|
 
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| REVIEW ARTICLE |
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| Year : 2013 | Volume
: 15
| Issue : 2 | Page : 69-75 |
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Does docosahexaenoic acid play a role in infant malnutrition in the children of Fulani nomads in Northern Nigeria?
Robert H Glew1, Dorothy J VanderJagt2
1 Department of Surgery, School of Medicine, University of New Mexico, Albuquerque, New Mexico, USA
2 Department of Biochemistry and Molecular Biology, School of Medicine, University of New Mexico, Albuquerque, New Mexico, USA
| Date of Web Publication | 24-Dec-2013 |
Correspondence Address:
Robert H Glew
Department of Surgery, School of Medicine, MSC 10 5610, 1 University of New Mexico, Albuquerque, NM 87131 0001
USA
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/2276-7096.123574
Malnutrition is a major contributor to the death of children under 5 years of age in sub-Saharan Africa. Furthermore, poor nutrition causes stunting and underweight in infants and children while at the same time putting at risk normal neurologic and cognitive development. A recent study of rural Fulani infants up to age 2 years in northern Nigeria found that more than one-quarter were stunted and underweight. The nutritional status of these infants was relatively sound at birth but progressively declined over the following 2 years. While insufficient dietary macronutrients such as protein and carbohydrate and micronutrients such as iodine, zinc, vitamin A and iron may well have contributed to their post-natal growth retardation, in this report we raise the possibility that inadequate intake of essential long-chain ω-3 fatty acids, docosahexaenoic acid (DHA) in particular, by infants during the first few years of life may play a role in childhood malnutrition in this part of the world, especially in populations like the Fulani pastoralists who live far-removed from the ocean which would otherwise provide access to DHA-rich seafood. We conclude this piece by suggesting several approaches for improving the DHA status of pregnant and lactating Fulani women and their offspring in Nigeria. Keywords: Docosahexaenoic acid, fatty acids, Fulani, malnutrition, Nigeria
How to cite this article:
Glew RH, VanderJagt DJ. Does docosahexaenoic acid play a role in infant malnutrition in the children of Fulani nomads in Northern Nigeria?. J Med Trop 2013;15:69-75 |
How to cite this URL:
Glew RH, VanderJagt DJ. Does docosahexaenoic acid play a role in infant malnutrition in the children of Fulani nomads in Northern Nigeria?. J Med Trop [serial online] 2013 [cited 2023 Mar 26];15:69-75. Available from: https://www.jmedtropics.org/text.asp?2013/15/2/69/123574 |
| Aims and Scope | |  |
The aim of this article are two-fold: (1) To draw attention to the possible contribution low levels of arachidonic acid (AA) and the very long-chain polyunsaturated fatty acid (LCPUFA) docosahexaenoic acid (DHA) may make to stunting and underweight in malnourished infants born to DHA-depleted mothers in land-locked regions of sub-Saharan Africa; and (2) to suggest ways to improve the DHA status of pregnant and lactating women, their children, and other vulnerable members of these at-risk communities, such as the elderly and victims of trauma (e.g., burns, motor-vehicle accidents) and people with infection.
| Background | | |
In developing countries, especially those located in sub-Saharan Africa and South Asia, malnutrition is a leading cause of death in children under 5 years of age, accounting for more than half of the 10.9 million childhood deaths worldwide. [1],[2] In sub-Saharan Africa mortality in children under 5 years of age has several causes: Acute respiratory infections, malaria, diarrhea and malnutrition. [3],[4] In addition, inappropriate breast-feeding practices contribute strongly to the high mortality rate in under 5-year olds [5] and these include: Failure to exclusively breast feed during the first 4 months of life; [3] early introduction of weaning foods; [6] use of nutritionally inadequate weaning foods; and microbial contamination of foods.
