You are on page 1of 14

Special Article

Impact of fortied blended food aid products on nutritional status of infants and young children in developing countries
Ana B Prez-Expsito and Barbara P Klein
Fortied blended foods were developed in the 1960s to improve the nutritional status of children suering from malnutrition. The present review was conducted to examine the impact that fortied blended foods used in humanitarian relief programs have had on the health and nutritional status of infants and young children with moderate malnutrition, or at risk of undernutrition, in developing countries. Published articles were identied using electronic databases and general Web searches. Search terms included commodity types and names and terms related to food assistance and fortication programs. Positive eects on recovery from moderate acute malnutrition and weight gain were observed when fortied blended foods were distributed as dietary supplements. Prevention of severe micronutrient deciencies in populations reliant on food aid has been reported, but measurements of micronutrient status have rarely been conducted. Evidence of the ecacy of fortied blended foods for improving nutritional outcomes is currently limited and weak.
nure_255 706..718

2009 International Life Sciences Institute

INTRODUCTION Population growth, poverty, conicts, social exclusion, governance, trade policies, inequality, and natural disasters are some of the causes of food insecurity in the world.1 Fortied blended foods (FBFs) with high protein and micronutrient content, such as corn-soy milk (CSM) and wheat-soy blend (WSB), were developed in 1967 as part of a strategy from the United States to improve child nutrition. The strategy was to deliver a supplement to preschool children suering from moderate malnutrition through the United States Agency for International Development (USAID) P.L. 480 Title II food assistance program.24 FBFs have been since then distributed around the world by the USAID and other international agencies.The main donors to the World Food Program (WFP) in 2008 were the United States, Saudi Arabia, the European Commission, Canada, and Japan; approximately 41% of donations came from the United States and nearly 40% of them were in the form of food aid commodities, including FBFs.5

In the early 1980s, increasing costs and scarcity of non-fat dry milk (a main component of CSM) resulted in the development of corn-soy blend (CSB), which is now the most commonly used FBF.2 US commodity requirements are regulated by the United States Department of Agriculture (USDA), while locally produced variants of CSB and WSB are overseen by organizations such as the WFP and UNICEF.6,7 Since formulations and forticants vary among all products, the nutrient content and bioavailability of the products may also dier. Given that the main donor of FBFs is the United States and USAID is interested in improving these products, this review focuses mainly on US commodities, but other locally produced formulations are included as well. Ingredient breakdowns for the CSB and WSB FBFs produced in the United States are presented in Table 1. While food aid has doubtlessly saved millions of lives, few changes have been made to the nutritional composition of FBFs in the last decade. In 1988, vitamin A

Aliations: AB Prez-Expsito is with the Program in International and Community Nutrition, Department of Nutrition, University of California, Davis, Davis, California, USA. BP Klein is with the Department of Food Science and Human Nutrition, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA. Correspondence: AB Prez-Expsito, Program in International and Community Nutrition, Department of Nutrition, University of California, Davis, One Shields Ave, Davis, CA 95616, USA. E-mail: abperezexposito@ucdavis.edu, Phone: +1-530-574-7104, Fax: +1530 7523406. Key words: corn-soy blend, food aid, fortied blended foods, malnutrition, supplementary feeding
doi:10.1111/j.1753-4887.2009.00255.x Nutrition Reviews Vol. 67(12):706718

706

Table 1 Typical components of fortied blended foods distributed by USDA/USAID. Ingredient Corn-soy blend (%) Wheat-soy blend (%) Cornmeal, processed 69.9 Soy our, defatted, toasted 21.8 20.0 Straight grade wheat our* 37.9 Wheat protein concentrate* 35.0 Soybean oil 5.5 4.0 Vitamin antioxidant premix 0.1 0.1 3.0 3.0 Mineral premix
* Bulgur our (52.9%) and wheat protein concentrate (20%) may be substituted. Mineral premixes are dened in commodity specications for CSB and WSB issued by USDA (2008).36

levels in FBFs were increased by a factor of two. In 1998, magnesium was added, zinc levels were increased, and vitamin B12 was decreased, but no systematic approach has evolved to develop products suited to the nutritional needs of vulnerable populations.2 The current calculated nutrient content of FBFs produced in the United States is presented in Table 2. FBFs have come to be used as one-size-ts-all products for a wide array of vulnerable groups, including infants and young children, pregnant and lactating women, people living with HIV/AIDS, and populations reliant exclusively on food aid. Although FBFs have been used in food aid programs for a long time, eorts to evaluate their eectiveness have not been rigorous. Relatively little research has been conducted to test their ecacy in improving nutritional outcomes, in part because of technical diculties in collecting data, but also because of dierences among programs.8 FBFs are frequently distributed through supplementary feeding programs. In 1982, an extensive review was conducted of available reports from supplementary feeding programs for young children in developing countries; the results indicated the programs had no consistent impact on improving the nutritional status of young children.9 However, data obtained from these programs is dicult to interpret due to the variety of interventions included in dierent programs, variable program performance, as well as the lack of information on selection criteria, target population, type of food-aid product, frequency and duration of distribution, amounts, preparations, and source of provision (e.g., WFP, USAID, local production, etc.) variables that are not reported in the review mentioned above.10 Several of the programs reviewed in 1982 included FBFs, but the evaluation was not able to separate the independent eect of FBFs on nutritional status from the eects of other program interventions. Therefore, inferences about these results must be assessed carefully and cannot be used to evaluate the eectiveness of FBFs to overcome malnutrition in vulnerable groups.
Nutrition Reviews Vol. 67(12):706718

Various strategies have been developed to improve the nutritional status and health of vulnerable populations; however, their eectiveness in improving nutritional outcomes has not always been clearly established.11 Assessing the ecacy and eectiveness of ongoing interventions designed to mitigate the adverse eects of malnutrition in beneciary populations is the rst stage for their modication and improvement. The purpose of the present review is to present an evaluation of published research on the ecacy and eectiveness of the FBFs used in humanitarian relief programs to improve the health and nutritional status of infants and young children with moderate malnutrition, or at risk of undernutrition, in developing countries. IDENTIFICATION OF STUDIES Articles included in this review were identied using PubMed and the Cochrane Library with no restrictions regarding date, age, or language. The search terms used included commodity types and names and terms related to food assistance and fortication programs. Additional references and materials were obtained from Google, ocial Web sites of international agencies and nongovernmental organizations (NGOs), bibliographies of published documents, and personal contacts with experts, international agencies, and NGOs. In addition to articles published in peer-reviewed journals, the present review includes non-peer-reviewed articles and program evaluation and eld reports. Since FBFs were designed to overcome moderate malnutrition in infants and young children, studies involving severely malnourished populations or adults were not included. The treatment of severe malnutrition, as well as the impact of other foodaid products, such as lipid-based spreads or micronutrient powders, has been addressed in studies specic to those populations. Studies that did not describe the food provided and studies/evaluations in which the nutritional status and health-related outcomes were not assessed or not clearly described were excluded from this review.
707

