Address for correspondence: Hélène F. Delisle, Ph.D., Department of Nutrition, Faculty of Medicine, Université de Montréal, PO Box 6128 Downtown Station, Montreal Que, Canada H3C 3J7. email@example.com
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 micronutrient 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 children, 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. Addressing 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, malnutrition, and ill-health.
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 children, families, and societies. Improving women's resources, including health, nutrition, education, and decisional power, is critical not only on the basis of equity, but also out of concern for the health of children and adults of several generations. Addressing the dual nutritional burden which weighs so heavily on women of developing countries (DCs) is a challenge, and promising approaches will be discussed. Moving beyond simply describing these problems as they affect women toward taking action for change is pivotal for the Millennium Development Goals (MDGs) to be achieved, since nearly all of them are directly or indirectly connected with improved condition of women.
Poverty and the Dual Forms of Malnutrition [Dysnutrition]
Poverty is the root cause of malnutrition and explains to a large extent its persistence in the developing world. Since the turn of the century, poverty and malnutrition have declined, but in an uneven fashion.1 There are varying degrees of poverty. Three quarters of the 162 million ultra-poor (living on less than $0.50 per day) are concentrated in sub-Saharan Africa, and the remainder are in South Asia. It is in those regions, where poverty and hunger are severe, that progress has been particularly slow. The Global Hunger Index is lowest in sub-Saharan Africa and South Asia. However, at variance with South Asia, there was little progress since 1990 in child underweight and under-five mortality rates in sub-Saharan Africa, although food-energy deficiency declined by 10%, which points to the slow progress of maternal health and nutrition.
Poverty goes beyond income inequality, encompassing health, social, and gender inequalities. It also refers to various types of deprivation and exclusion. It has been defined as including the different conditions of life with lack of access to basic needs, resources, and services, and it is often characterized by lack of freedom, education, and opportunities, in addition to lack of income and inequalities.2 Maternal health disparities are primarily evidenced in wide differences in maternal and neonatal death rates. Nearly all maternal and newborn deaths occur in DCs where women have inadequate access to health care.3“Time poverty” has been used to describe the situation of African women whose production and domestic (unpaid) work leaves little time for leisure or even for child care or for participating in development activities.4 Time poverty represents a critical dimension of women's poverty. Work burdens are gender-differentiated, and this may even be exacerbated in contexts of HIV/AIDS.4 In Benin, 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 extent that no leisure time was left.5
Hunger and overall undernutrition are usually considered synonymous. However, a more insidious form of malnutrition, that of “hidden hunger,” consists of specific micronutrient deficiencies, such as iron, iodine, and vitamin A deficiency disorders, to mention only the most prevalent. Micronutrient malnutrition is widespread and the consequences are life threatening for women and children.
Another form of malnutrition that is now spreading in DCs is related to obesity and other chronic diseases. It is often regarded as the opposite of undernutrition and is sometimes referred to as “overnutrition.” However, “overnutrition” is somewhat a misnomer because while obesity, for instance, is the result of energy intake in excess of requirements, it may also overlap with dietary inadequacies in micronutrients and fiber. We therefore suggest the term “dysnutrition” to encompass the whole range of nutritional problems: malnutrition, which comprises undernutrition and specific micronutrient deficiencies, and nutrition-related chronic diseases (NRCDs) including disorders of overnutrition and dietary imbalances.6 While malnutrition (undernutrition and micronutrient deficiencies) is traditionally considered a problem of the poor, NRCDs are seen as problems of the affluent, and this is one of the reasons NRCDs have been neglected in DCs up to recently. While hunger (or food insecurity) typifies poverty, obesity may also be associated with poverty. Indeed, except in extreme poverty, food insecurity often translates into energy-sufficient and even excessive, but poor quality, diets. Obesity of poverty is observed in industrialized countries, as well as in DCs undergoing the nutrition transition. Obesity and other NRCDs, such as diabetes and cardiovascular disease (CVD) are on the rise in DCs, even in low-income countries (but then particularly in cities), and they can no longer be considered diseases of affluence.7 Additionally, there is mounting evidence that the two forms of malnutrition are synergistic. According to the theory of the early origins of chronic diseases,8 nutritional insults in utero or during infancy permanently change the body's structure, function, and metabolism in such a way that the risk of chronic diseases, including diabetes and CVD is increased in later life. Therefore, early malnutrition exacerbates the health risks associated with the nutrition transition. Prevention of NRCDs is now a public health priority worldwide, and the World Health Assembly adopted in 2004 the WHO Global Strategy on Diet, Physical Activity, and Health.9