Malnutrition early in life can have detrimental life-long consequences; after age 2 years, one is unlikely to compensate for the deficits (e.g., intelligence, bone health) accrued during the first 2 years. Furthermore, many experts who have studied malnutrition in infants and children on a global basis believe that pregnancy through the first 24 months of life represent the critical window for improving child nutrition. [7] However, the opportunity for nutritional interventions after 2 years of age to prevent or reverse stunting should not be underestimated.
Historically, research into the nutritional causes and consequences of malnutrition has progressed through several phases. In the initial phase, initiated largely by the groundbreaking work of Dr. Cicely Williams in Ghana in the 1930s, research on malnutrition in developing countries focused mainly on deficiencies of calories (kwashiorkor) or both protein and calories (marasmus) as the primary causes of malnutrition. The second phase extended investigations into the role particular micronutrients such as iron, iodine and zinc [8],[9],[10],[11] and the B vitamins, folate and vitamin B12 in particular, play in malnutrition. [11],[12],[13]
More recently, appreciating the need to move beyond protein-calorie deficits and micronutrient deficiencies, nutritionists are now focusing their attention on other dietary factors such as choline, carnitine and the LCPUFA whose contributions to global malnutrition and infant mortality remain to be determined. Recent research points to the importance of AA and the very long-chain ω-3 fatty acids, eicosapentaenoic acid (EPA) and DHA in normal physical growth and neurologic development in the early years of life. [8],[14],[15],[16],[17],[18],[19],[20] However, it is important to keep in mind that macronutrient and micronutrient deficiencies may coexist, thereby implying that multiple nutrient interventions may be required to correct the malnutrition.
Moreover, the contribution of various political, economic and environmental factors to malnutrition in both urban and rural areas of developing countries cannot be overlooked. [1],[13] These include: Poverty; food insecurity (bad weather, too little rain, too much rain, poor soil, lack of fertilizer); ignorance of good feeding practices fueled by adult illiteracy and early marriage; lack of access to safe, clean water; poor sanitation; inappropriate complementary feeding; lack of appropriate breastfeeding (e.g., absence or premature cessation of breastfeeding); poor maternal nutrition resulting in intrauterine growth retardation; lack of essential health services (including immunizations); excessive number of children under five years of age; and gastrointestinal and respiratory infections.
| The Nutritional Importance of LCPUFAs, DHA in Particular, to Infant Growth and Development | | |
The long-chain LCPUFAs AA (20:4n-6), EPA (20:5n-3) and DHA (22:6n-3) play critical roles in infant growth, development and immune function. AA and DHA in particular are the most abundant LCPUFA in neural tissues, including the brain and retina. [21],[22],[23],[24],[25],[26] The neonate accumulates large amounts of AA and DHA in synaptosome cell membranes and the cerebral cortex, [27] especially during the third trimester and the first 6 months of life. An adverse maternal fatty acid status early in pregnancy is associated with reduced fetal growth. [28] DHA, as a constituent of membrane phospholipids, also plays critical roles in a variety of other membrane functions (e.g., hormone and ligand binding to the plasma membrane of cells, signal transduction, solute transport, ion channels), protection against oxidative damage [29] and regulation of neurotransmitter metabolism and gene expression. [30]
An expanding body of clinical evidence indicates that DHA enhances neurocognitive development of human infants and is critical for normal growth and neurodevelopment, certainly through the first 12 months of life [15],[16],[17],[27],[29],[31],[32],[33],[34] and perhaps extending into adolescence as well. [14] DHA may also be important in maintaining cognitive function during middle adulthood. [35] Although newborn infants are capable of metabolizing AA and DHA from linoleic acid and α-linolenic acid, respectively, this capacity is thought to be inadequate to meet the demands of the developing tissues. [36],[37],[38]
| Determinants of the Docosahexaenoic Acid Content of Human Milk | | |
Although in many parts of the world breast milk is the major source of DHA for infants during the first 6 months or more of life, the proportion of DHA in human milk fat is highly variable [39],[40],[41],[42] ranging from a low of 0.05-0.10% in women whose diets do not habitually include seafood, free-range hens eggs or other foods or supplements that provide relatively large amounts of DHA, [43] to proportions exceeding 1.0% in women who consume salmon, tuna or other ocean fish one or more times per week. [18],[39] The DHA percentage for the milk fat of most women in most of Europe, Canada and the US is in the range 0.2-0.4%. In contrast, relative to DHA, the AA content of human milk is much more constant, tending towards an average value of 0.4-0.5% of total fatty acids. [40],[44],[45],[46] Such relative constancy in the proportion of AA in breast milk reflects resistance to changes in maternal intake of AA and its precursor, namely the ω-6 fatty acid, linoleic acid. [40] For that reason, the remainder of this review will focus on DHA.
