Addressing the Double Burden of Malnutrition in Developing Countries: Need for Strategies to Improve the Lean Body Mass

Abstract

The double burden of childhood undernutrition and adult-onset adiposity-related chronic diseases is a key concern in many developing countries that are currently undergoing epidemiological and nutrition transition. Impaired linear growth with suboptimal lean body mass development seems to be the link between these 2 seemingly contrasting forms of malnutrition. Studies assessing the role of early nutrition in the later lean body mass development have shown consistent positive association. In addition, the nutrition during life course, especially the dietary intake of protein, zinc, calcium, and vitamin D status, impacts the lean body mass. Promoting increased intake of these important nutrients throughout life course would, therefore, be important for optimal development and maintenance of lean body mass. Diversified diets with increased consumption of nutrient-rich foods, especially milk and other animal source foods, are crucial for the development of optimal body composition and alleviation of the double burden of malnutrition.

Introduction

The double burden of malnutrition, indicated by high prevalence of childhood undernutrition as well as adiposity-related chronic diseases, is a key concern in many low- and middle-income countries including India that are currently undergoing nutrition and epidemiological transition. ^1,2 As per the estimates by the International Diabetes Federation, over 70 million adults in India are diabetic and more than 35 million adults are prediabetic. ³ Recent evidence from Indian Council of Medical Research - India Diabetes (ICMR-INDIAB) study showed that, in the urban population older than 55 years of age, the prevalence of diabetes was almost 25%. ⁴ It is predicted that by 2040, India will have the highest number of diabetics in the world. ³ Concurrently, the prevalence of obesity in adults, which was <10% in 2005-2006, has increased to 20% in 2015-2016. ^5,6 However, the prevalence of undernutrition in adults, as indicated by a body mass index (BMI) of <18.5 kg/m², which is considered “chronic energy deficiency,” is still high in India affecting almost 20% of men and women. ⁶ In addition, childhood undernutrition, including low birth weight, stunting, and underweight, is highly prevalent and is still a priority area. ⁶ Addressing the current double burden of 2 apparently contrasting forms of malnutrition poses enormous challenge for the nutrition policies of developing countries in order to address the problems of underweight and overweight simultaneously.

Body Composition and Cardiometabolic Risk

A large number of studies from India and other Asian countries have shown elevated cardiometabolic risk within a range of BMI which is considered as normal. ⁷ This has been attributed to the peculiar body composition with high fat and low muscle mass in Asians compared to the other ethnic groups. ^{8 -10} For example, a study conducted in 278 low-income group women living in an urban slum in Hyderabad, India, which assessed their body composition using dual energy X-ray absorptiometry, showed that although these women were not obese as per the BMI criteria (mean BMI 21.9 kg/m2), they had adipose body composition with mean body fat percentage of 33. ¹¹ Moreover, a steep rise in the body fat percentage with an increase in BMI was observed within the normal BMI range, as the BMI values of 20 and 22 kg/m2 corresponded to the body fat percentage of 30 and 35, respectively. The BMI range corresponding to optimal body fat percentage of <30 for this population would be very narrow and close to the BMI of 18.5 kg/m² which is associated with enhanced mortality and morbidity. The question of defining a BMI cutoff for adiposity in Indians, therefore, requires rethinking. Instead, attention needs to be focused on reducing the slope of the BMI–body fat relationship by enhancing the lean body mass and muscle mass of an individual. The anthropometric correlates of body fat distribution analyzed in this study provide valuable insights regarding how it might be possible to achieve optimal body composition in this population. Analysis of body composition in women in different tertiles of height in the above-mentioned study showed that women in the highest tertile of height, despite their higher body weight, did not have higher body fat. Taller height in the study women was linked with significantly higher lean body mass without concurrent higher fat mass, suggesting that achieving a higher lean body mass without increase in body fat percentage is possible with improvement in height. A number of studies in other settings have also demonstrated a link between short stature and elevated risk of diabetes. ¹² The above-mentioned evidence suggests that the population-level strategies aiming at reducing the double burden of malnutrition should focus on achievement of the optimal body composition by reducing childhood stunting and achieving optimal growth during adolescence.

Nutrition during Life Course and Optimal Body Composition

Early Nutrition and Later Body Composition

It has been suggested that the adipose phenotype in relatively thin individuals may be “programmed” by undernutrition in early life, as the ethnic differences in body composition have been observed even at birth in a few studies. ^13,14 In addition, a large number of observational studies have indicated that compromised nutrition and growth during early life is linked with lower lean body mass and higher risk of metabolic syndrome in later life. ^{15 -17} The lower muscle mass linked with early undernutrition observed in Indians represents reduced metabolic capacity possibly through decreased glucose clearance. ¹² Weight gain after the critical period of early childhood is related to elevated body fat, which not only promotes faster maturation but also increases the metabolic load and the risk of diabetes and cardiovascular disease. ^18,19 In a large, long-term prospective cohort study from New Delhi, India, increased BMI in early childhood was associated with enhanced adult lean body mass, but the BMI and BMI gain in later childhood were associated with higher fat mass during adulthood. ²⁰