Table 2 Calculated nutrient composition of USDA corn-soy blend (CSB) and wheat-soy blend (WSB) per 100 g dry product. Ingredient Unit of measure CSB WSB Nutrient Water g 9.4 8.8 Energy kcal 377.0 349.0 Protein g 15.3 20.5 Total lipid (fat) g 7.0 5.9 Ash g 1.7 3.1 Carbohydrate, by g 63.4 58.5 dierence Fiber, total dietary g 6.6 13.2 Mineral Calcium mg 830.0 864.0 Iron mg 17.9 20.9 Magnesium mg 170.6 296.0 Phosphorus mg 620.0 849.0 Potassium mg 627.0 874.0 Sodium mg 330.0 333.0 Zinc mg 5.6 8.2 Copper mg 0.9 1.3 Manganese mg 0.8 4.6 Selenium mcg 8.4 2.0 Iodine mcg 56.9 57.0 Vitamin Vitamin C mg 40.1 40.1 Thiamine mg 0.5 0.9 Riboavin mg 0.5 0.5 Niacin mg 6.2 7.9 Niacin equivalent mg 4.2 4.7 Pantothenic acid mg 3.1 3.2 Pyridoxine mg 0.4 0.2 Folate mcg 286.0 216.0 mcg 1.3 1.3 Vitamin B12 Vitamin A IU 2472.0 2318.0 Vitamin A mcg RE 779.0 771.0 Vitamin E mg TE 5.6 13.1 Vitamin K mcg 2.3 25.2 Vitamin D mcg 5.0 5.0
Data from SUSTAIN: Values calculated from ingredient composition in USDA Nutrient Data Bank and may dier slightly from USAID Commodity Reference Guides for CSB and WSB. Values represent premix levels plus intrinsic levels present in cereal-soy blends.

Randomized controlled trials (RCTs) are considered the gold standard for evaluating interventions, but due to ethical and feasibility considerations, the impact of nutrition and public health interventions are sometimes dicult to assess using this approach.12 Evaluating the ecacy and eectiveness of these interventions based only on RCTs could bias the evidence towards interventions that are more feasible but not necessarily more eective than interventions evaluated less rigorously.13 Observational quantitative epidemiological designs can complement the information obtained in RCTs by evaluating factors the latter cannot address.12 To provide a broader spectrum of information, randomized and non-randomized experimental designs, quasi-experimental designs with dierent comparison groups, cohort studies, and relevant observa708

tions from program and eld reports were included in the present review. The limitations of such studies that could potentially bias the results are assessed and discussed. Studies comparing multiple interventions were classied by type according to the criteria previously described by Victora et al.13 based on units of treatment (individuals or clusters), mechanism of delivery, and recipient compliance with the intervention. Observational studies were classied using standard epidemiological classications. DESCRIPTION OF STUDIES REVIEWED A total of 11 published studies and reports assessing either the ecacy or eectiveness of FBFs to improve the
Nutrition Reviews Vol. 67(12):706718

Table 3 Number and source of studies and reports reviewed. Source Research studies published in peer reviewed journals PubMed / Cochrane 6 Google / ocial websites References from published documents 1 Personal contacts 1 Total 8 health and nutritional status of infants and young children with moderate malnutrition, or at risk of undernutrition, in developing countries were included in this review. Specic sources and types of documents retrieved are described in Table 3 and a summary of the studies reviewed is presented in Table 4. Almost half of the studies were observational studies with no control group. Infants and young children receiving supplementary food in the form of WSB or CSB were included as a control or a comparison group in 6 of 11 studies of infants and young children; this prevented us from calculating eect sizes and statistically assessing the magnitude of the eect FBFs might have on nutritional status. Nevertheless, certain outcome measurements in the groups receiving FBFs were used to evaluate their eect. Recovery from moderate acute malnutrition (wasting) Recovery from moderate acute malnutrition, dened as weight-for-height z score (WHZ) > -2 or height-forheight > 85% of the median + no edema has been used as an indicator of program success in many supplementary feeding interventions. Five of the reviewed studies evaluated recovery from moderate acute malnutrition as an outcome measurement of the intervention; they followed children with moderate acute malnutrition until recovery or the end of the intervention.1416 In a group of studies conducted by Vautier et al.14 in three dierent countries (Liberia, Burundi, and Goma), CSB was distributed as a supplement in a large-scale, dry, take-home supplementary feeding program for moderately malnourished children and their families. Children with moderate acute malnutrition (weight-for-height 80% of the median, no edema, and height of 110 cm in Burundi and 130 cm in Liberia and Goma) received a monthly ration of supplementary food including oil, sugar, and CSB (2100 g in Liberia and 1600 g in Burundi and Goma); the food was distributed through supplementary feeding centers for 8 months in Liberia and 6 months in Burundi and Goma. The calories provided in the monthly rations diered by country. The intervention also included supportive family rations and other health-related interventions. A total of 40,223 children were included in all three countries. Children were followed until recovery from
Nutrition Reviews Vol. 67(12):706718