The DHA content of the milk triglycerides a woman produces is strongly and positively correlated with the amount of DHA she consumes. [32] For example, a woman who consumes 81 mg of DHA per day will secrete a milk fat that contains 0.2% DHA compared with another who consumes 131 mg of DHA and whose milk fat contains 0.32% DHA. Jensen et al.[47] showed that the breast milk of mothers who received 200 mg/day of algal DHA supplement contained 0.35% DHA versus 0.20% DHA in the placebo group.
In a study we conducted in 2008 of the diets and milk of breastfeeding Hispanic and non-Hispanic white women in New Mexico, [48] their mean DHA intake was only 47 mg and DHA accounted for just 0.11% of the fatty acids in their milk fat. Bergmann et al.[49] estimated that an intake of 200 mg/day of DHA from mid-pregnancy through lactation would be sufficient to support normal neurodevelopment. A workshop sponsored by the U.S. National Institutes of Health and International Society of Fatty Acids and Lipids recommended an intake of 300 mg/day of DHA for pregnant and nursing women in the United States. [50]
Based on our knowledge of the components of the typical diets of urban dwellers and rural Fulani in northern Nigeria, it is highly unlikely that the intake of nursing infants, children or adults in either of these environments is anything close to these amounts of DHA.
| Fatty Acid Composition of the Milk Fat of Fulani Women | | |
For the past 30 years, together with collaborators in the US and Nigeria, the authors have conducted studies centered on maternal/child health in sub-Saharan Africa. In 2006 we reported the results of our analysis of the fatty acid composition of the milk fat of 41 Fulani women living a pastoral lifestyle in northern Nigeria. [51] We found that DHA accounted for 0.22% of the fatty acid total, a value which is below the 0.30-0.40% range recommended by most expert panels. [45] In an ongoing study of pregnant women and their newborns in New Mexico, [52] we found that even though the DHA status of most of the pregnant women in our study was grossly sub-optimal (as determined by fatty acid analysis of maternal serum phospholipids), the DHA status of their newborns was normal relative to well-nourished, healthy infants and children elsewhere in the world. This observation agrees with that of other investigators who argue that during pregnancy a fetus will extract from its mother's circulation all of the DHA it requires for normal growth and development in utero. However, one should be cautious and not conclude that an infant born to a DHA-depleted mother will have DHA stores sufficient to sustain its own normal growth during the first few months of life. Studies are needed to test these hypotheses. Of course, one should keep in mind that zinc deficiency can contribute to stunting [53] and that zinc is required by enzymes in the pathway that converts α-linolenic acid into DHA in humans. [54]
| Malnutrition in Fulani Infants Under 2 Years of Age in Nigeria | | |
Although numerous studies have examined the effect of maternal nutritional status on fetal development and infant birth weight, the literature contains few reports about the relationship between the nutritional status of lactating women and the growth of their infants who have been continuously breastfed for the first 2 years of life. Our interest in this question was motivated by the results of previous studies we conducted of the fatty acid content and composition of the milk of Fulani women in Nigeria. [55],[56] From those studies we learned that the milk of Fulani women and women living in the city of Jos contained levels of the essential ω-3 fatty acid α-linolenic and the nutritionally critical ω-3 LCPUFA DHA that were below the levels recommended by expert international panels. In light of this knowledge, we hypothesized that the Nigerian infants who had been breastfed continuously, but not exclusively, for 2 years would show signs of malnutrition, as evidenced by reductions in height, weight and head circumference relative to World Health Organization (WHO) standards.
