A pellagra epidemic in Kuito, Angola
By Sophie Baquet and Michelle van Herp

Sophie Baquet is the headquarter nutritionist in MSF Belgium and Michel van Herp, Headquarters epidemiologist in MSF Belgium. This article is based on field visits to Kuito between August 1999 and March 2000 and from field reports. There is also a contribution from Jeremy Shoham based on a recent review of pellagra in emergencies carried out on behalf of WHO.
Angola has been at war for more than 20 years. A second peace process, initiated at the end of 1994 lasted until 1998 when conflict resumed. Since late 98, more than one hundred thousand people living in Bié province (in the central high plateau of Angola) have fled conflict and sought asylum around Kuito town (the provincial capital of Bié). The population of Kuito town and surrounding area has been estimated at 155,000, with about 110,000 Internally displaced people (IDPs) currently sheltered in various sites around the town. Kuito is effectively now an enclave due to the high level of military activity in the area and is known to be one of the heaviest mined cities in the world.
With little potential for food production by the local population and the numerous displaced people living in Kuito, most of this population are completely dependent on WFP (World Food Programme) rations. Small agricultural fields and seeds have been allocated to the displaced population but harvests are generally poor and insufficient. The purchasing power of the resident population has rapidly decreased due to inflation and the activities of most traders had been reduced due to the war.
MSF Belgium has been present in Bié province since the end of 1989. MSF's work has included operating feeding centres and supporting Kuito general hospital. At the end of July 1999 the first cases of pellagra were diagnosed in Kuito. This marked the beginning of the largest pellagra outbreak documented in the world for displaced or refugee populations since the outbreak in Malawi in 1990 when more than 18,000 cases of pellagra were reported among Mozambican refugees.
Case definition

Classical skin lesions - Cassal's necklace.
The case definition for diagnosis of pellagra used in Kuito was dermatitis on two different and symmetrical sites exposed to sunlight or what is know as a cassal's necklace (see photo).
These classical skin lesions only seem to occur more often in older persons. Furthermore, individuals that do not go outdoors, i.e. are not exposed to sunlight, do not get the skin lesions either. Although the triad of dermatitis, diarrhoea, and dementia is distinctive, these symptoms do not occur in every patient. The earliest manifestations do not include dermatitis and in one third of florid cases dermatitis is the only sign.
The outbreak and the response
Local health professionals in Kuito know about pellagra, but only a few cases a year are seen. From July 1999, a marked increase in cases was seen and the phenomena rapidly became epidemic.
Between August 99 and January 2000, 898 cases of clinically diagnosed pellagra were seen in the hospital (see graph). Once the diagnosis was confirmed patients were referred to the supplementary feeding centre where they received a standard protocol of nicotinamide 50 mg (adults = 3 x 2 tablets/day for 15 days; children = 3 x1 tablet/day over 15 days), vitamin B complex tablets, and a supplementary ration of CSB and dry fish.
The data showed that 83% of pellagra cases were female and that 85% of cases were over 15 years of age. Sixty six percent of cases were IDPs (Table 1a). The attack rates at the end of November were 2.6/1,000 inhabitants. Attack rates by age and sex are given in Table 1b.
It should be noted that the attack rate only reflects dermatitis cases reported at the treatment centres by passive detection and therefore probably underestimates the true attack rate.
Reminder about pellagra

The pellagra case definition was dermatitis on two different and symmetrical sites exposed to sunlight. © P. Delchevalerie
Pellagra is caused by Niacin (Nicotinic acid) deficiency. The condition can be fatal and is often associated with other vitamin B deficiencies. Niacin (vitamin B3) is a water-soluble vitamin widely distributed in plant and animal food but in very small amounts. Rich sources of niacin include groundnuts, fish, meat and pulses. The body can synthesise niacin from the amino acid tryptophan.
The recommended daily requirements range from 13 to 15 mg nicotinic acid equivalent for women and 16 to 19 mg for men. During pregnancy and lactation an additional 2 and 5 mg nicotinic acid respectively are required. For infants and children, 6 and 11 mg daily are recommended, respectively.