Although majority of the observational studies have used birth weight as a proxy for early nutritional status, it has been suggested that the size at birth may not be the most appropriate indicator of nutritional status, because apart from nutrition, it is affected by genetic influences as well as by a number of other environmental factors such as maternal infections, smoking, access to health care, and so on. ²¹ Studies evaluating the long-term impact of nutrition interventions in early life, therefore, provide valuable information on the relationship between early nutrition and later outcomes. For example, a community-based study from Guatemala examined this relationship using the opportunity provided by a randomized controlled trial of maternal energy protein supplementation during pregnancy, although this trial was primarily conducted to evaluate the nutrition intervention for improving pregnancy and birth outcome. The study showed that nutrition supplementation in early life was associated with a taller height and a higher lean body mass in adolescence, especially in females. ²² Another study from India, the Andhra Pradesh Children and Parents Study, assessed the long-term impact of a nutritional supplement provided to pregnant women and their young children through a government-funded program—Integrated Child Development Services—on the body composition and cardiovascular risk indicators in the offspring in later life. ^23,24 When the participants were examined during adolescence, those from the intervention group were taller and had favorable cardiometabolic risk profile compared to the control group participants. ²³ However, during later follow-up when the participants were aged 18 to 21 years, the beneficial impact of the nutrition intervention on body composition was no longer seen. On the other hand, their contemporary socioeconomic status, diet, and physical activity were the major determinants of the lean body mass at this time point. ²⁴ Although the study allowed realistic estimation of the long-term impact of a nutrition intervention provided through the government program, it is possible that the effective dose of supplement was too small due to possible sharing of the supplement with other family members, as the consumption of the supplement was not supervised. Other reason for the observation that the favorable impact of nutrition intervention in early life on lean body mass and cardiometabolic disease risk did not persist beyond adolescence could be due to “dilution” of the programming effect of early nutrition by diet and other lifestyle changes over the duration of follow-up when the study villages urbanized rapidly.

Overall, there is consistent evidence suggesting that larger birth weight and higher postnatal growth in early life are associated with a higher lean body mass in later life. On the other hand, a few studies that assessed the long-term impact of protein energy supplementation in early life on the later lean body mass indicate modest and inconsistent benefit.

Nutrition in Childhood and Adolescence and Later Body Composition

Apart from the role of early nutrition in “programming” of the lean body mass, evidence suggests that nutritional influences continue to exert significant impact on the body composition throughout life course. In developing countries, undernutrition linked with suboptimal diets continues beyond first 1000 days and results in the “accumulation of risks” as a result of long-term gradual insults. ²⁵ A large number of studies (observational as well as intervention studies) in schoolchildren and adolescents from low- and middle-income countries have reported a positive influence of dietary protein and micronutrients such as zinc and calcium as well as optimal vitamin D status on the lean body mass. ^{26 -29} Low intake of milk and other animal source foods that are rich sources of the abovementioned nutrients, therefore, contributes substantially to the low lean body mass and the double burden of malnutrition in developing countries.

Possible Mechanisms underlying Double Burden of Malnutrition

Substantial evidence shows that low birth weight and undernutrition during childhood increases the risk of suboptimal body composition with low lean body mass and high fat mass. The coexistence of high rates of childhood undernutrition and high proportion of adults with low lean body mass in countries such as India supports this evidence. Lifestyle changes associated with nutrition transition, especially the excessive intake of processed foods and reduced physical activity, may further enhance fat deposition. In addition, the low muscle mass itself may predispose to fat accretion by influencing the energy balance, as the synthesis and breakdown of muscle protein are principally responsible for the energy expenditure of resting muscle. ³⁰ It has been estimated that a deficit of 10 kg in muscle mass translates to a conservation of 100 kcal/d in energy expenditure, which in turn translates to accumulation of 4.7 kg fat mass per year. ³¹ In addition, childhood stunting is associated with long-term adaptations such as impaired fat oxidation and preferential oxidation of carbohydrate, and therefore, stunted children tend to have a tendency to accumulate fat in later life. ³² The energy conservation and fat accretion in adults are also caused by lower physical activity linked with childhood stunting. ³³ It thus appears that the poor muscle mass linked with undernutrition during life course could be an important reason for the high fat phenotype in this population.