Program evaluation reports 1 1

Field reports 1 1 2

moderate acute malnutrition or the end of the program. Program coverage in Burundi was very low (29%), while in Liberia it was 70% and in Goma it was 93.7%. The overall recovery from malnutrition (weight-forheight > 85% of the median without edema for 2 consecutive weeks) was 77%, while the country-specic proportions were 81.3% in Liberia, 79% in Goma, and 66.8% in Burundi. Length of stay in the program before recovering was 50 days in Liberia and Goma, and 70 days in Burundi. The extent to which these changes in nutritional status were sustained over time was not reported. Two studies conducted in Malawi used a comparison group receiving fortied CSB to assess the ecacy and eectiveness of RUF (ready-to-use food) on the nutritional status of moderate acute malnourished children by measuring recovery rates.15,16 Two main formulations of these products were compared to CSB: ready-to-use therapeutic food (RUTF) and ready-to-use fortied spreads (RUFS). (The development of dierent products and formulations of ready-to-use food has led to an array of names and acronyms. For the purpose of this review, the names and acronyms from the original papers were used.) Both of the products evaluated have similar characteristics; the main dierence between them is the energy and nutrient density of the product. RUTFs were designed for use as the only food in the nutritional rehabilitation of severely malnourished children, covering all the nutrition requirements to overcome severe malnutrition. RUFS were developed as supplements to complement habitual diets for the management of moderate malnutrition and the prevention of undernutrition in at-risk populations.17 The rst study conducted by Patel et al.15 in a rural area of Malawi provided monthly supplementary feeding with either 7 kg of RUTF or 50 kg of fortied CSB to children aged 1060 months who were at risk of malnutrition (weight-for-height > 80% of the median but <85%). CSB was produced locally according to WFP specications. Mothers were asked to feed their children seven times a day and to prepare CSB in the same manner as Nsima, the regions traditional dough made of corn our. Compliance with these instructions and intakes of supplementary food were not measured for any of the interventions. In total, 372 children were included (RUTF = 331; CSB = 41). Prospective allocation of either
709

710

Table 4 Summary of reviewed studies of fortied blended foods. Author Study type*/Sample size Setting and participants Public health regimen Malawi; children Galpin et al. (2007)21 ecacy (n = 41) 5.506.49 mo; WHZ > -2, no edema Intervention 25 g/d RUFS or 50 g/d RUFS or 72 g/d CSB. Duration 1 month Malawi; children 52 mo; WAZ < -2 SD, HAZ < -2 SD 92 g/d RUFS or140 g/d maize/soy our (not fortied). Health education, illnesses treatment. 12 weeks (food provided) + 12 weeks post-suppl (no food)

Maleta et al. (2004)20

Public health delivery ecacy (n = 61)

Matilsky et al. (2008)16 8 weeks or recovery

Public health delivery ecacy (n = 1810) 2 months

Menon et al. (2007)24

Public health delivery ecacy (S-WSB/n = 254; WSB/n = 161)

Malawi; children 660 mo; -3 WHZ < -2 Haiti;children 924 mo; Hb > 70 g/L

Main results Weight increment in all three groups. No dierence among groups. No breast milk displacement. RUFS higher weight-for-height gain. No eect on other growth outcomes. Maize/soy fortied our gained weight despite no increment in energy intake. RUFS higher energy, iron, and zinc intake. CSB recovery = 72%; RUFS recovery = 80%. Higher weight gain and MUAC in milk-RUFS. Hb increased in S-WSB and declined in WSB. Anemia prevalence in S-WSB reduced (52.3 to 28.3%).

Patel et al. (2005)15 Malawi; children 1060 mo; >80%WHM < 85% Malawi; children 5.56.99 mo; adequate weight-for-length

Public health delivery ecacy (n = 372)

CSB or milk-RUFS or soyRUFS; 75 kcal/kg body wt/d. 8 kg/mo S-WSB oil + 1 sprinkles sachet or 8 kg/mo WSB + oil. Household ration; health education; preventive services; home visits. 7 kg/mo RUTF or 50 kg/mo CSB (WFP). 8 weeks

Phuka et al. (2008, 2009)22,23

Public health delivery ecacy (n = 168; follow-up n = 149)

71 g/d fortied maize/ soy our or 25 g/d RUFS or 50 g/d RUFS.

1 year; 2 year follow-up; (no food intervention)

Nutrition Reviews Vol. 67(12):706718

Ruel et al. (2008)18

Public health program eectiveness (n = 1481)

Haiti. Preventive: all children 623 mo and children 2459 mo WAZ < -3. Recuperative: children 659 mo WAZ < -2

8 kg/mo WSB + oil. General ration; health education; growth monitoring; parasites treatment; immunizations; vitamin A supplement; ORS provision; home visits.

Preventive:18 months for 623 mo; 9 months for 2459 mos. Recuperative: 9 months

CSB recovery = 73%; RUTF recovery = 86%; RUTF higher rate gain for weight, height, and MUAC. No dierence in weight, length, MUAC, WAZ, WHZ, and HAZ. Severe stunting less frequent in RUFS groups. Cumulative incidence of severe stunting after 3 y higher in maize/our. No dierence in Hb or ferritin. Nutritional status deteriorated in all groups but more in the 25 g RUFS. Preventive more eective to reduce undernutrition. Both delivery methods might have mitigated the eect of political, economic, and climatic crisis on undernutrition.

Stevens et al. (2001)26 Field report Kenya; children under 5 y and pregnant and lactating women CSB or maize and pulses (2015 kcal/d). N/A

Nutrition Reviews Vol. 67(12):706718

Swindale et al. (2004)19 Program evaluation (n = 29) Programs in Africa, Asia, and Latin America; children < 2 y Title II MCHN. No description of specic food. N/A

Upadhyay et al. (1999)27 and Blanck et al. (2002)28 Field report Bhutanese refugees in Nepal; general population in refugee camp General food ration (rice, lentils, oil, salt, sugar, and fresh vegetables) + 40 g FBF/d rice; nutrition education; change from polished rice to parboiled.

September, 1993January, 1999

Vautier et al. (1999)14 Cohort study (Liberia/ n = 12,259 Goma/ n = 18,723 Burundi/ n = 9,241) Liberia; Goma; Burundi. Children: WHM 80%; height 130 cm ( 110 cm in Burundi)

Liberia (2100 g/mo CSB +oil+sugar); Goma (1600 g/mo CSB+oil+sugar+milled biscuit); Burundi (1600 g/mo CSB +oil+sugar) Family rations (Liberia/ Burundi); General food (Goma); Immunizations (Liberia/Goma); Medical Care; Feeding sessions

8 months or recovery

Scurvy cases before intervention. Scurvy cases decreased after diet improvement and CSB supplementation. Underweight reduced by 1.9 percentage points per year. Stunting reduced by 2.4 percentage points per year. Cases of scurvy, beriberi, and pellagra before FBF. Decline in incidence of scurvy, beriberi, and elimination of pellagra after the introduction of FBF. Increase in cases of angular stomatitis after withdrawal of FBF. Liberia (coverage = 69.9%; recovery = 81.3 %; length of stay = 50 d); Goma (coverage = 93.7%; recovery = 79 %; length of stay = 50 d); Burundi (coverage = 29.6%; recovery = 66.8 %; length of stay = 70 d).