The initial clinical features of pellagra are non-specific and include anorexia, prostration, weight loss, headache and a burning sensation in the mouth. The fully developed syndrome, described by the "three D's" consists of dermatitis, gastrointestinal symptoms (diarrhoea), and finally mental impairment (dementia). Eventually the fourth 'D' can occur - death.
Niacin deficiency was endemic and often epidemic among poor population in Europe and USA until the middle of the 20th Century. It was first reported 250 years ago and followed the introduction of maize (low in niacin compared to other cereals) to Europe from the Americas.
Niacin deficiency is now endemic at very low levels amongst the rural poor in Africa where maize is the principal cereal. Examination of rural health centre records may show a few cases - especially during the 'hungry season'. However, outbreaks of pellagra have only occurred in recent years amongst emergency affected populations. The limited epidemiological data available from these emergencies indicate that it affects principally adults, particularly women. When a niacin and/or tryptophan - deficient diet is consumed, the lead-time for developing signs of pellagra is about 2 to 3 months.
The general ration provided by humanitarian agencies was meant to ensure an intake of 1800 kilocalories per person. The commodities were maize flour, pulses, oil and salt. The logistical constraints to supplying the food ration regularly in Kuito were considerable as almost everything had to come in by air. The target groups for the general ration were IDPs and others identified as vulnerable in the resident population (under five, pregnant and lactating, and disabled persons). From November 1999, families with malnourished children were also included as vulnerable, as well as families with pellagra cases.

Between April and December 99 general food rations provided an average of 8 mg niacin per person per day. From November dried fish (a niacin rich food) was distributed to pellagra cases and their families as well as to individuals attending feeding centres and their families. This was seen as a preventive measure.
In view of the fact that the general food distribution did not provide enough niacin, and other sources like CSB were not yet available in the ration until June 2000, a distribution of vitamin B complex tablets to all women aged 15 and over was organised as an emergency response by MSF and other humanitarian agencies in December 1999. The target group was chosen only because of lack of resources to organise a distribution to the entire population Thirty tablets were distributed to all women. A nutritional survey conducted in December 1999 assessed compliance with intake of vitamin B complex tablets by counting the number of tablets left in the distributed bag after a set number of days. The survey found low compliance.
It was concluded that a vitamin B tablet distribution campaign did not seem to be the most effective solution to control a pellagra outbreak. Furthermore, targeting women with tablets was an emergency measure, but not a satisfactory option, as all strata of the population were probably deficient in niacin.
At a multi-agency meeting held in January 2000 it was agreed that the general ration should be supplemented with CSB (rather than groundnuts as the latter lacks riboflavin and pyridoxine both of which are necessary for the conversion of tryptophan into niacin) and that the priority group for receiving the expanded ration should be the displaced. Consensus was also reached that the possibility of including vulnerable residents should also be investigated.
Table 1a: Distribution of pellagra cases per main demographic characteristic, 1999, n = 571 cases, MSF. | ||
Distribution by sex | male: ...............................98 female: ..........................473 |
(17%) (83%) |
Distribution by age | < 15 years: ......................86 ? 15 years: ....................485 |
(15%) (85%) |
Distribution by residential status | resident: ........................196 displaced: .....................372 |
(34%) (66%) |
Table 1b: Attack rates per main demographic groups, n = 571 cases, 1999, MSF | ||||
IDPs | Resident | Total pop. | ||
n = 110,000 IDPs | n = 130,000 inhab. | n = 240,000 pop. | ||
Male | < 15 y | 0.8 / 1,000 | 0.5 / 1,000 | 0.65 / 1,000 |
>= 15 y | 1.4 / 1,000 | 0.6 / 1,000 | 1.0 / 1,000 | |
Female | < 15 y | 1.2 / 1,000 | 0.4 / 1,000 | 0.8 / 1,000 |
>= 15 y | 10.2 / 1,000 | 4.5 / 1,000 | 7.1 / 1,000 | |
Total | 3.4 / 1,000 | 1.5 / 1,000 | 2.4 / 1,000 |
Discussion
By January 2000 a number of important issues and lessons about the outbreak and response had been identified at multi-agency meetings and through discussion with knowledgeable experts.