Three widely accepted approaches to assessing the nutritional status of infants and young children in developing countries include the anthropometric parameters of height (length), weight and head circumference and the calculation of a Z-score for each of these parameters. Z-scores are calculated by subtracting the median length, weight or head circumference of the reference population at a particular age from that of the infant, and dividing that difference by the standard deviation of the reference population of the same age.
In 2009, we published the results of a cross-sectional study of the growth characteristics of infants from birth to 2 years of age who were born to urban or rural women in and around the city of Jos. [57] Jos is located on Nigeria's fertile plateau which is situated in the north-central part of the country. A total of 100 mother/baby pairs participated in the study: They were divided nearly equally between urban dwellers representing different ethnic groups and Fulani living in three settlements located 25-40 km northeast of Jos.
We compared these three growth parameters to WHO standards using Z-scores for these three parameters. When the data for the urban and rural infants were pooled, 26% of the 2-year-old infants were stunted and 17% were underweight. When we plotted the various Z-scores versus infant age, two generalizations stood out. First, when we extrapolated the statistically-generated, best-fit lines back to the time of birth, the lines for each of the three growth parameters - height, weight and head circumference - all intersected the ordinate at or above a Z-score of zero. These results indicated that at birth, the mean height, weight and head circumference of the Nigerian infants were coincident with the mean values of the corresponding WHO standards. We therefore concluded that, on average, the infants in our study had not experienced significant growth retardation in utero. Second, the negative slopes in all three of these plots indicated that during the first 2 years of life the nutritional status of the infants markedly and progressively deteriorated. In other words, faltering of growth in the Nigerian children appears to start immediately after birth and progresses throughout the first 2 years of life, which is unusual since in the absence of suboptimal complementary feeding growth faltering usually begins at 6 months.
When the data for the infants were separated based on whether they and their mothers lived in the city of Jos or in a rural area, large differences were observed in the nutritional status of the two groups of infants. Noteworthy was the fact that whereas several dozen different ethnic groups were represented in the pool of urban subjects in our study, all of the mother-baby pairs in the rural areas were members of a pastoralist Fulani community. Although in terms of nutritional status the Z-scores of the urban infants and young children compared favorably to the WHO standards, at 2 years of age the length, weight and head circumference Z-scores for the Fulani infants fell in the negative range. We hypothesize, therefore, that at the time of birth the fatty acid composition of serum phospholipids of babies born to Fulani women will contain a proportion of DHA that is within the range of values that obtain for healthy newborns in developed countries. However, we predict that because the breast milk and the usual cereal-based complementary foods consumed by nursing Fulani infants represent a DHA-poor diet, these infants will not receive the amount of DHA required for optimum growth. These two hypotheses would account for the progressively declining Z-scores for the length, weight and head circumference of Fulani infants following their birth.
