A Report on the Investigation
into Recurrent Epidemics of
Pellagra in Kuito, Angola
Michael Golden
February 2002
Food and Nutrition Technical Assistance Project (FANTA)
Academy for Educational Development 1825 Connecticut Ave., NW Washington, DC 20009-5721
Tel: 202-884-8000 Fax: 202-884-8432 E-mail: fanta@aed.org Website: www.fantaproject.org
This publication was made possible through
support provided to the Food and Nutrition
Technical Assistance (FANTA) Project by the
Office of Health, Infectious Disease and
Nutrition of the Bureau for Global Health at the
U.S. Agency for International Development,
under terms of Cooperative Agreement No.
HRN-A-00-98-00046-00 awarded to the
Academy for Educational Development (AED).
The opinions expressed herein are those of the
author and do not necessarily reflect the views
of the U.S. Agency for International
Development.
Recommended citation:
Golden, Michael. A Report on an Investigation
into Recurrent Epidemics of Pellagra in Kuito,
Angola. Washington, D.C.: Food and Nutrition
Technical Assistance Project, Academy for
Educational Development, 2002.
Copies of the publication can be obtained
from:
Food and Nutrition Technical Assistance
Project
Academy for Educational Development
1825 Connecticut Avenue, NW
Washington, D.C. 20009-5721
Tel: 202-884-8000
Fax: 202-884-8432
Email: fanta@aed.org
Website: www.fantaproject.org
ACKNOWLEDGEMENTS
This report was compiled and revised by Caroline Grobler-Tanner
(FANTA). Thanks to Bill Hagleman, Carolyn Mutumba, Jon Brause, and
Eunyong Chung of USAID and Bruce Cogill of the FANTA Project for
their support and input. Assistance was provided by FANTA’s Juliette
Jack Banerjee, Heather Finegan, Alain Otarola and Angela Johnson.
The investigation on which this report is based was carried out in Angola
by Dr. Michael Golden. Dr. Golden thanks all those who contributed to
this report. Particular thanks to Heather Evans, Robert Hellyer and Jeffrey
Ashley at USAID/Luanda and the Medicins Sans Frontieres-Belgium team
in Kuito and Camacupa. Paola Valenti and Yvonne Grellety assisted in
the field visit and contributed greatly to the observations and discussion.
Leopoldina Neta, UNICEF field officer in Kuito, arranged all of the local
visits. Oladipo Onayemi, WFP Nutritionist, opened doors that would
otherwise have been closed. Thanks also to Jeremias Samalungo, Maluna
de Costa and Francois Jesus of the local WFP office, Claudia Lopas
(OCHA), Mark Wright and Sheri Laker (SCF, UK), Daniel Julia (CARE),
Domingos Castro (ICRC), Alcedo dos Santos and Pedro Siloka (Africare),
Mike McDonagh and colleagues (Concern) and Professor Luis Bernadino.
Special thanks to Jose Dias Van-Dunen, Vice Minister of Health, for his
concern and understanding and to the people of Angola.
ACRONYMS
CMR
CSB
CSM
ICSM
FAA
IDP
MINARS
MSF-B
OCHA
PICs
TFC
UNITA
WFH
WFP
Crude Mortality Rate
Corn Soy Blend
Corn Soy Milk
Instant Corn Soy Milk
Angolan Army
Internally Displaced Person
Ministry of Reinsertion and Social Affairs
Medicins Sans Frontieres Belgium
UN Office for the Coordination of Humanitarian
Assistance
Program Infant Centers
Therapeutic Feeding Center
National Union for the Total Independence of Angola
Weight for Height
World Food Program
CONTENTS
Executive Summary
i
1. Introduction
1
1.1
1.2
1
3
Overview of Pellagra
Background – Bie Province
2. Methods
5
3. Findings
6
3.1
3.2
3.3
3.4
3.5
3.6
3.7
3.8
3.9
6
9
11
13
15
17
18
22
3.10
Pellagra Diagnosis and Evolution of the Epidemic
Pellagra Cases
Pellagra Prevalence
Nutritional Status of Pellagra Patients
Pellagra and Malnutrition
Pellagra and Nutrition and Mortality Survey Data
Pellagra, Morbidity and Mortality
Food Distribution
Energy and Micronutrients in the
Distributed Food Rations
Food Security and Agricultural Activity
27
31
4. Recommendations
34
Appendix 1
38
Executive Summary
EXECUTIVE SUMMARY
Recurrent reports of outbreaks of pellagra in Bie province, Angola have caused concern among
implementing agencies and donors. USAID/Food for Peace-Emergency Programs requested the Food
and Nutrition Technical Assistance (FANTA) project to conduct a review of the pellagra situation in
Bie province (Kuito) to provide an understanding of the determinants of pellagra and to make
recommendations for appropriate interventions. A field visit investigation was conducted in
July/August 2001. Key findings and recommendations are summarized below and expanded upon in
depth in the body of the report.