Abbreviations: CSB, corn-soy blend; FBF, fortied blended food; HAZ, height-for-age z score; Hb, hemoglobin; MCHN, Maternal and Child Health and Nutrition; MUAC, middle upper arm circumference; ORS, oral rehydration salts; RUFS, ready-to-use fortied spreads; RUTF, ready-to-use therapeutic food; S-WSB, sprinkles added to WSB; WAZ, weight-for-age z score; WHM, weight-for height median; WHZ, weight-for-height z score; WSB, wheat-soy blend. * Studies were classied according to Victora et al. (2004).13

711

the RUTF or the CSB supplements was conducted using a stepped-wedge design with no randomization. No dierences were reported in the baseline characteristics of the groups. After 8 weeks of intervention, 73% of the children in the CSB group had weight-for-height 85% of the median. The proportion of children above this cuto point in the RUTF group was higher (86%). Statistical signicance of this dierence was not reported. Sixty-one percent of the children who received RUTF were measured 6 months after the intervention, but no follow-up measurements were carried out for the children who received CSB during the intervention. In the second study conducted in Malawi, supplementary feeding with 75 kcal/kg body weight/day provided through either milk-peanut RUFS, soy-peanut RUFS, or locally produced fortied CSB was delivered to moderately acute malnourished children aged 660 months (-3 WHZ < -2) for 8 weeks or recovery.16 A total of 1810 children were included in the intervention and evenly distributed among groups. Caretakers were instructed on how much product to feed the children and specic messages about not sharing food and using supplements as medical treatment were emphasized. No information about actual preparation of CSB in the household or compliance was collected. Recovery, dened as WHZ > -2, was 72% in the CSB group and 80% in both RUFS groups (P = 0.016). Growth None of the reviewed studies was specically designed to assess the eects of FBFs on childrens growth. The results presented were derived either from studies using a CSB-supplemented group as a comparison group or measurements before and after the program intervention in which no comparison population was included. None of the studies provided guidance regarding the quantity and preparation of the CSB to be consumed. In some of the studies in which ready-to-use food was used as a supplement, compliance was monitored and/or instructions on usage were given. The study of Ruel et al.18 is an exception; those results were compared to data from a national survey in Haiti and the behavioral change component might have addressed instructions on the use of WSB. Inferences and generalizations about the results reported in the reviewed studies should take these limitations into account. A USAID evaluation of Title II MCHN programs reported that, after its implementation in several countries in Africa, Asia, and Latin America, underweight and stunting in children younger than 2 years were reduced on average by 1.9% and 2.4% per year, respectively.19 Title II MCHN programs include distribution of FBFs to beneciaries along with other interventions, such as preven712

tive care and nutrition education. Each of the programs has its own implementation that determines the type and amount of food provided. Details about the specic characteristics of each program are not usually provided in these evaluations and they might aect comparability with other studies. A study carried out in Haiti assessed two dierent targeting strategies (preventive and recuperative models) for delivering a large-scale MCHN program.18 The intervention included a monthly provision of fortied WSB (8 kg) and 2.5 kg of oil among other program interventions. Results showed that targeting malnourished children aged 2459 months and all children aged 623 months (preventive model) signicantly reduced the prevalence of stunting (height-for age Z score < -2), underweight (weight-for-age Z score < -2), and wasting (weight-for-height Z score < -2) by 4%, 6%, and 4%, respectively, in comparison to the recuperative model that only targeted underweight children aged 659 months. The results suggest that both delivery methods mitigated the eect of political, economic, and climatic crisis on childhood undernutrition based on comparison data from a national survey conducted during the study period. The authors inferred that the eect of each delivery method on overcoming undernutrition in the study population was in addition to the eect of MCHN programs reported by Swindale et al.19 None of the studies were designed to evaluate the individual eect of each program component on the recipients nutritional status. In the study by Patel et al.15 described in the previous section, higher weight, height, and middle-upper-arm circumference (MUAC) gains were reported in the children receiving RUTF than in the children receiving CSB as supplementary food. Weight gain after 8 weeks of supplementation was 3.1 2.7 g/kg/d in the RUTF group versus 1.4 2.5 g/kg/d in the CSB group (P = 0.0002), while height gain was 0.28 0.27 mm/d and 0.17 0.21 mm/d (P = 0.003), respectively. MUAC gain was 0.30 0.31 mm/d in the RUTF group versus 0.18 0.29 mm/d in the CSB group (P = 0.02). In a regression model, the type of supplement used was found to signicantly determine weight-for-height after the intervention (P = 0.001). Another study conducted by Matilsky et al.16 (described above) found that the type of supplement (soy/peanut-RUFS versus locally produced CSB) had a signicant eect on weight gain and MUAC gain. The actual weight and MUAC gains are not reported. After 8 weeks of supplementation, no eect on linear growth was observed in any of the treatment groups (n = 896). In contrast to the studies described above, three studies, also conducted in Malawi, did not nd statistically signicant dierences in growth when comparing ready-to-use food with CSB during the supplementation
Nutrition Reviews Vol. 67(12):706718