Addressing the Double Burden of Malnutrition

To address the double burden of malnutrition in transitioning countries like India, it is imperative that public health interventions focus on the “developmental programming” by improving early life nutrition as well as improving nutrition during life course. Several studies that assessed the impact of different macro/micronutrient supplementation interventions during pregnancy in reducing the intrauterine growth retardation have been reported. A meta-analysis, which included 11 studies that provided balanced protein calorie supplementation during pregnancy, found that the intervention reduced the risk of giving birth to small-for-gestational age infants by around 30%. ³⁴ On the other hand, studies that assessed the impact of multiple micronutrient supplementation, compared to the iron folate supplementation, showed a much lower benefit with an estimated reduction of 10% in the proportion of small-for-gestational age babies. ³⁵ However, the modest benefit of antenatal multiple micronutrient supplementation in reducing intrauterine growth restriction may not persist later in childhood as indicated by a meta-analysis which did not find a significant benefit of antenatal multi-micronutrient supplementation for improvement in weight, height, and weight-for-height z score at 5 years of age in the offspring. ³⁶ Another randomized controlled trial from India, which included more than 6500 women, assessed the impact of improving women’s dietary micronutrient intake (with a supplement made with micronutrient-rich foods such as dried green leafy vegetable powder, milk powder, fresh green leafy vegetables, dried fruit, chickpeas, and sesame seeds) before conception and throughout pregnancy on the birth weight of the offspring. ³⁷ The intervention had no overall significant effect on the birth weight of the offspring, but the subgroup analyses indicated a possible increase in birth weight if the maternal supplementation was initiated ≥3 months before conception. Furthermore, in a subgroup of women who had a higher prepregnancy BMI (>21.8 kg/m2), the supplementation resulted in >100-g increase in birth weight compared to the control group. This is in contrast to studies on maternal protein energy supplementation during pregnancy, where the impact on birth weight was high in women who were most undernourished and vulnerable. ³⁴ The findings are, however, consistent with data from multiple micronutrient supplementation trials in pregnancy which showed a greater impact on birth weight in mothers with higher BMI. ³⁸ It is interesting to note that in the presence of protein energy deficiency as indicated by low BMI, the beneficial impact of micronutrients was not seen possibly due to inadequate substrate availability for utilization by the supplemented micronutrients. The authors suggested that extra macronutrients, in addition to micronutrients, may be needed to improve the birth weight of the offspring in undernourished women from the low- and middle-income countries.

Observational studies from high-income countries have shown a positive association between maternal milk intake and offspring birth weight. ^39,40 Data based on intervention studies from developing countries are scarce, but a few observational studies have indicated a strong association of milk intake during pregnancy with the birth size of the offspring. ⁴¹

Apart from maternal diet, maternal body composition may also influence the birth weight of the offspring as indicated by a study from India which showed that maternal lean body mass, not fat mass, was a major determinant of birth weight. ⁴² Thus, improving lean body mass, especially of girls and women, would be important for breaking the intergenerational cycle of undernutrition.

Importance of Animal Source Foods

Animal source foods, particularly meat and dairy products, are rich sources of high-quality protein and micronutrients including zinc, iron, calcium, and vitamin B₁₂. The micronutrients in the animal source foods are more bioavailable compared to those from the plant source foods. Proportion of energy provided by animal source foods typically varies from 5% to 10% in low-income countries compared to >30% in industrialized countries. ⁴³ Increasing the intake of animal source foods in population groups consuming monotonous cereal-based diets may improve the lean body mass and linear growth in children. For example, a study from Kenya examined the impact of supplementation with a meat, milk, or energy supplement on the growth and muscle mass of schoolchildren compared to a control group without a supplement. After almost 2 years of supplementation, the children in the meat group had significantly higher gain in mid-upper-arm muscle area than the other groups. To a lesser extent, children who received the milk or energy supplement also gained more mid-upper-arm muscle area than the controls. ⁴⁴ Another community-based study from Malawi, which examined the efficacy of dietary diversification by increased intake of animal source foods, especially whole dried fish with bones, in young children, showed that the intervention resulted in increased muscle mass, although it did not impact weight or height gain. ⁴⁵ Substantial evidence demonstrates that higher intake of milk is positively associated with linear growth and higher lean body mass in infancy, childhood, and adolescence. ⁴⁶ Analysis of the National Family Health Survey data (third round in 2005-2006) from India also indicated that milk consumption had a strong positive association with the height of men and women. ⁴⁷ The growth-promoting effect of milk can be attributed to its high-quality protein, multiple micronutrients (vitamin B₁₂, vitamin A, riboflavin, and folate), and stimulation of growth factors. ⁴⁸

Consumption of animal source foods including milk and milk products is very low in developing countries like India as indicated by the data based on the surveys conducted by the National Nutritional Monitoring Bureau in rural households. ⁴⁹ An increase in consumption of dairy and other animal source foods in India and other developing countries would be important for alleviating the double burden of malnutrition.

Conclusion

The double burden of childhood undernutrition and adiposity-related, adult-onset chronic diseases in countries undergoing epidemiological and nutrition transition is a significant public health problem and nutrition policy challenge. Suboptimal lean body mass seems to be the link between these 2 forms of malnutrition, and these 2 problems need to be considered as dual manifestations of a common problem of the low-quality diets lacking important food groups such as dairy and other animal source foods. Consistent evidence suggests that higher birth weight and better nutritional status in childhood have a strong positive influence on the lean body mass in later life. In addition, the nutritional influences, especially the dietary intake of nutrients such as protein, zinc, calcium, and vitamin D status, impact the lean body mass throughout the life course. Improving the consumption of diverse foods, especially milk and other animal source foods, is necessary for developing optimal body composition. Nutrition interventions for tackling undernutrition should aim to increase the lean body mass to address the double burden of malnutrition.