO insisted guidelines for simultaneously tackling undernutrition,
on preparing the workforce for the growing burden of micronutrient malnutrition, overnutrition, and dietary
chronic diseases.84 imbalances.
182 Annals of the New York Academy of Sciences
In summary, improving nutrition, in particular University World Institute for Development Economics
women’s nutrition, is critical for health, poverty reduc- Research. Amsterdam. Research Paper No. 2007/54.
tion, and development, and it has to be mainstreamed. 12. FRONGILLO, E.A. & F. BÉGIN. 1993. Gender bias in food
intake favors male preschool Guatemalan children. J. Nutr.
Healthy diets and lifestyles are obviously key for pre-
123: 189–196.
venting the various forms of under- or overnutrition, 13. PELLETIER, D. L. & E.A. FRONGILLO. 2003. Changes in child
but for the behavioral risk factors to recede, an en- survival are strongly associated with changes in malnutri-
abling political, physical, socioeconomic, and cultural tion in developing countries. J. Nutr. 133: 107–119.
environment is needed so that required changes are 14. HARVEY, P. 2007. Improving women’s nutrition: a require-
feasible. The rising tide of NRCDs is now a compelling ment for achieving the Millennium Development Goals.
reason to tackle the dual burden of malnutrition in http://www.a2zproject.org/docs/HRHS_Harvey.pdfp.
15. POPKIN, B.M. 2006. Global nutrition dynamics: the world is
DCs. Research as well as surveillance should be uti-
shifting rapidly toward a diet linked with noncommunica-
lized to fuel advocacy efforts and to inform policy and ble diseases. Am. J. Clin. Nutr. 84: 289–298.
programming. 16. PRENTICE, A.M. & S.A. JEBB. 2003. Fast foods, energy den-
sity and obesity: a possible mechanistic link. Obesity Rev.
4: 187–194.
Conflicts of Interest 17. DREWNOWSKI, A. & S. SPECTER. 2004. Poverty and obesity:
the role of energy density and energy costs. Am. J. Clin.
The author declares no conflicts of interest. Nutr. 79: 6–16.
18. PINSTRUP-ANDERSON, P. & F. CHENG. 2007. Still hungry.
Sci. Am. 297: 96–103.
19. ABEGUNDE, D.O., C.D. MATHERS, T ADAM, et al. 2007. The
References burden and costs of chronic diseases in low-income and
middle-income countries. Lancet 370: 1929–1938.
1. AHMED, A.U., R.V. HILL, L.C. SMITH, et al. 2007. The 20. WHO. 2006. Preventing chronic disease: a vital investment.
world’s most deprived. Characteristics and causes of ex- WHO. Geneva.
treme poverty and hunger. IFPRI. Washington. 2020 Dis- 21. PRENTICE, A.M. 2006. The emerging epidemic of obesity in
cussion Paper No. 43. developing countries. Int. J. Epidemiol. 35: 93–99.
2. VORSTER, H. H. & A KRUGER. 2007. Poverty, malnutrition, 22. FEZEU, L., B. BALKAU, A.P. KENGNE, et al. 2007. Metabolic
underdevelopment and cardiovascular disease: a South syndrome in a sub-Saharan African setting: central obesity
African perspective. Cardiovasc. J. Africa 18: 321–324. may be the key determinant. Atherosclerosis 193: 70–76.
3. SAVE THE CHILDREN. 2007. State of the World’s Mothers 23. CARLIN, L., T. ASPRAY & R. EDWARDS. 2001. Civilization
2006. Save the Children. Wesport, CT. and its discontents: non-communicable disease, metabolic
4. BLACKDEN, M. & Q. WODON (Eds). 2006. Gender, time use syndrome and rural-urban migration in Tanzania. Urban
and poverty in Sub-Saharan Africa. Washington: World Anthropol. 30: 51–70.
Bank Working Papers No. 73. 24. ADAIR, L.S. & A.M. PRENTICE. 2004. A critical evaluation
5. NTANDOU, G., H. DELISLE, V. AGUEH & B. FAYOMI. 2008. of the fetal origins hypothesis and its implications for de-
Physical activity and socioeconomic status explain rural- veloping countries. J. Nutr. 134: 191–193.
urban differences in obesity: a cross-sectional study in 25. LOCKYER, L. & M. BURY. 2002. The construction of a mod-
Benin (West Africa). Ecol. Food Nutr. (in press). ern epidemic. The implications for women of the gender-
6. DELISLE, H. & O. RECEVEUR. 2007. Les <<dysnutritions>> ing of coronary heart disease. J. Adv. Nurs. 39: 432–440.
dans les pays en développement (lettre). [‘Dysnutrition’ in 26. VORSTER, H.H., A. KRUGER, C.S. VENTER, et al. 2007. Car-
developing countries (Letter)]. CMAJ 176: 65. diovascular disease risk factors and socio-economic posi-
7. EZZATI, M., V.S. HOORN, C.M.M. LAWES, et al. 2005. Re- tion of Africans in transition: the THUSA study. Cardio-
thinking the “diseases of affluence” paradigm: global pat- vasc. J. Africa 18: 315–322.