period; however, post-intervention measurements differed among groups in one study.2022 The rst study, conducted by Maleta et al.,20 supplemented underweight and stunted children aged 52 months with either 92 g of RUFS or 140 g of maize/soy our (Likuni Phala) for 12 weeks. The Likuni Phala provided during this study was not fortied with micronutrients. Empty sachets of RUFS were collected to monitor compliance, but no measurement of compliance or supplement preparation in the maize/soy our group was described. The intervention also included health education to caregivers and treatment of illnesses. Both groups showed an increase in weight during the supplementation period, with no signicant dierences among groups (n = 61). Children receiving maize/soy our showed an increase in weight without increasing energy intake, possibly due to the eect of the other interventions provided. No dierences in linear growth were observed in any group. Children were followed for 12 weeks after the supplementation period, during which time no food was provided. Children receiving RUFS during the intervention had higher weight scores than the ones receiving maize/soy fortied our (P = 0.01), presumably due to the sustained eect of micronutrient supplementation on improving appetite. Galpin et al.21 supplemented breastfed infants aged 5.56.5 months who had adequate WHZ scores with either 25 g of RUFS, 50 g of RUFS, or 72 g of CSB. Energy density was lower in the CSB group (1.1 kcal/g) than in both groups receiving fortied spreads (5.3 kcal/g). After 1 month of supplementation, weight increased signicantly in all three groups, with no signicant dierences among groups (n = 44). Compliance and amounts of supplements consumed were directly monitored by weekly home visits in the eld. In another study conducted by Phuka et al.,22 fortied maize/soy our (Likuni Phala) was provided to infants aged 5.56.99 months who had adequate weightfor-height scores. A total of 168 infants were randomly assigned to receive either 25 or 50 g of RUFS or 71 g Likuni Phala for 1 year. Empty containers were collected to measure compliance in the RUFS groups only. At the end of the study period, no dierences were observed among groups in the overall changes in weight, length, MUAC, weight-for-age, weight-for-length, or height-forlength. The proportion of infants developing severe and moderate-to-severe underweight or wasting was not different among groups but severe stunting occurred signicantly less frequently in the groups receiving RUFS than in the group receiving Likuni Phala (P = 0.008). Statistical analysis showed that the eect of the intervention depended on the infants initial length-for-age. For infants with initial length-for-age below the median, weight and height gains were signicantly higher in the
Nutrition Reviews Vol. 67(12):706718

group receiving 50 g RUFS than in the Likuni Phala group. The results of a 2-year follow-up of the Phuka study, in which childrens growth was assessed but no food was provided, were recently published.23 The cumulative incidence of severe stunting over the 3-year study period (1 year of supplementation and 2 years of follow-up) was 20% for the Likuni Phala group, 10% for the 25 g RUFS group, and 3.6% for the 50 g RUFS group (P = 0.03) (n = 149). The cumulative incidence of moderate-tosevere stunting was similar in the three groups. Weightfor-age Z scores (WAZ), height-for-age Z scores (HAZ), and weight-for-height Z scores (WHZ) decreased in all groups, indicating the nutritional status deteriorated over time in all groups when no additional food was provided. Children who received 25 g of RUFS showed greater deterioration in their nutritional status, as measured by WAZ, than children who received 50 g of RUFS (P = 0.04). The dierences were larger in children who were stunted at baseline (P = 0.01). Supplementation with 50 g of RUFS prevented the delay of linear growth velocity in infants, a nding that has been reported frequently in low-income settings. It is recognized that the lack of information on dietary intake during the post-supplementation period limits interpretation of the results. Micronutrient status Vitamin and mineral premixes are added to FBFs, when produced, but their impact on the nutritional status of vulnerable populations has not been studied frequently. In the study conducted by Maleta et al.,20 underweight children aged 52 months who received a ready-to-use food for 12 weeks had higher iron and zinc intake than children receiving 140 g of locally prepared, fortied maize/soy our (Likuni Phala). Hemoglobin (Hb) concentrations in children aged 924 months receiving WSB from the United States or powdered micronutrients in the form of SprinklesTM added to WSB (S-WSB) were compared in a study conducted in Haiti.24 Mothers were educated on the use of SprinklesTM, but it is not clear if information about the use of WSB was provided. After the intervention, mean Hb increased by 5.5 g/L in the S-WSB group (P < 0.001), while it declined by 1.0 g/L in the WSB group (P < 0.001). Anemia prevalence in children supplemented with S-WSB was reduced from 52% to 28% (P < 0.001), and the proportion of children who became anemic after the intervention was twice as large in the group consuming fortied WSB alone (29%) compared with the group which had SprinklesTM added to the blend (11%). In the study conducted by Phuka et al.22 in Malawi, no dierences in Hb or ferritin concentrations were reported when 618-month-old infants were
713

supplemented with either 25 or 50 g of RUFS or 71 g of fortied maize/soy our. Children in the maize/soy our group received 5 mg of iron per day, while the iron content in both the 25- and 50-g dose of RUFS was 8 mg. This study was primarily designed to assess growth and no sample size calculation was reported; thus, it is not possible to determine the adequacy of sample size for detecting small dierences in iron status among groups. Severe micronutrient deciencies in populations that rely exclusively on food aid have been reported in several studies.25 Two reports from the eld were included in this review.26,27 Stevens et al.26 reported cases of scurvy in a displaced population in Wajir, Kenya. This population was dependent on food aid for its survival, receiving a general food ration that included only maize and black tea for 5 months. Since the food provided did not contain vitamin C, clinical signs of scurvy started to appear in recipients of all genders and ages. Reported cases of scurvy decreased after improvements were made to the diet (addition of pulses and oil) and blanket supplementation with fortied CSB provided by the WFP was introduced to children <5 years of age and to pregnant and lactating women. It was observed that fortied CSB was shared in the household, thereby beneting all groups. The monthly food ration included CSB formulated at 185% (52 mg) of the recommended intake for vitamin C. (The RDA percentage is based on daily mean population requirements of 2100 kcal, 58 g protein, 0.9 mg thiamine, and 28 mg vitamin C as reported by WHO in 1997.) Weeks after the distribution of fortied CSB, biochemical analyses were conducted to determine what, if any, specic micronutrient deciencies were present. Unfortunately, the results of these biochemical tests were not reported, and since the symptoms observed are unspecic and concurrent micronutrient deciencies and other diseases might exist, the specic presence of vitamin C deciency is not clear. In another eld report from a camp receiving Bhutanese refugees, cases of scurvy (vitamin C deciency), beriberi (thiamine deciency), and pellagra (niacin deciency) were reported.27 After the addition of 40 g of FBF per capita to the general ration (rice, lentils, oil, salt, sugar, and fresh vegetables), the introduction of parboiled rice instead of polished rice, and the provision of nutrition education sessions, declines were observed in the incidence of scurvy and beriberi, and pellagra was eliminated. Cases of angular stomatitis (a clinical sign of micronutrient deciencies) were reported after FBF was withdrawn from the food ration due to program constraints.28 Specic groups within this population that presented symptoms of deciency or beneted from the intervention were not described.
714

Breast-milk intake Only one of the reviewed studies assessed breast-milk intake when CSB or RUFS was provided as complementary food for 1 month in infants aged 5.56.49 months.21 This ecacy study concluded that neither the introduction of fortied spreads nor 72 g/d of fortied CSB as complementary foods aected breast-milk intake in infants with WHZ > -2, no edema, and no severe illnesses. Breast-milk intake was directly measured using deuterated water.