The Vulnerability of Women to Both Forms of Dysnutrition
Preschool children are one of the two groups most vulnerable to malnutrition. The second group is women and girls, who are also disproportionately affected by nutritional disorders associated with hunger or undernutrition and micronutrient deficiencies, but also affected by nutrition-related chronic conditions, such as obesity and diabetes. Yet women are more resilient physiologically than men. Given similar economic and health resources, they tend to live longer than men, although inequalities and discrimination may blunt this advantage. The most striking exceptions are in Qatar, Pakistan, Maldives, and Bangladesh, where average healthy life expectancy is at least 2.5 years higher in men than women.10
Women are doubly vulnerable to undernutrition or micronutrient deficiencies, owing to their high nutritional requirements for pregnancy and lactation, and also because of gender inequalities in poverty. In some but not all poor regions, gender discrimination in food allocation may also contribute to women's nutritional vulnerability. In Vietnam, for example, based on two sets of household surveys 5 years apart, men reaped proportionally more nutritional benefit from economic development than women, as reflected in food access and body weight data.11 This sort of discrimination was also observed in Guatemala when comparing dietary intake of boys and girls.12 Malnutrition usually evokes the specter of severely wasted children and adults, but it is not necessarily visible. Moderate malnutrition, with stunted growth, is also responsible for excess mortality in children,13 not only the clinical and severe forms of kwashiorkor and marasmus. It is estimated that malnutrition is involved in 50% of child deaths in DCs, according to WHO. In women of reproductive age, malnutrition is a major contributor to maternal mortality, and it is evidenced by stunting, chronic energy deficiency (CED), and micronutrient malnutrition. Maternal malnutrition is a major determinant of low birth weight in DCs. According to Harvey, iron deficiency anemia is responsible for 22% of maternal deaths and 24% of neonatal deaths.14
Women are also more vulnerable than men to obesity and other NRCDs, which have not replaced malnutrition-related diseases in DCs, resulting in the double burden of dysnutrition, primarily in southern Asia and sub-Saharan Africa. This double burden is now observed in low- and middle-income DCs. It is partly the result of the rapid nutrition transition characterized by major shifts of populations' eating patterns and lifestyles.15 Fueled by globalization, urbanization, technological evolution, and income changes, the nutrition transition involves progressive westernization of diets, with increased consumption of energy-dense, highly processed foods and drinks,16,17 and a more sedentary lifestyle owing to motorized transportation and mechanized work.
In a recent general press paper on world hunger, Pinstrup-Anderson and Cheng describe the dual nutritional problem of deficiencies and hunger in some households and obesity and related diseases in others.18 They remind that poverty is the main reason that hunger and nutritional deficiencies persist. However, they do not refer to obesity associated with poverty.
Nutrition-related Chronic Disease Risk Factors in Women of Developing Countries
The burden of chronic diseases in DCs is much higher than usually perceived. In 2005, chronic diseases—mainly CVDs, cancer, chronic respiratory diseases, and diabetes—were responsible for 50% of total disease burden in 23 countries which account for 80% of chronic disease mortality in DCs.19 WHO insisted on the need to address noncommunicable diseases, a neglected problem in DCs.20 Women are at a disadvantage: their age-standardized death rate for chronic diseases is 86% higher in DCs than in developed countries, whereas in men, it is 54% higher in DCs compared to developed countries.19 Furthermore, these deaths occur at an earlier age in DCs compared to high-income countries, depriving families and societies of adults in their productive years.
The nutrition transition fuels the increase of the metabolic syndrome, which is a clustering of CVD risk factors (obesity, insulin resistance, high blood pressure, dyslipidemia) in DCs, including sub-Saharan Africa.21,22 Urbanization is one determinant of the nutrition transition and the resulting upsurge of chronic diseases, such as abdominal obesity, type 2 diabetes, hypertension, dyslipidemia, and CVD. The interaction of adaptation, modernization, and stress is at play in the disease changes that accompany urbanization.23 DCs may be particularly vulnerable to nutrition transition because of recent or concurrent undernutrition, as it may compound the chronic disease risk associated with higher-fat diets, lack of physical activity, and other lifestyle patterns, such as tobacco smoking. In other words, as is so well put by Adair and Prentice, prenatal factors contribute to a phenotype that may be more sensitive to lifestyle factors associated with the development of obesity and the chronic diseases.24
Vorster and Kruger explored possible mechanisms to explain the known relationships among poverty, undernutrition, and CVD in DCs.2 They postulated that the link between poverty and CVD in South Africa could be explained by the high prevalence of undernutrition in children aged 1–9 years (9% underweight, 23% stunting, 3% wasting), the high prevalence of overweight in adults (54.5% in men and 58.5% in women), and the negative changes in diets (and lifestyles) when Africans urbanize, acculturate, and adopt western patterns.