What might the cause be for the progressively worsening nutritional status of the Fulani infants following birth? While acknowledging that infections and the feeding of nutritionally inadequate cereal-based (e.g., millet, maize, guinea corn) weaning foods, may well have contributed to the malnutrition experienced by these infants during their first 2 years of life, we hypothesize that deficiencies in certain critical nutrients in the milk of the Fulani mothers who were breastfeeding continuously for at least 2 years also contributed significantly to their children's malnutrition. Through our own studies we learned that the milk of women in the city of Jos and that of Fulani women living in hamlets in rural areas was deficient in particular critical nutrients, including copper and zinc [58] and the fatty acids linoleic acid and DHA. [55],[59]
Furthermore, the results of other studies we conducted in northern Nigeria documented the fact that some of the locally-prepared weaning foods used in Jos and surrounding areas are deficient in DHA and several of the essential amino acids and trace minerals required for the optimum growth and development of young children. [60],[61]
| Growth of Nigerian Children Over the Age of 2 Years | | |
According to the WHO standards, [62],[63] over 38% of Nigerian children under 5 years of age are stunted and over 28% are underweight. Using these criteria, according to the results of a cross-sectional survey of the growth characteristics and body composition of 350 infants and children in rural hamlets of the semi-nomadic Fulani in northern Nigeria, we found that 20% of the subjects between the age of 1 and 16 years were stunted. [64] In contrast, Ekpo et al.[65] reported that 38.7% of "settled" Fulani children in southwestern Nigeria in the age range 6 months to 15 years were stunted.
The much larger risk of stunting in Fulani children whose families had presumably given up cattle-rearing and settled in towns, relative to children whose families were still living in rural areas and raising cattle, suggests that urbanization may have been detrimental to the linear growth of some of the children in our study. However, in both of these studies the prevalence of underweight in Fulani children was in the range of 10-14%, which is much lower than that of stunting. Thus, it seems that substandard nutrition in Fulani infants and young children compromises their height more than their weight. However, it is possible that Fulani families moved from rural areas and settled in towns because they experienced adverse conditions (e.g. drought, famine, violence, cattle diseases) that forced them to give up cattle rearing. Thus, since Ekpo et al. may have been studying a self-selected population that had experienced poor nutrition which adversely affected the growth of their children before the families had settled in an urban area, it may be that urbanization per se was not responsible for the childhood malnutrition.
| Dietary Sources of Docosahexaenoic Acid for Rural Fulani | | |
Plants in general, including the cereals such as maize, millet and sorghum, are the staple of the Fulani diet, but they do not contain AA or DHA. In fact, most plants have a relatively simple fatty acid composition consisting of only 8-10 fatty acids of which palmitic acid, stearic acid, oleic acid, linoleic acid and α-linolenic acid account for 90% or more of the fatty acid total. Although humans can metabolize some of the dietary-derived essential ω-3 fatty acid α-linolenic acid into DHA, it is widely believed that this capacity is limited and insufficient to satisfy the daily DHA needs of adults. [66],[67] Thus, humans depend on non-plant foods to provide them with the DHA they need to meet their daily DHA requirement.
Cow milk and the butter oil ("man shanu") Fulani produce by fermenting cow milk do not contain nutritionally significant amounts of DHA. [68] However, meats (e.g., beef, chicken) and seafood do contain nutritionally important amounts of DHA. Unfortunately, in most Fulani communities meat is expensive and beyond the economic reach of most of the population. As for seafood, since most Fulani pastoralists inhabit regions of Nigeria and West Africa in general that are far from the sea and because refrigerated transport is costly, DHA-rich seafood such as tuna and salmon is not a realistic option for the Fulani. We have shown that fresh-water fish in northern Nigeria do not contain nutritionally useful amounts of EPA or DHA. [69] On the other hand, eggs of free-range hens contain more DHA than commercial eggs and are widely available and relatively inexpensive throughout sub-Saharan Africa, including Fulani settlements. Furthermore, it would be highly unusual to find a Fulani household in a rural area where chickens are not raised. We have compared the fatty acid content and composition of free-range and "commercial", caged hens in Nigeria and found that the eggs of the former contain three-fold more DHA than the latter. [70]
| How Might the Docosahexaenoic Acid Content of the Diet of Fulani Pastoralists be Increased? | | |
The place to start is with the eggs of free-range eggs, even though, as stated above, such eggs contain only modest amounts of DHA. We recently analyzed the fatty acid composition and content of the yolks of eggs produced by free-range hens in a Fulani village in Bauchi State and Plateau State in northern Nigeria. We found that the egg yolks contained, on average, slightly more than 5 mg of DHA per gram fresh weight. Since the average weight of the egg yolks was 15 g, this means that one egg from a free-range hen contained about 75 g of DHA. Compared to the 200-400 mg of DHA nutrition experts in the US and Australia [50],[71],[72] recommend that a pregnant or lactating women should consume each day, this means that one egg per day from a free-range hen would satisfy 25-35% of this need if one considers 200 mg/day of DHA as an adequate amount of DHA for good health. Moreover, as few as two such eggs per day would satisfy at least half of the DHA requirement of pregnant or lactating women. According to these calculations, it seems free-range hens' eggs offer a partial, but significant and sustainable, solution to the DHA problem in Fulani communities. Nevertheless, other sources of DHA for humans should be sought.