ASSESSING THE AVAILABLE EVIDENCE FOR EFFICACY AND EFFECTIVENESS OF FBFS FOR VULNERABLE POPULATIONS The present review included 11 studies that used dierent approaches and designs to assess the impact that food-aid interventions providing FBFs had on the nutritional status of infants and young children with moderate malnutrition, or at risk of undernutrition, in developing countries. The studies were conducted in eight countries. In addition to the retrieved studies, a program evaluation report analyzing data from 29 dierent programs (Title II MCHN) implemented in Africa, Asia, and Latin America was reviewed. None of the studies in this review was specically designed to assess the eects of FBFs on childrens growth; therefore, comparison groups to evaluate the eect of FBFs on nutritional status were not established. On the contrary, the results presented here were all derived from studies in which a CSB-supplemented group was established as a comparison group or from measurements assessed before and after interventions in which there was no comparison group, with the exception of the study conducted in Haiti.18 This is a considerable limitation for the analysis of the published evidence, given that any observed eect could be inuenced by many other factors not related to the intervention; therefore, inferences and generalizations about the signicance of the results may not be possible. Recovery from moderate acute malnutrition (WHZ < -2) in the reviewed studies that included CSB as a supplementary food was 76%, on average. The minimum percentage reported was 66.8% and the maximum 93.7%. Unfortunately, the available evidence is insucient to draw a conclusion as to whether the observed eect on the nutritional status of moderately malnourished populations is due to the specic characteristics of FBFs or if the introduction of any type of food provided under such conditions would have had a similarly positive impact. Higher rates of recovery (average, 83%) were observed when using an RUTF or an RUSF as
Nutrition Reviews Vol. 67(12):706718

supplementary feeding for children with moderate acute malnutrition. A recent retrospective study of 82 emergency supplementary feeding programs providing FBFs, implemented by 15 organizations mainly in Africa and Asia from 2003 to 2005, found a 69% overall recovery rate from moderate acute malnutrition.10 Interestingly, this study observed that the presence of general rations in the program and the crisis duration each had a signicant impact on malnutrition recovery rates. In the case of the study conducted in Burundi, Liberia, and Goma, other interventions were provided, but the eect of environmental and social conditions was not evaluated; thus, those conditions could have inuenced the observed eect of FBFs on malnutrition recovery. Title II MCHN programs include supplementary feeding with FBFs among other health and educational interventions. The study conducted in Haiti by Ruel et al.,18 and an evaluation of 29 programs in dierent countries, reported important reductions in the prevalence of underweight, wasting, and stunting when FBFs were provided as part of a program, especially when the program was targeted to all children aged 623 months and not only the ones who were already moderately malnourished.19 The eect of each program component on the nutritional status of the children receiving aid cannot be separated from the overall impact. A series of studies, mainly conducted in Malawi, have been designed to evaluate the ecacy and eectiveness of dierent formulations of ready-to-use food on the growth of malnourished children or groups at risk of malnutrition. The results of these studies are not consistent. Signicant dierences in weight gain were found between either RUTF or RUFS and CSB in the study conducted by Matilsky et al.,16 while no dierences in weight gain were reported by Galpin et al.21 It is interesting to note that Maleta et al.20 and Phuka et al.23 found dierences in weight gain and WAZ, respectively, only in post-intervention measurements. This implies that ready-to-use food might be able to prevent underweight once the food supplement ceases to be provided, presumably due to an eect that the additional micronutrients in the diet has on childrens appetite and susceptibility to infections. This long-term eect of supplementation has not been observed using FBFs as a food intervention. Signicant dierences between RUFS and locally produced CSB on MUAC gain were only described in the studies conducted by Patel et al.15 and Matilsky et al.,16 and only the study by Patel et al. reported a signicant increase on linear growth in the group receiving RUFS versus locally produced CSB.15 Evaluating micronutrient status within the context of program evaluation or in emergency settings is rarely
Nutrition Reviews Vol. 67(12):706718

conducted because of logistical diculties, required technical expertise, and high cost. In Haiti, Menon et al.24 found a signicant reduction in the prevalence of anemia when micronutrient powders in the form of SprinklesTM were added to WSB; a reduction in Hb concentration was additionally observed in the children receiving WSB without SprinklesTM. In Malawi, Phuka et al.22 found no dierences in Hb or ferritin concentration after 618month-old infants received either 25 or 50 g of RUFS or 71 g of fortied maize/soy our as supplements. The extent to which eects on iron status in populations receiving FBFs will be observed will depend on iron bioavailability from the supplement. Iron absorption from an iron-fortied WSB (10 mg of iron as ferrous sulfate/100 g of WSB) has been reported to be as low as 1.15% (0.771.71). When ascorbic acid was added to the blend at a 1:5 iron-ascorbic acid ratio, absorption increased to 2.4% (1.613.58).29 The WSB tested in this particular study was fortied with ferrous sulfate, an iron salt used in fortication that is better absorbed and less stable in storage than ferrous fumarate. WSB is usually fortied with ferrous fumarate and iron absorption from WSB might, therefore, be lower in general. Taking these absorption gures and the iron content of the blend into account, WSB would only provide (in the best-case scenario) between approximately 4050% of the iron requirement for infants and young children. Therefore, the lack of eect of FBFs on iron status and increments in the prevalence of anemia in recipient populations is not surprising. Adding milk to the blend could potentially increase iron absorption by up to 6%, as shown in iron-absorption studies using CSM.30 The cost-eectiveness and feasibility of other strategies to improve mineral absorption, such as dephytinization to reduce the phytic acid content of FBFs, could be assessed as well.29 Reports from the eld noted a reduction in the clinical signs of vitamin C deciency after the inclusion of FBFs to a blanket supplementary feeding program in displaced and refugee populations fully dependent on food aid.26,27 It is not clear if micronutrient deciencies were conrmed by biochemical indicators and which population groups were aected or beneted from FBF supplementation. The fact that some symptoms of micronutrient deciencies were reported again after FBFs were withdrawn from the program suggests that FBFs may be preventing severe micronutrient deciencies in populations that rely on food aid for survival. The reported results might be biased due to lack of control groups and lack of data on other factors that could be aecting the nutritional status of these populations in conditions of social disruption and displacement. Given the low levels of vitamin C in FBFs and the high losses of the vitamin that occur during FBF preparation and storage, the pos715