Among resource-poor populations, women may be at greater risk of CVD, which is the single largest cause of women's deaths, accounting for one-third of the total worldwide.25 CVD risk factors are also increasing in women of DCs and will contribute to more women's than men's deaths by 2040.25 Some risk factors play a greater role in women than men: high triglyceride concentrations, low HDL-cholesterol, and diabetes. In the THUSA (Transition and Health during Urbanization in South Africa) study on CVD risk factors in South Africa, there were indications that while in men the CVD burden was heavier among the better-off, in women overweight/obesity (prevalence of 58.5%) and some other risk factors affected the rich and the poor.26
Although there are more similarities than differences in CVD risk factor trends in developed and DCs according to a recent review,27 one risk factor is particularly critical in DCs, and it is the risk associated with poor early growth and nutrition.28 Inadequate growth and nutrition in utero is associated with increased chronic disease risk, according to the theory of the early origins of chronic diseases.8 Poor nutrition in infancy, which is still highly prevalent in DCs, also appears associated with later chronic disease, although the evidence is less documented than in the case of intrauterine malnutrition. Several mechanisms may explain the link between early life undernutrition and chronic diseases, including programmed metabolic adaptation to an environment of scarcity in utero, by virtue of developmental plasticity.29 High blood pressure is the chronic disease risk factor which has been the most consistently associated with poor early growth in several population and age groups.30 Insulin resistance, abdominal obesity, and CVD have also shown links with fetal malnutrition reflected in low birth weight.31
Hypertension is widespread in DCs, particularly in sub-Saharan Africa.32–34 Its prevalence is not consistently higher in urban or better-off settings, which our studies in Benin confirmed (unpublished data). In poor Nordeste, Brazil, hypertension was more prevalent among women than men (38.5% versus 18.4%, respectively).35 Some studies suggest that illiterate and underweight women are at greater risk of being hypertensive than educated or normal weight women, although overweight/obese women are also at higher risk compared with normal weight women.36 Low socio-economic status (SES) was a significant risk factor for high blood pressure in both adolescent males and females in Congo.37 A U-curve may be postulated for the association of nutritional or economic status with the risk of hypertension.
The prevalence of overweight and obesity is much higher among women than men in most DCs. In low-income countries, the risk of obesity (and comorbidities) is higher in more affluent groups, but the burden shifts to poorer groups as GNP rises; the shifting point is the middle national income, according to the World Bank grouping of countries based on per capita income.38 Obesity is increasing rapidly under the influence of urbanization and westernization of diets, lifestyles, and culture. Cultural factors may also contribute to the higher prevalence of overweight or obesity in women compared to men. In several African countries, the ideal of beauty is not leanness, in contrast with western countries, but rather overweight, which is also a social status symbol.39,40 The gender difference occurs already at adolescence. In semi-urban areas of Congo (Kinshasa), the prevalence of overweight and obesity was 68.5% in female school adolescents, versus 24% in male adolescents.37
Physical inactivity as a CVD risk factor in DCs is of concern: 60–85% of the population of developed countries or DCs do not undertake sufficient physical activity to gain health benefits.25 Lack of physical activity is more of a problem in women in several settings, and particularly so among adolescent girls and low SES women. Studies in sub-Saharan countries, including in South Africa41 and Benin5 confirm that inactivity is related to women's overweight/obesity.
The Double Nutritional Burden in Women
The shift toward obesity and related chronic diseases in DCs does not mean that malnutrition (undernutrition and micronutrient deficiencies) is no longer a problem. In actuality, both forms often coexist and characterize the double burden of dysnutrition. The double nutritional burden weighs heavily on already inadequate and overextended health budgets of DCs.19 The double burden is also deleterious for societies and families. It may be observed at the individual level, and especially among women. The double burden is also observed within households, and it is usually reflected in the coexistence of maternal overweight/obesity and child chronic or acute malnutrition. Its increasing prevalence at the household, community, or country level is typical of rapidly transitioning countries, and is becoming a major public health concern. It may take the form of overlapping stunting or micronutrient malnutrition and obesity, as well as underweight in part of the population and overweight and obesity-related comorbidities in the other.