We encourage local entrepreneurs in land-locked regions of Nigeria and other places in sub-Saharan Africa to investigate the possibility of using fish farms as a means of producing fish such as trout, salmon or catfish that contain useful amounts of DHA. Farm-raised catfish have less DHA and EPA compared their wild counterparts; however, some farm-raised salmon and trout contain about the same amounts of DHA and EPA as wild salmon and trout. [72] To accomplish this goal is certainly a formidable challenge, but one well worth undertaking. Perhaps the Nigerian government could be encouraged to provide funding for such research projects. One must keep in mind, however, that the fatty acid composition of farmed fish, especially with regard to the percentages of DHA and EPA, are highly dependent on the feed they receive.
Following this same line of reasoning, entrepreneurs in the private sector and officials in state and federal governments should invest in research aimed at developing algal sources of DHA. Algae are an excellent source of DHA and EPA. In addition, technology has advanced to the point where glycerol from biodiesel can be converted in high yield to DHA by the microalgae Schizochytrium limacinum. [73] No doubt, the creation of fish-farms and algae fermentation industries that might contribute to satisfying the DHA needs of populations in sub-Saharan Africa is a distant and fanciful dream at the moment. Until the dream is realized, these populations should be encouraged to increase their utilization of an economically-feasible and widely available source of DHA, namely the eggs of free-range hens. This worthwhile task could be promoted by political and academic leaders, public health officials and other health-care professionals.
Perhaps one day plant molecular biologists will devise means by which genes encoding the enzymes that metabolize α-linolenic acid into DHA can be introduced into traditional African plants such as the cereal staples millet, corn and sorghum. This would provide a long-term, sustainable solution to the problem of increasing the DHA content of populations in Africa and elsewhere who live far from marine sources of this critical fatty acid.
| Research Opportunities | | |
Infants in the first 2 years of life who are born into an impoverished environment merit special attention: They are likely to have minimal stores of micronutrients and a poor DHA status because of limitations in the nutritional quality of their intrauterine environment and mothers' milk, and nutrient deficiencies of local weaning foods. The time is ripe for a study of the effects of DHA-rich supplements on the health of pregnant and lactating Fulani women in Nigeria and the growth, development and general well-being of their infants and children, particularly during the 1 st months and early years of life. The main aim of such studies should be to determine the extent to which DHA supplements might blunt or prevent the stunting and wasting that affects so many of the youngest and most vulnerable individuals in this population of rural pastoralists. Furthermore, since complementary foods for malnourished and at-risk infants and children are available in certain regions of sub-Saharan Africa, including Nigeria, [60],[61] and other parts of the world, efforts to identify ways to increase the content of very long long-chain ω-3 fatty acids such as DHA in these foods should be a priority for future research in the region. However, one must keep in mind, as emphasized by Stein et al.[20] that since single nutrient interventions may not improve growth, future studies need to ensure that a comprehensive nutritional intervention involving a micronutrient supplement (e.g., iron, zinc, vitamin B12) accompanies any trial of DHA supplementation.
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