terns of nutritional risks in relation to economic develop- 27. GHOLIZADEH, L. & P. DAVIDSON. 2008. More similarities
ment. PLoS Med. DOI: 10.1371/journal.pmed.0020133. than differences: an international comparison of CVD
8. BARKER, D.J.P. (Ed). 1992. Fetal and Infant Origins of Adult mortality and risk factors in women. Health Care Women
Disease. BMJ Publ Group. London. Int. 29: 3–22.
9. WHO. 2004. Global strategy on diet, physical activ- 28. DELISLE, H. 2002. Programming of chronic disease by
ity and health. Fifty-seventh World Health Assembly. impaired foetal nutrition: evidence and implications
WHO. Geneva. Available at: http://who.int/gb/ebwha/ for policy and intervention strategies. WHO, Dept
pdf_files/WHA57/A57_R17-en.pdf. Nutrition for Health and Development. Geneva.
10. WHO. 2007. World Health Statistics. WHO. Geneva. Avail- WHO/NHD/02.3.
able at: www.who.int/whosis/whostat2007/en/index. 29. GLUCKMAN, P.D., M.A. HANSON & C. PINAL. 2005. The de-
html. (Accessed 2008 January 10). velopmental origins of adult disease. Matern. Child Nutr.
11. MOLINI, V. & M. NUBÉ. 2007. Is the nutritional status of 1: 130–141.
males and females equally affected by economic growth? 30. LAW, C. 2005. Early growth and chronic disease: a public
Evidence from Vietnam in the 1990s. United Nations health overview. Matern. Child Nutr. 1:169–176.
Delisle: Poverty and Intergenerational Malnutrition 183
31. BARKER, D.J. 2006. Adult consequences of fetal growth re- overnutrition in India. J. Epidemiol. Community Health
striction. Clin. Obstet. Gynecol. 49: 270–283. 61: 802–809. doi:10.1136/jech.2006.053801.
32. DENNISON, C.R., N. PEER, K. STEYN, et al. 2007. Determi- 47. GARRETT, J.L. & M.T. RUEL. 2005. Stunted child-overweight
nants of hypertension care and control among peri-urban mother pairs: prevalence and association with economic
Black South Africans: the HiHi study. Ethn. Dis. 17: 484– development and urbanization. Food Nutr. Bull. 26: 209–
491. 221.
33. YUSUF, S., S. HAWKEN, S. OUNPUU, et al. 2004. Effect of 48. DOAK, C., L.S. ADAIR, C. MONTEIRO & B.M. POPKIN.
potentially modifiable risk factors associated with myocar- 2000. Overweight and underweight coexist within house-
dial infarction in 52 countries (the INTERHEART study): holds in Brazil, China and Russia. J. Nutr. 130: 2965–
case-control study. Lancet 364:937–952. 2971.
34. STEYN, K., K. SLIWA, S. HAWKEN, et al. (INTERHEART 49. KHOR, G.L. & Z.M. SHARIF. 2003. Dual forms of malnu-
INVESTIGATORS IN AFRICA). 2005. Risk factors associated trition in the same households in Malaysia—a case study
with myocardial infarction in Africa. The INTERHEART among Malay rural households. Asia Pacific J. Clin. Nutr.
Africa Study. Circulation 112: 3554–3561. 12: 427–438.
35. FLORÊNCIO, T.T., H.S. FERREIRA, J.C. CAVALCANTE & A.L. 50. RAPHAEL, D., H. DELISLE & C. VILGRAIN. 2005. Households
SAWAYA. 2004. Short stature, obesity and arterial hyper- with undernourished children and overweight mothers:
tension in a very low income population in North-eastern is this a concern for Haiti? Ecol. Food Nutr. 44: 147–
Brazil. Nutr. Metab. Cardiovasc. Dis. 14: 26–33. 165.
36. SHAKHATREH, F.M.N., A.A. SULEIMAN, F.I. MOHAMMED & 51. BOUZITOU NTANDOU, G.D., B. FAYOMI & H. DELISLE.
A.A. ALWAN. 2008. Hypertension among females in a 2005. Malnutrition infantile et surpoids maternel dans
highly disadvantaged community in Jordan. Health Care des ménages urbains pauvres du Bénin. Cahiers Santé
Women Int. 29: 39–53. 15: 263–270.