Double Burden of Malnutrition at the Country Level
Women are more exposed than men to the double burden. In Brazil, for instance, there were roughly two cases of underweight for one case of obesity in 1975; the ratio was reversed in 1997.38 Low-income women were more susceptible to both underweight and obesity. The combined prevalence, considered by the authors as a proxy for the total burden of nutritional diseases, was significantly higher in low-income than high-income women in both surveys: 22% versus 17% in 1975, and 22% versus 15% in 1997, respectively.
The double burden of dysnutrition is currently most problematic in middle-income DCs of Latin America and North and South Africa. While CED or underweight (BMI < 18.5 kg/m2) remains the major nutritional problem among women of low-income countries, the double burden of underweight and overweight/obesity (BMI ≥ 25 kg/m2) is emerging in South Asia and sub-Saharan Africa. In Bangladesh, for instance, in nationally representative samples of women of reproductive age, the prevalence of CED between 2000 and 2004 was 38.8% among rural and 29.7% among urban poor women, while 4.1% and 9.1%, respectively, were overweight or obese. It has been suggested to lower the BMI cutoffs of overweight and obesity in Asian populations because of evidence of emerging CVD factors and diabetes below the standard overweight cut-point of 25 kg/m2, possibly because of a proportionally higher percentage of body fat for any BMI in Asians compared to Caucasians.42 In Bangladeshi women, an additional 9.6% of rural and 18.9% of urban poor women were considered at risk of overweight, with a BMI at or above 23 kg/m2.43 Although in urban poor areas, the comparatively wealthier group had a higher prevalence of overweight/obesity (12.2%), the rate was 8.4% among the poorest women. Over the 5-year period, CED declined and overweight/obesity increased in both settings, but the increasing trend of high BMI was more marked in rural than urban women. In The Gambia, data collected a decade ago showed that the prevalence of CED was 18% and affected all social strata, whereas obesity was primarily a problem of urban women, with one-third affected beyond the age of 35 years.44
In resource-poor countries, a still-predominant feature of the double burden is that undernutrition tends to cluster among the impoverished and overweight/obesity among the more affluent. This is typical of the early stages of the nutrition transition. However, the situation is rapidly evolving, and overnutrition coexists increasingly with undernutrition even among the poor.
The Food and Agriculture Organization of the United Nations, on the basis of case studies in six DCs, proposed a typology of countries with respect to the double burden of malnutrition.45 Three country types are delineated, corresponding to advancing stages of the nutrition transition. The first group includes India and the Philippines. These countries are still in the early transition stages, with persistent undernutrition and micronutrient deficiencies in children and adults, and only emerging problems of obesity, diabetes, and high blood pressure in urban areas. The second type is illustrated by South Africa, where child stunting and micronutrient malnutrition are still widespread, but overweight/obesity is more a problem than undernutrition in adults. The third type, corresponding to a still more advanced stage of the nutrition transition (China, Egypt, Mexico), is characterized by a low prevalence of undernutrition, but the overlap of stunting and overweight/obesity in children, while in adults obesity is high or rapidly increasing, with increasing diabetes and coronary heart disease rates as correlates.
In Benin (West Africa), our on-going studies on the nutrition transition and cardiometabolic risk factors in adults of urban and semi-rural areas show that underweight is as prevalent in semirural women as overweight/obesity is among city women (see Table 1).
Table 1. Nutritional status of women aged 25–60 years in three sites in Benin (West Africa)
Large city (Cotonou) N = 100
Medium-size city (Ouidah) N = 85
Semi-rural outskirts (Ouidah) N = 85
Underweight (BMI < 18.5 kg/m2)
Normal weight (18.5 ≤ BMI < 25)
Overweight (25 ≤ BMI < 30)
Obese (BMI ≥ 30)
Income and gender inequalities appear to have additive or compound effects. In India, for instance, it was found that state income inequality increased the likelihood of both undernutrition and overweight among women, that is, of the double nutritional burden, even after adjusting for several individual and state-level covariates.46 For one standard deviation increment in income inequality measured by the Gini coefficient, the odds ratio of being underweight increased by 19% (P = 0.02) while the odds ratio of being obese increased by 21% (P < 0.001). The adverse effect of state income inequality is also observed for overweight. The contextual inequality appears to exacerbate the known impact of individual SES as low SES women experience the greatest risk of underweight whereas the high SES ones are exposed to higher obesity risk. The authors suggested that, in regions in economic transition and growth, focusing on reducing economic inequalities is likely to address the dual burden.