- Although an average intake of 15-20 mg of niacin per person per day prevents pellagra for all age groups, this applies to healthy individuals. However, as people had been subsisting on the deficient for many months body stores would have been depleted in response to infection and other metabolic stresses so that it was critical to increase body stores to stave off overt deficiency. Also, the majority of the population in Kuito were exposed to malaria, diarrhoea and an increased risk of other infections and therefore may have had a greater requirement.
- The fact that the general ration was deficient in many nutrients including all those implicated in pellagra led to the conclusion that CSB would be the best food supplement to improve the intakes of a wide range of nutrients. Groundnuts and beans, although rich in niacin, have relatively low levels of riboflavin and pyridoxine which are both required to convert tryptophan to niacin.
- There was uncertainty about the amount of niacin in maize - food composition tables show much variability. It is therefore important to advocate for 'nutrient content' labelling of maize so that it is possible to determine more accurately the amount of supplement to include in the ration to make up for any niacin shortfall.
- Although the case definitions used ensured that the diagnosis was not in doubt, the actual numbers with niacin deficiency in the population were grossly underestimated. Children would be eating the same diet as adults and have the same proportionate requirements for niacin, but would not necessarily show the skin lesions of pellagra - they may get diarrhoea. Classical signs are much less common in young children than in adults.
There were many possible explanations for the high prevalence of pellagra amongst females over 15 years of age; demographic profile, different health seeking behaviour, different sunlight exposure (men go bare chested so will not get cassals necklace in sunlight), real dietary differences, different clinical expression of illness and hormonal differences. - In the longer term a more appropriate solution should be found than supplementing the general ration with fortified CSB. Strategies used in similar situations have included fortification of the maize in local mills and commercial fortification of maize in country or in the country of origin.
Update on situation
A second vitamin B distribution was carried out at the end of February/March 2000. This was targeted to everyone in Kuito and implemented as CSB had as yet to be included in the general ration. As can be seen from the graph, the number of cases of pellagra began to decline markedly in February and March. This was probably due to a combination of factors, i.e. the vitamin tablets distribution, a diversified WFP ration (including groundnuts), less sunshine and a small harvest. However, as can also be seen from the graph, pellagra cases were beginning to reappear again by the end of April. Although WFP had been promising the delivery and addition of CSB to the general ration since early in 2000 none had been distributed in the general ration by the end of May 2000.
Conclusions and recommendations
This epidemic underscores once more the vulnerability of food aid dependent population to micro-nutrients deficiency diseases such as pellagra (an easily preventable nutritional deficiency).
Despite international nutrition official recommendations, relief programmes failed to provide the minimum recommended daily allowances (RDA) of essential micronutrients to Kuito's vulnerable population.
Although it was recognised that niacin rich foods needed to be urgently added to the general ration, this proved not to be possible. In the event niacin rich foods (dried fish and CSB) were only targeted through feeding centres. It was unclear whether this occurred as a result of logistical difficulties, or due to inadequate provisioning of, or access to CSB. In any event given the current policy of ensuring adequate micro-nutrient intake for populations totally dependent on food aid through the provision of fortified blended foods, established in the most recent WFP/UNHCR MOU, questions need to be asked about why this was not possible during the Kuito emergency. There is also an issue (which may well relate to the lack of supply or access to CSB) about only targeting niacin rich supplements to pellagra cases and malnourished children and their respective families. This curative strategy is arguably unethical. In a situation where there is a clear public health emergency of large proportion it should surely be incumbent upon the international community to prevent further cases of this disease occurring and provide niacin rich food to the whole population.
Many observers and experts believe that there needs to be a review of the diagnostic criteria for pellagra. In this case relying on narrow dermatologically based diagnostic criteria may have obscured a high prevalence in other demographic groups (i.e. it wasn't just women over 15 years of age who were suffering). In the event due to lack of resources, this led to an initial vitamin tablet distribution to adult females only.
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Reference this page
Sophie Baquet and Michelle van Herp (). A pellagra epidemic in Kuito, Angola. Field Exchange 10, July 2000. p11. www.ennonline.net/fex/10/pellagra
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