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International Notes Outbreak of Pellagra Among Mozambican Refugees - Malawi, 1990

Micronutrient deficiency disorders, including pellagra, have emerged as major problems in refugee populations that depend on international relief assistance for food supplies (1,2). This report summarizes an investigation of pellagra that occurred among Mozambican refugees in Malawi during 1990.

Since 1987, approximately 900,000 Mozambicans have fled armed conflict in their homeland to seek refuge in neighboring Malawi. Approximately half are housed in refugee camps; the remainder live in villages integrated with the local Malawian population. Overall refugee relief assistance is coordinated by the Office of the United Nations High Commissioner for Refugees (UNHCR). Health care is provided by Malawian Ministry of Health personnel assisted by private voluntary organizations. During July-October 1989, 1169 cases of pellagra were detected among Mozambican refugees settled in 11 sites (including both camps and integrated villages) in southern Malawi (1). From February 1 through October 30, 1990, 17,878 cases were reported among 285,942 refugees (attack rate (AR)=6.3%) (Figure 1).

During the 1989 outbreak, Medecins Sans Frontieres, Paris (MSF), the private voluntary organization that provided health care in the 11 sites, established a passive surveillance system in which persons with pellagra who presented to health facilities were recorded separately. (Previously, pellagra cases were reported as unspecified "nutritional disorders" according to the national disease surveillance system.) In July 1990, active case detection was instituted, and detailed information was collected on each patient (including age, sex, address, nationality, date of arrival in Malawi, duration of illness, and clinical signs).

A case of pellagra was defined as dermatitis on two different and symmetrical sites exposed to sunlight or a typical Casal's necklace (Figure 2). Of a sample of 992 case-patients reported in 1990, approximately 60% had associated stomatitis, and 19% had diarrhea. Diagnosis was confirmed at the National Institute of Agronomy in Paris by urinalysis for niacin metabolites (2-pyridone and N1-methyl nicotinamide) in four cases of clinical pellagra (3).

ARs ranged from 0.5% to 13.2% among the 11 refugee sites. The AR for children aged less than 5 years was 1.6%, and for all other age groups combined, 7.3%. Based on population estimates provided by the UNHCR, the AR for females was 7.8 times higher than that for males. ARs in camps were higher than those in integrated villages.

To identify potential risk factors for illness, MSF conducted a matched-pair case-control study from June 11 through June 23. Cases selected were the first 126 consecutive persons with pellagra at the outpatient facility of the three most affected sites. For each patient, one age-, sex-, and location-matched control was selected. Each patient and control provided information about sociodemographic characteristics, nutritional habits, and sources of food. A multivariate analysis suggested that three factors independently protected against pellagra: daily groundnut consumption (odds ratio (OR)=0.1; 95% confidence interval (CI)=0.01-0.95), home maize milling (OR=0.3; 95% CI=0.1-0.5), and garden ownership (OR=0.3; 95% CI=0.15-0.6).

For 1989 and 1990, food supply records from UNHCR, the World Food Program, and the Malawian government were used to calculate the mean daily per capita quantity of available niacin equivalents (ANE) in food distributed to refugees, based on bioavailability of 30% of the niacin in maize flour (4). Groundnut distribution had been disrupted from January through May 1989 and again from January through July 1990, with a corresponding mean daily distribution during these periods of approximately 4.0 mg ANE per person per day (Table 1) (5).

In August 1990, a groundnut supply was identified on the world market, purchased, transported to Malawi, and distributed to refugees by UNHCR; MSF; and Save the Children Fund, United Kingdom. In addition, nicotinamide was used to treat clinical cases, and vitamin B complex tablets were distributed as a preventive measure to refugees living in camps. Active surveillance of new cases is being used to quantify the impact of prevention and control measures. Reported by: P Malfait, MD, A Moren, MD, Epicentre, Paris, France; G Malenga, MD, J Stuckey, MD, Office of the United Nations High Commissioner for Refugees, Blantyre Sub-office, Malawi; A Jonkman, MD, Regional Health Officer, Malawian Ministry of Health, Blantyre, Malawi; MG Etchegorry, MD, Medecins Sans Frontieres, Paris, France; G Begkoyian, MD, Medecins Sans Frontieres, Blantyre, Malawi; JC Dillon, PhD, National Institute of Agronomy, Paris, France. P Hakewill, MD, Office of the United Nations High Commissioner for Refugees, Geneva, Switzerland. Technical Support Div, International Health Program Office; Div of Nutrition, Center for Chronic Disease Prevention and Health Promotion, CDC.