Double Nutritional Burden Households
The phenomenon of coexistence of child undernutrition and maternal overweight/obesity in the same households has been described in several DC settings, including South Africa, China, Brazil, Haiti, and Benin.47,48 Comparing Russia, China, and Brazil, the prevalence of the double burden among households was very similar: 8% in Russia and China, and 11% in Brazil, based on national surveys.48 In a poor rural community of Malaysia, 15.7% of mother/child pairs showed the double burden,49 which is quite similar to what we observed in a shanty town of Port-au-Prince, Haiti (14%) and in poor neighborhoods of Cotonou, Benin (16%).50,51
The coexistence of maternal overweight and child underweight in the same household portrays rapid nutrition transition.52 It suggests that similar circumstances, whether environmental, behavioral, or individual, favor the development of underweight in children and overweight in mothers.53 It may also illustrate the differential rate of change of the prenatal and postnatal environment.29 The prenatal environment is determined by maternal size, body composition, and metabolism, which is partly determined in turn by the mother's own growth in utero and during infancy and childhood. In the nutrition transition context, small mothers have small babies because of maternal size constraints, and then the children grow rapidly owing to more favorable factors in the postnatal environment. Mothers exposed to the nutrition transition context may become overweight or obese, while their children are stunted, perhaps since intrauterine life. In an analysis of secondary data on more than 600 mother/child pairs in Mexico, it was found that maternal central obesity and child stunting were present in 6% of pairs. The odds of having a stunted child were twice as great 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” households had a higher SES than households with a malnourished child and no maternal overweight. Interestingly, we also found that a more diversified diet was protective of the double burden, implying that food insecurity contributes to both adult overweight and child malnutrition (see Table 2). Thus, maternal obesity and child stunting do not have opposite causes but appear as responses to the same insults at different stages of the lifecycle. We also found in the same study that compared with households with only maternal overweight, those with a malnourished child had poorer household sanitation. Similarly, in a study in the North West Province of South Africa, poor hygiene practices were a major determinant for child undernutrition.55 Low education of mothers was also a major determinant of child undernutrition, which again underlines the role of maternal profile for child nutritional status.
Table 2. Predictors of the concurrent presence of malnutrition in at least one child and maternal overweight51
The most widely studied phenotype of the double burden at the individual level is that of stunting and overweight/obesity, whether in children or in adults. Other types are the overlap of stunting with hypertension or insulin resistance, and of anemia and obesity. According to published data, all these manifestations of the double burden of dysnutrition are more common in women than in men.
The association between stunting in infancy and obesity later on in life has been reported in several studies conducted in nutrition-transitioning countries.56 And stunting in infancy is already present at birth in many cases, as a result of maternal constraint or poor nutrition. The mechanism is not yet elucidated, but it has been proposed that defective fat oxidation, as observed in stunted children in Brazil, may be a culprit.57
In Egypt, the odds of being overweight/obese were 80.8% higher in women of reproductive age who were possibly deficient in micronutrients based on per capita supply of vitamin A, iron, and zinc in the household.58 This study concludes that the overlap between micronutrient inadequacies and obesity is not given enough attention by policy makers and researchers as well, and one of the implications is that food subsidies aggravate the obesity problem as these target energy-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 pressure was significantly more prevalent among stunted adults compared to normal-height adults, particularly in women.35 Short stature, an epidemiological indicator of chronic malnutrition in early life, was more strongly associated with high blood pressure in women than men. The odds ratio for hypertension in stunted women compared to nonstunted ones was 1.98 (95% CI [Confidence Interval] 1.22–2.96). The negative association of stature with hypertension, as well as with obesity, was observed in women, but not in men. Indeed short stature was the single most important risk factor for hypertension in women. In the Congo, it was observed that in male adolescents but not in female adolescents, chronic malnutrition as well as obesity was a risk factor for high blood pressure.37
A small case–control study conducted in Mexico showed that men who had suffered malnutrition in their early years were more prone to insulin resistance when they developed abdominal obesity, suggesting that obesity may have more adverse effects in individuals who were exposed to early malnutrition.59 This study was only conducted in men, but several other reports linked low birth weight with increased insulin resistance in men and women, including a study on 600 men and women aged 45 years in China.60
Probably the most prevalent phenotype of double dysnutrition is the simultaneous presence of micronutrient malnutrition and overweight/obesity, as “transitional” diets are typically energy dense but micronutrient poor. This situation is of concern not only because of the adverse health outcomes of both forms of dysnutrition, but also because micronutrient deficiencies may actually contribute to chronic diseases.61,62 The evidence is still limited and research in this area is direly needed, but micronutrients in short supply in several DCs, including folate and antioxidants, such as iron, zinc, vitamin C, and carotenoids, may contribute to CVD (and certain types of cancer). Zinc deficiency is widespread in DCs. It could contribute to oxidative stress and to the development and progression of diabetes as well, by virtue of its antioxidant properties and also because of the metabolic links between zinc and insulin in the pancreas.61 Analysis of cross-sectional data from Egypt, Mexico, and Peru revealed that overweight women did not necessarily meet their iron requirements. The prevalence of overweight was above 50% in all three countries, reaching 77% in Egypt. While the odds of anemia were lower in overweight/obese women in Egypt and Peru, there was no difference among BMI groups in Mexican women.