sibility that FBFs could be preventing scurvy needs further investigation.31 The potential eect of other micronutrients included in FBF formulations to improve the nutritional status of vulnerable populations has not been assessed; further research is required to assess their adequacy in the current formulation. Galpin et al.21 evaluated breast milk intake in nonmalnourished infants between 5.5 and 6.5 months of age. No displacement of breast milk was observed when 72 g of CSB was introduced as a complementary food. This is important to consider when recommending that FBFs be introduced as complementary foods to nonmalnourished infants younger than 6.5 months who are still breastfeeding, since this is the age group in which the introduction of solid food is controversial and in which the potential to impact breast milk displacement is elevated. In a recent systematic review on complementary feeding, it was concluded that fortied complementary foods are able to impact the micronutrient status of children but they have little impact on childrens growth.32 Another meta-analysis on the eect of multiplemicronutrient interventions on health and development outcomes in micronutrient-decient populations showed that fortied foods had the largest eect on Hb concentrations compared to other forms of micronutrient delivery, but the eect on growth and motor development in children was weaker.33 According to the available evidence, micronutrient deciencies in vulnerable populations may not be suciently alleviated by FBFs as they are currently formulated. Although our review was mainly focused on FBFs from programs sponsored by the United States, other locally produced blends were also included; nevertheless, most of the reviewed studies did not report the source of the FBF used. Another limitation in the reviewed literature is that most of the studies did not provide information to recipients regarding the correct preparation or use of the food aid distributed, nor did they monitor consumption or compliance; this was particularly evident in the group receiving FBFs. Assessment of FBF eectiveness requires knowledge of the products preparation and other inputs from the nal consumer such as fuel and kitchen supplies, dilution of the product might occur, and intra-household sharing may take place. Moreover, FBFs are produced in dierent settings and in accordance with dierent regulations. For instance, the WFP and UNICEF guidelines do not include the dehulling or degermination steps included in the USAID requirements, mainly because of the associated cost. All of these factors could inuence energy and nutrient intake, the sensory characteristics of the supplement, and the nutrient bioavailability, which also aects the comparability of results among studies.
716

The causal relationship between food provision and nutritional status is very complex and depends on factors that are not strictly biological.34 The reviewed evidence on the ecacy and eectiveness of FBFs is not strong enough to establish a causal relationship between the distribution of FBFs as a food aid intervention and a positive impact on the nutritional status of infants and young children. CONCLUSION FBFs were introduced in the 1960s and, since then, have been part of a sustained strategy designed to alleviate food insecurity in vulnerable regions of the world. However, their impact on the nutritional status of populations has not been evaluated rigorously and, in almost 40 years, very little research has been conducted on them; this reects the fact that, over the years, food-aid programs have been mostly resource-driven rather than analysis-driven.35 Positive eects on weight gain and recovery from moderate acute malnutrition have been observed in populations receiving FBFs as food-aid supplements. Prevention of severe micronutrient deciencies in populations reliant on food aid has also been reported. But direct measurements of the micronutrient status of vulnerable populations receiving FBFs have rarely been conducted. Well-designed evaluations to test the ecacy and eectiveness of FBFs on linear growth and development are, likewise, lacking. Thus, since the available scientic evidence on the ecacy and eectiveness of FBFs for improving the nutritional status of vulnerable populations is very limited and weak, it is not currently possible to reach denite conclusions . The provision of FBFs worldwide is constrained by tight regulations that depend on national budgets, producers prots, and overall food production in the United States and other FBF-producing countries. Changes in the US food-aid strategy would aect all of these relationships and have an economic impact that could risk the provision of food aid at a global level. The inclusion of new strategies in humanitarian assistance programs that could potentially have a greater eect on the nutritional status of recipient populations needs to be evaluated; if sustainability is to be assured, the economic and social eects of such strategic changes, as well as the political commitment to them, need to be taken into account. Acknowledgments Funding and other assistance. This review was conducted in collaboration with SUSTAIN (Sharing Science and Technology to Aid in the Improvement of Nutrition: www.sustaintech.org) through a grant to SUSTAIN from
Nutrition Reviews Vol. 67(12):706718

the Bill & Melinda Gates Foundation for the Roundtable on Food Aid Product Optimization for Nutritional Outcomes held in October, 2008. The authors thank the SUSTAIN team for providing important information and editing support, especially Lisa Fleige, Elizabeth Turner, Alicia Greeneld, Cassandra Miller, Sara Schaefer, and Sue Wunder. Declaration of interest. AB Prez-Exposito has no relevant interests to declare. BP Klein is aliated with the Illinois Center for Soy Foods at the University of Illinois at Urbana-Champaign, which received funding from the Illinois Soybean Association.

15.

16.

17.

18.

REFERENCES
1. Ahmed A, Hill R, Smoth L, Wiesmann D, Frankenburger T. The World's Most Deprived: Characteristics and Causes of Extreme Poverty and Hunger. 20202 Discussion paper 43. Washington, DC: International Food Policy Research Institute; 2007. 2. Marchione TJ. Foods provided through U.S. government emergency food aid programs: policies and customs governing their formulation, selection and distribution. J Nutr. 2002;132(Suppl):S2104S2111. 3. Combs G. Development of a supplementary food mixture (CSM) for children. PAG Bull. 1967;7:1524. 4. Senti F. Guidelines for the nutrient composition of processed foods. Cereal Sci Today. 1972;17:157161. 5. World Food Program. Contributions to WFP in 2008. Available at: http://www.wfp.org/appeals/Wfp_donors/ index.asp?section=3&sub_section=4. Accessed 23 December 2008. 6. World Food Program. Specications for Corn Soy Blend (CSB). Available at: http://foodquality.wfp.org/ FoodSpecications/BlendedFoodsFortied/CSBWFP/tabid/ 139/Default.aspx. Accessed 30 December 2008. 7. UNICEF. UNIMIX Corn-soy Blend. Available at: http:// www.supply.unicef.dk/Catalogue/. Accessed 23 December 2008. To obtain details about the product, UNIMIX needs to be typed in the search engine. Select UNIMIX (CSB). 8. Austin J. Nutrition Programs in the Third World. Cambridge: Oelgeschlager, Gun and Ham Publishers, Inc.; 1981. 9. Beaton GH, Ghassemi H. Supplementary feeding programs for young children in developing countries. Am J Clin Nutr. 1982;35:863916. 10. Navarro-Colorado C. A retrospective study of emergency supplementary feeding programmes. ENN and Save the Children. June 2007. Available at: http://www.ennonline.net/ pool / les / research / Retrospective_Study_of_Emergency_ Supplementary_Feeding_Programmes_June%202007.pdf. 11. Bhutta ZA, Ahmed T, Black RE, et al. What works? Interventions for maternal and child undernutrition and survival. Lancet. 2008;371:417440. 12. Black N. Why we need observational studies to evaluate the eectiveness of health care. BMJ. 1996;312:12151218. 13. Victora CG, Habicht JP, Bryce J. Evidence-based public health: moving beyond randomized trials. Am J Public Health. 2004;94:400405. 14. Vautier F, Hildebrand K, Dedeurwaeder M, Herp M. Dry supplementary feeding programmes: an eective short-term