Editorial Note

Editorial Note: Pellagra is a nutritional deficiency disease characterized by dermatitis on areas of the body exposed to sunlight, such as the face, neck, arms, and legs. In severe cases, diarrhea, dementia, and eventually death can occur. First described by Gaspar Casal in Spain in the mid-18th century, pellagra was highly prevalent in maize-consuming populations (e.g., in the southeastern United States, Mediterranean countries of Europe, and North Africa) until the 1930s. In the 1920s, Casimir Funk in France and Joseph Goldberger of the U.S. Public Health Service determined that the cause of pellagra was a nutritional deficiency (6). The specific micronutrient lacking in the diet of pellagra patients was eventually identified as niacin (nicotinic acid or niacinamide). During World War II, pellagra declined in the United States because of mandatory enrichment of bread flour and other cereal grains with niacin. Socioecoconomic factors that also contributed to the elimination of pellagra in the United States, Italy, and other areas with endemic pellagra were the cessation of sharecropping and the resulting increased access to pellagra-protective foods.

A high proportion of dietary niacin is derived from tryptophan, which is metabolized in the body to niacinamide; the common association of pellagra with diets high in maize results from the low tryptophan content of the principle maize protein (zein) and the biologically unavailable form of niacin in maize (7). In Mexico and Central America, where maize is the staple cereal, pellagra is prevented by treatment of maize-flour with lime ("alkali cooking"), which increases the bioavailability of the niacin. Sporadic cases of pellagra continue to be reported from Egypt, India, and countries in eastern and southern Africa. In the 1970s, greater than 100,000 cases of endemic pellagra were reported annually in South Africa (8).

The 1990 pellagra epidemic in Malawi was the most extensive reported in the world since World War II. More than 18,000 cases were reported from all districts, hosting approximately 900,000 refugees in southern Malawi, for an overall AR of 2.0% (J Stuckey, UNHCR, Blantyre, Malawi, unpublished data, December 1990). However, ARs varied greatly by location, from less than 0.5% in integrated villages to 1.2%-11.3% in districts where refugees lived in camps. ARs in integrated villages may have been lower than in camps because refugees in such settings had increased access to alternative food sources of niacin.

Because groundnuts were not available for prolonged periods during 1990, the food ration for Mozambican refugees contained about 4.0 mg ANE (or less than 2.0 mg per 1000 kcal energy intake), substantially less than the recommended daily allowance (RDA) of 6.6 mg per 1000 kcal (4). Because of the high niacin equivalent (NE) content in groundnuts, consumption of this item was protective against pellagra in refugees in Malawi. Although home milling of maize probably does not substantially increase dietary niacin, it may reflect access to other dietary sources.

The higher risk for pellagra among refugee women is consistent with reports of pellagra in the southeastern United States in the early 1900s and might reflect decreased access to foods containing niacin (e.g., meat, fish, and nuts), as well as a higher requirement for NE per 1000 kcal (9). In contrast, the lower AR for children aged less than 5 years may result in part from breastfeeding (i.e., milk has a high niacin content); however, the data from Malawi do not differentiate risk between children aged less than 2 years and 2-5 years.

The outbreak in this report underscores the vulnerability of refugee populations to micronutrient deficiency diseases. Other micronutrient deficiency diseases reported from refugees in Africa have included scurvy, vitamin A deficiency, iron deficiency anemia, and beriberi (2). The severe morbidity and mortality associated with micronutrient disorders, such as pellagra and scurvy, emphasize the need to supply minimal levels of energy and micronutrients to dependent refugee populations, as recommended by the United Nations (10). Donor organizations must be aware of the need to provide adequate amounts of basic food commodities to relief agencies. Public health surveillance systems established in refugee populations should include micronutrient deficiency disorders among routinely monitored health problems.


  1. Moren A, Le Moult D. Pellagra cases in Mozambican refugees

(Letter). Lancet 1990;335:1403-4.

2. Toole MJ, Waldman RJ. Prevention of excess mortality in refugee and displaced populations in developing countries. JAMA 1990;263:3296-302.

3. Sandhu JS, Fraser DN. Measurement of niacin metabolites in urine by high-pressure liquid chromatography: a simple, sensitive assay of niacin nutritional status. Int J Vitam Nutr Res 1981;51:139-44.

4. National Research Council, Commission on Life Sciences, Food and Nutrition Board. Recommended dietary allowances. 10th ed. Washington, DC: National Academy Press, 1989.

5. Watt BK, Merrill AL. Composition of foods: raw, processed, and prepared. Revised ed. Washington, DC: US Department of Agriculture, 1975. (Agricultural handbook no. 8).

6. Roe DA. A plague of corn: the social history of pellagra. Ithaca, New York: Cornell University Press, 1973:99-123.

7. Jukes TH. The prevention and conquest of scurvy, beri-beri, and pellagra. Prev Med 1989;18:877-83.

8. Anonymous. Preventing pellagra (Editorial). S Afr Med J 1979;56:542-3.

9. Carpenter KJ, Lewin WJ. A reexamination of the composition of diets associated with pellagra. J Nutr 1985;115:543-52. 10. United Nations Administrative Committee for Coordination/International Nutrition Planners Forum. Nutrition in times of disaster: report of an international conference, September 27-30, 1988. Geneva, Switzerland: United Nations Administrative Committee for Coordination, Subcommittee on Nutrition/International Nutrition Planners Forum, 1989.

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