The Insidious Impact of Maternal Dysnutrition on the Health of Whole Societies
Gill et al. reviewed the evidence linking maternal health with development and proposed an interesting framework on the key links at the individual, family, and society level.63 Women are mothers and individuals; they are also family members and citizens. This framework is useful to better comprehend how women's health, and notably their nutritional status, impacts all those levels, and in the present and future generations. Women's health is connected with their own status, their education, employment, and decisional power. Their status is conducive to better health, and conversely, their health contributes to their status and condition. It is primarily as mothers that women have been the focus of health efforts. Maternal health affects women's survival and the health and survival of their children. Nutrition is critical for maternal health and for reducing maternal mortality in DCs. For instance, as already mentioned, iron deficiency anemia reportedly accounts for 22% of maternal deaths and for 24% of neonatal deaths.14 Indeed, interventions to improve maternal diets and to promote breastfeeding are relevant everywhere.
Women's status, health, and nutrition also impact families' income, welfare, and well-being, and it has been shown in several settings that maternal income, more than that men's income, is directly reflected in better nutrition and health of children.64 That poor maternal health and nutrition perpetuates the cycle of ill-health and malnutrition across generations is further described below. Although more research is required to explore these interrelationships in a more explicit manner, women's health is also an important determinant for their own productivity and for economic development at the macro level.63
A seminal paper by Asmani and Sen discusses the relationship of gender inequality and women's deprivation, on the one hand, and the health cost of these for the whole population, men included.65 Some adverse consequences of women's poor health and nutrition harm the entire population because the offspring are affected, as children and as future adults. The authors describe an overlapping health transition with two disease regimes, the old and the new regime. Gender inequality, which results in maternal poverty, malnutrition, and poor health, exacerbates the old regime through child undernutrition. It also exacerbates the new disease transition through the theory of the early origins of chronic diseases.8 Thus, gender inequality leads to this double jeopardy connected with maternal malnutrition, itself connected with inequality and deprivation. “What begins as the neglect of the interests of women ends up causing adversities in the health and survival of all in the developing world.”65 The consequences of maternal undernutrition are depicted in Figure 1, adapted from that of Asmani and Sen.65 Fetal growth restriction associated with maternal stunting (malnutrition in her early life), CED status, or poor diet are now known to be associated with low birth weight for gestational age and with a high risk of malnutrition in the children who survive. The offspring of malnourished mothers are also subsequently at increased risk of CVD, abdominal obesity, hypertension, and diabetes. Additionally, female offspring of malnourished mothers are at higher odds of becoming stunted women themselves and to have low–birth weight babies, thereby perpetuating the vicious cycle of malnutrition. Thus, malnutrition in mothers is responsible for intergenerational dysnutrition, especially in regions undergoing the nutrition transition.66,67 Intergenerational dysnutrition is also related to maternal obesity, which exposes the offspring to increased health risk associated with gestational diabetes and macrosomia.68 The long-term adverse impact of fetal malnutrition is an additional and compelling argument to concentrate on improving nutritional status of young girls and women, preferably before, but if not, as early as possible, and throughout pregnancy.28
Data from developed and DCs suggest that not only small size at birth, but also postnatal growth retardation in infancy followed with rapid weight gain in childhood, are independent factors of increased risk of adulthood obesity, diabetes, hypertension, and CVD. This is of concern for DCs, because 17% of the neonates have a low birth weight, that is, nearly three times as many as in developed countries.69 Adequate growth should be sought in the first 2 years of life, with particular attention to infants born small whose catch-up growth in height can only be achieved over this period. During childhood, the avoidance of accelerated weight gain, even among those of normal BMI is the main strategy to reduce the risk of obesity and metabolic syndrome.67,70
Policy and Strategies to Curb the Double Nutritional Burden
Poverty is complex and multidimensional, and so is dysnutrition. The causal links between the two, for there are, are bidirectional. In order to roll back poverty, measures to curb dysnutrition are essential. And conversely, investing in social capital of the poor, including through nutrition programs, may yield high returns in terms of improved health, especially of mothers and children.