37. LONGO-MBENZA, B., E. LUKOKI LUILA & J.R. M’BUYAMBA- 52. DOAK, C.M., L.S. ADAIR, M. BENTLWEY, et al. 2005. The
KABANGU. 2007. Nutritional status, socio-economic status, dual burden household and the nutrition transition para-
heart rate, and blood pressure in African school children dox. Int. J. Obesity 29: 129–136.
and adolescents. Int. J. Cardiol. 121: 171–177. 53. STEYN, N.P., D. LABADARIOS, E. MAUNDER, et al. 2005. Sec-
38. MONTEIRO, C.A., W.L. CONDE & B.M. POPKIN. 2004. The ondary anthropometric data analysis of the national food
burden of disease from undernutrition and overnutrition consumption survey in South Africa: the double burden.
in countries undergoing rapid nutrition transition: a view Nutrition 21: 4–13.
from Brazil. Am. J. Pub. Health 94: 433–434. 54. BARQUERA, S., K.E. PETERSON, A. MUST, et al. 2007. Coex-
39. SIERVO, M., P. GREY, O.A. NYAN & A.M. PRENTICE. 2006. istence of maternal central adiposity and child stunting in
Urbanization and obesity in The Gambia: a country in Mexico. Int. J. Obes. 31: 601–607.
early stages of the demographic transition. Eur. J. Clin. 55. TLADINYANE, P. 2003. The difference in factors influencing
Nutr. 60: 455–463. childcare between others/caregivers of undernourished
40. HOLDSWORTH, M., A. GARTNER, E. LANDAIS, et al. 2004. and well nourished children aged 1–4 years in Oukasie
Knowledge of dietary and behaviour-related determi- (Brits), North West Provence (masters thesis). Pretoria:
nants of non-communicable disease in urban Senegalese MEDUNSA.
women. Int. J. Obesity Related Metab. Disord. 28: 1561– 56. SAWAYA, A.L., P. MARTINS, D. HOFFMAN & S.B. ROBERTS.
1568. 2003. The link between childhood undernutrition and risk
41. KRUGER, H.S., C.S. VENTER, H.H. VORSTER, et al. 2002. of chronic diseases in adulthood: a case study of Brazil.
Physical inactivity is the major determinant of obesity in Nutr. Rev. 61:168–175.
black women in the North-West Province, South Africa: 57. HOFFMAN, D.J., A.L. SAWAYA, I. VERRESCHI, et al. 2000.
the THUSA study. Nutrition: Int. J. Appl. Basic Nutr. Sci. Why are nutritionally stunted children at increased risks
18: 422–427. of obesity? Studies of metabolic rate and fat oxidation in
42. WHO EXPERT CONSULTATION. 2004. Appropriate body- shantytown children from Sao Paolo, Brazil. Am. J. Clin.
mass index for Asian populations and its implications for Nutr. 72: 702–707.
policy and intervention strategies. Lancet 363: 157–163. 58. ASFAW, A. 2007. Micronutrient deficiency and the preva-
43. SHAFIQUE, S., N. AKHTER, G. STALLKAMP, et al. 2007. Trends lence of mothers’ overweight/obesity in Egypt. Econ.
of under- and overweight among rural and urban poor Hum. Biol. 5: 471–483.
women indicate the double burden of malnutrition in 59. BOULÉ, N.G., A. TREMBLAY, J. GONZALEZ-BARRANCO, et al.
Bangladesh. Int. J. Epidemiol. 36: 449–457. 2003. Insulin resistance and abdominal adiposity in young
44. VAN DER SANDE, M.A.B., S.M. CEESAY, P.J.M. MILLIGAN, men with documented malnutrition during the first year
et al. 2001. Obesity and undernutrition and cardiovascular of life. Int. J. Obesity 27: 598–604.
risk factors in rural and urban Gambian communities. Am. 60. MI, J., C. LAW, K. L. ZHANG, et al. 2000. Effects of infant
J. Pub. Health 91: 1641–1644. birthweight and maternal body mass index in pregnancy
45. FAO. 2006. The double burden of malnutrition. Case stud- on components of the insulin resistance syndrome. Ann.
ies from six developing regions. FAO. Rome. Food and Int. Med. 132:253–260.
Nutrition Paper No 84. 61. ECKHARDT, C.L. 2006. Micronutrient malnutrition, obe-
46. SUBRAMANIAN, S.V., I. KAWACHI & G. DAVEY SMITH. 2007. sity, and chronic disease in countries undergoing the
Income inequality and the double burden of under- and nutrition transition: potential links and program/policy
184 Annals of the New York Academy of Sciences