19.

20.

21.

22.

23.

24.

25.

26.

27. 28.

29.

strategy in food crisis situations. Trop Med Int Health. 1999;4:875879. Patel MP, Sandige HL, Ndekha MJ, Briend A, Ashorn P, Manary MJ. Supplemental feeding with ready-to-use therapeutic food in Malawian children at risk of malnutrition. J Health Popul Nutr. 2005;23:351357. Matilsky DK, Maleta K, Castleman T, Manary M. Supplementary feeding with milk/peanut and soy/peanut fortied spreads results in higher recovery rates than feeding with corn/soy blend in moderately wasted Malawian children. J Nutr. 2009; 139:773778. Briend A. Highly nutrient-dense spreads: a new approach to delivering multiple micronutrients to high-risk groups. Br J Nutr. 2001;85(Suppl 2):S175S179. Ruel MT, Menon P, Habicht JP, et al. Age-based preventive targeting of food assistance and behaviour change and communication for reduction of childhood undernutrition in Haiti: a cluster randomised trial. Lancet. 2008;371:588 595. Swindale A, Deitchler M, Cogill B, Marchione T. The Impact of Title II Maternal and Child Health and Nutrition Programs on the Nutritional Status of Children. Washington, DC: Food and Nutrition Technical Assistance Project, Academy of Educational Development, 2004. Available at: http://www. fantaproject.org/downloads/pdfs/pOP4.pdf. Accessed 10 December 2008. Maleta K, Kuittinen J, Duggan MB, et al. Supplementary feeding of underweight, stunted Malawian children with a ready-to-use food. J Pediatr Gastroenterol Nutr. 2004;38:152 158. Galpin L, Thakwalakwa C, Phuka J, et al. Breast milk intake is not reduced more by the introduction of energy dense complementary food than by typical infant porridge. J Nutr. 2007;137:18281833. Phuka JC, Maleta K, Thakwalakwa C, et al. Complementary feeding with fortied spread and incidence of severe stunting in 6- to 18-month-old rural Malawians. Arch Pediatr Adolesc Med. 2008;162:619626. Phuka JC, Maleta K, Thakwalakwa C, et al. Postintervention growth of Malawian children who received 12-mo dietary complementation with a lipid-based nutrient supplement or maize-soy our. Am J Clin Nutr. 2009;89:382390. Menon P, Ruel MT, Loechl CU, et al. Micronutrient Sprinkles reduce anemia among 9- to 24-mo-old children when delivered through an integrated health and nutrition program in rural Haiti. J Nutr. 2007;137:10231030. Toole MJ, Nieburg P, Waldman RJ. The association between inadequate rations, undernutrition prevalence, and mortality in refugee camps: case studies of refugee populations in eastern Thailand, 19791980, and eastern Sudan, 1984 1985. J Trop Pediatr. 1988;34:218224. Stevens A, Araru P, Dragudi B. Outbreak of micronutrient deciency disease: did we respond appropriately? Field Exchange. 2001;12:1517. Upadhyay J. Persistent micronutrient problems among refugees in Nepal. Field Exchange. 1999;5:45. Blanck HM, Bowman BA, Serdula MK, Khan LK, Kohn W, Woodru BA. Angular stomatitis and riboavin status among adolescent Bhutanese refugees living in southeastern Nepal. Am J Clin Nutr. 2002;76:430435. Hurrell RF, Reddy MB, Juillerat MA, Cook JD. Degradation of phytic acid in cereal porridges improves iron absorption by human subjects. Am J Clin Nutr. 2003;77:1213 1219.

Nutrition Reviews Vol. 67(12):706718

717

30. Ashworth A, March Y. Iron fortication of dried skim milk and maize-soy-bean-milk mixture (CSM): availability of iron in Jamaican infants. Br J Nutr. 1973;30:577584. 31. Institute of Medicine. Vitamin C Fortication of Food Commodities: Final Report. Washington, DC: National Academy Press; 1997. 32. Dewey KG, Adu-Afarwuah S. Systematic review of the ecacy and eectiveness of complementary feeding interventions in developing countries. Matern Child Nutr. 2008;4(Suppl 1):24 85. 33. Allen LH, Peerson JM, Olney DK. Provision of multiple rather than two or fewer micronutrients more eectively improves growth and other outcomes in micronutrient-decient children and adults. J Nutr. 2009;139:10221030.

34. Administrative Committee on Coordination/Subcommittee on Nutrition (ACC/SCN). What Works? A Review of the Ecacy and Eectiveness of Nutrition Interventions. Allen LH and Gillespie SR. Manila: ACC/SNC: Geneva in collaboration with the Asian Development Bank; 2001. 35. Maxwell D. Global factors shaping the future of food aid: the implications for WFP. Disasters. 2007;31(Suppl 1):S25S39. 36. United States Department of Agriculture. Commodity Operations Page USDA Web Site. Available at: http:// wwwfsausdagov/FSA/webapp?area=home&subject=coop& topic=pas-ex-cr. Accessed 10 December 2008.

718

Nutrition Reviews Vol. 67(12):706718

Copyright of Nutrition Reviews is the property of Blackwell Publishing Limited and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.