Much has been recommended, discussed, written, and planned in order to hasten progress in health and development, including the now famous MDGs. However, it is disconcerting that nutrition is still so much ignored or seriously neglected in policies for health, education, gender equality, or poverty reduction, particularly in sub-Saharan Africa, considering that it is the worst region in the world as regards child and maternal malnutrition and mortality rates. In the Commission for Africa report, for instance, Chopra and Darnton-Hill criticize the fact that the chapter on education and health devotes less than half a page to nutrition, and only to address parasite control and micronutrient support.71 Similarly, it was a surprise to us not to see a single mention of nutrition, diet, dietary education, or even food (except for food availability) in a whole paper on the management of diabetes in sub-Saharan Africa,72 given that healthy eating is the cornerstone of treatment as well as prevention of type 2 diabetes. Much advocacy effort is needed for nutrition to be mainstreamed, and particularly so for addressing chronic diseases connected with the nutrition transition in resource-poor DCs.
Nonetheless, there are encouraging policies and strategies as regards gender equality, women's health and nutrition, and empowerment. Women's education is empowering,73 and it may bring about major improvements in maternal and child nutrition.74 Additionally, women's empowerment is one of the most effective ways of cutting down birth rates.65 Maternal malnutrition is responsible for excess maternal and neonatal mortality; improvements in women's nutrition will decrease mortality, while increasing the nutritional status of surviving children. Additionally, improved maternal nutrition will contribute to enhancing the economic productivity of women and decreasing in their progeny the chronic disease risk associated with poor nutrition in early life. As stated in a UNICEF report on the state of children, gender equality is central to realizing the MDGs.75 More gender equality will empower women to overcome poverty and will assist their children, families, communities, and countries as well. Improving nutrition, particularly that of women, is also considered key to meeting the MDGs.14 Based on the premise that investing in nutrition and gender is an investment in MDGs with a high return, the International Center for Research on Women and its partners successfully implemented the Nutrition Gender Initiative in Ghana, India, and Bangladesh between 2002 and 2005.76 The goal of the Nutrition and Gender Initiative (NGI) is to add nutrition and gender objectives and actions into development programs and thereby contribute to achieving the following MDGs, through action research, communication, and advocacy: eradication of poverty and hunger; achievement of universal primary education; reaching gender equality and empowerment of women; reduction of child mortality; and improvement of maternal and reproductive health. The project views nutrition as a cross-cutting issue, interconnected with gender, and involving several development sectors and players. The NGI strives to find suitable approaches to addressing malnutrition throughout the lifecycle as a means of improving gender equality, along with enhancing institutional capacity for gender analysis, nutrition programming, and advocacy.
Several risk factors and opportunities for prevention are similar for chronic diseases, such as cancer, CVD, and diabetes. Additionally, the same behavioral risk factors are observed in developed countries and DCs.33,34 However, programs to prevent obesity and related chronic diseases are rather new in several DCs. A wide range of such programs was described in a summary paper77 and encompassed worksite, community-based school, and national programs to improve diet and increase physical activity in 14 DCs. The template presented by van der Sande and colleagues for the prevention and control of CVD in sub-Saharan Africa is still highly relevant.78 As suggested in this paper, a comprehensive program will be more acceptable and effective if it combines prevention and treatment. As noted for South Africa, the poor, however, may have limited knowledge on, or interest in, primary prevention of CVD behavioral risk factors, as meeting their basic needs takes up all their attention and energy.2 Furthermore, the poor have limited access to secondary prevention. They are therefore at high risk and should be targeted, but promoting healthy lifestyles, including an adequate but prudent diet, may not be enough inasmuch as limited access to resources is a major constraint to healthful behaviors. Means of increasing access to resources are therefore needed, and particularly so among women, who are disproportionately poor and disproportionately affected in their own health and that of their children by poverty. Means of coupling nutritional improvement with women's income generation should be sought and exploited as much as possible. This was the concept behind the red palm oil development project in Burkina Faso, with the dual objective of improving vitamin A nutrition of mothers and children and of generating income for women extracting and retailing the oil.79
The overlap of malnutrition and NRCDs in the same population groups is a challenging issue to health bodies. Creative initiatives are direly needed. Governments have to be involved in the prevention and control of chronic diseases, were it only to help individuals to make informed choices regarding risk behaviors through fostering the generation of relevant information, and making this information widely available and understood.19 Addressing obesity and chronic diseases simultaneously is not simple. It even creates a “cultural shock” among decision makers,80 as policies and programs have been focusing on food insecurity, undernutrition, and micronutrient deficiencies. Vorster and Kruger plead for an integrated, transdisciplinary, and multisectoral approach to break the vicious cycle of poverty and undernutrition for the long-term prevention of CVD.2 Governments must feel the pressure. Diabetes may be a key word, as the associated health costs are enormous, and health ministries are well aware of them, more so than of the health risk associated with obesity.81 Linking diabetes with child obesity and with maternal risk may be a worthy strategy.
Promoting diets that are adequate, well-balanced, and safe yet affordable and in line with cultural practices and local food production appears as one of the pillars of the prevention of the double burden of malnutrition,82 along with the promotion of physical activity. The 2004 WHO global strategy on diet and physical activity focused on food, agriculture, and multisectoral policies to promote healthy eating and physical activity.9 Traditional diets, oftentimes more diversified and higher in fruits and vegetables, need to be rehabilitated, and physical activity has to become socially desirable. Brazil offers an interesting example. A national food and nutrition policy was designed early in the new century to continue to combat nutritional deficiencies, while also addressing the prevention of NRCDs.83 The policy is essentially to promote, protect, and support healthy eating and lifestyle patterns through legislative measures, communication, and capacity building.
As stressed by Eckhardt, the most important strategy for reducing the double burden of micronutrient malnutrition and overweight/obesity in nutrition-transitioning countries is to enhance diet quality throughout the life cycle.61 For this purpose, developing dietary guidelines appears important. Food-based dietary guidelines should become available at the country or regional level in order to take account of cultural patterns. For those individuals already diagnosed with diabetes, health professionals should devise location-specific and tailor-made eating plans based on up-to-date international recommendations. For all of this to happen, the current paucity of well-trained nutritionists in several sub-Saharan regions urgently needs to be remedied. Indeed a 2005 report by WHO insisted on preparing the workforce for the growing burden of chronic diseases.84
Preventing all forms of dysnutrition among women is key, and measures should start early. The school setting, for instance, is particularly appropriate for preventive actions.85,86 A recent WHO initiative intended to fight the double burden of malnutrition in schools, the “Nutrition-friendly School Initiative,” is being promoted and tested. As suggested by some,39 young generations in emerging countries are likely to be responsive to messages for the prevention of obesity, much like in western countries, because of their exposure to global media.
Maternal and child nutrition should not be dichotomized, however, because they are closely connected. This is in line with the approach of the continuum of care for maternal, newborn, and child health.87 Nutrition ought to be integrated in the continuum of care, at adolescent, prepregnancy, neonatal, and child care levels. For instance, adolescent and prepregnancy nutrition is part of family and community care, and folate and iron supplementation is integrated into reproductive health care. It is argued in the same paper that if the eight proposed continuum of care packages were implemented to reach most families, the lives of 2/3 of the 10 million babies and children dying every year could be saved, and many of the half-million maternal deaths could be averted, along with many stillbirths. However, the dual burden of malnutrition in women and the dramatic adverse effects in the progeny is not explicitly considered in this strategy.
Surveillance, which provides appropriate information for advocating for policy and action tailored to address the double burden of dysnutrition, is required, as recently emphasized.71 Sawaya and colleagues, in a review of the association between chronic undernutrition and hypertension, also suggested that healthcare practitioners working in low-income urban communities monitor blood pressure in order to detect and treat in timely fashion high blood pressure that tends to be associated with early life malnutrition.88
Research needs in the realm of the double burden of dysnutrition in DCs are pressing. Research priorities may include, in addition to epidemiological and surveillance data on chronic disease risk factors and the prevalence of the double burden, the links between micronutrient malnutrition and chronic diseases, the contribution of stress of life to chronic diseases particularly in urban settings, changes in food provisioning of urban and rural communities, and the relevance and effectiveness of location-specific dietary guidelines for simultaneously tackling undernutrition, micronutrient malnutrition, overnutrition, and dietary imbalances.
In summary, improving nutrition, in particular women's nutrition, is critical for health, poverty reduction, and development, and it has to be mainstreamed. Healthy diets and lifestyles are obviously key for preventing the various forms of under- or overnutrition, but for the behavioral risk factors to recede, an enabling political, physical, socioeconomic, and cultural environment is needed so that required changes are feasible. The rising tide of NRCDs is now a compelling reason to tackle the dual burden of malnutrition in DCs. Research as well as surveillance should be utilized to fuel advocacy efforts and to inform policy and programming.