Key findings reveal the prevalence of pellagra is higher than previously thought. At the same time
there has been an increase in kwashiorkor. Both pellagra and kwashiorkor are diseases related to poor
diet. Mortality rates have recently risen sharply to crisis proportions. The analysis reveals that
nutritional deficiencies underlie this increase in mortality. However, these nutritional deficiencies
are not reflected in the rates of wasting. Thus the quality of the diet in Kuito area needs to be urgently
addressed. A comprehensive strategy to address the problem of micronutrient deficiency in Bie
province is suggested. Immediate actions to reduce morbidity and mortality include revisions to the
ration levels, market interventions to reach those not receiving a ration, seed diversity and small
animal production. Strategies to prevent further epidemics include milling and fortification of
imported maize and addressing the shortage of land.
Key Findings
Pellagra is a disease caused by consumption of a diet of low quality. It is caused by a dietary
deficiency of niacin, pyridoxine and riboflavin. Niacin is taken pre-formed as well as being
synthesized in the body from the amino acid tryptophan. This synthesis is not efficient and requires
pyrodoxine (B6), riboflavin (B2), iron and possibly zinc. In essence, clinical pellagra is a multiple
micronutrient deficiency syndrome that occurs when there is a diet consisting of a staple that is
intrinsically low in available niacin. Clinical pellagra causes dermatitis (skin lesions), diarrhea and a
neurological condition similar to dementia. As with most nutritional deficiencies, there are many
mild cases for each severe clinical manifestation (the iceberg effect) and mild cases contribute to
morbidity and mortality in a population. Pellagra is associated with maize as the staple in the diet.
For the past three years, annual epidemics of pellagra have been reported in the Kuito area of Angola.
The prevalence of pellagra is about 10% in the displaced camps around Kuito and about 30% in
Camacupa. On the surface, this prevalence may not seem alarming, however, it should be noted that
while 10-30% of the population show clinical signs, almost everyone will have sub-clinical niacin
deficiency that over time and on the same diet will become moderate or severe cases. The most likely
explanation for a high prevalence of pellagra in Bie province in particular is partly related to caserecognition and partly due to the cultural practices of the local population. Pellagra may exist in other
maize eating populations in Angola, but this has not been investigated. Prevalence is highest among
adult women partly for metabolic reasons but perhaps also because women form the bulk of the adult
population. Adolescents and youths are also affected. It is unlikely that the pellagra is currently a
dominant direct cause of mortality although it almost certainly contributes to mortality ascribed to
other illnesses.
i
Executive Summary
The pellagra patients presenting at clinics are of normal weight or are overweight. This is
because deficiency of the nutrients niacin, riboflavin and pyridoxine (so called ‘type I nutrients’)
give rise to specific symptoms but do not cause loss of body weight (wasting). However, type I
deficiency does cause severe illness including pellagra, kwashiorkor, immunoincompetence and
death. The population is in nutritional crisis with a continued high mortality rate for over three
years. This has recently increased sharply to crisis proportions (Crude Mortality Rate
4/10,000/day according to survey derived data). Although nutritional deficiencies underlie this
excess mortality, it is not reflected in the rate of wasting (global malnutrition rate <-2Z scores
weight for height).
A major proportion of the population is entirely dependent upon humanitarian aid. Almost 60% of
the population receives humanitarian aid and over two-fifths of all food eaten in the area is flown in
by the World Food Program. Without this sustained effort, the population would starve. However,
problems associated with the distribution together with increasing reliance on maize and recent
decreases in the amount of fortified blended foods have resulted in food rations with a niacin content
low enough to cause overt clinical pellagra in otherwise healthy experimental subjects. In addition,
evidence reveals that there is also an increase in edematous malnutrition (kwashiorkor), which is also
related to a poor diet. Kwashiorkor is now the leading cause of death in the IDP camps. The recent
pellagra epidemic is thus symptomatic of serious micronutrient deficiencies. Therefore, it is critical
to take steps to improve the quality of the diet that is eaten in Kuito and the surrounding area.
Recommendations
There should be a comprehensive strategy to address the problem of micronutrient deficiency in
general and pellagra in particular in Bie province. The immediate actions will be relatively
expensive, but will reduce morbidity and save lives. These actions should be viewed as a short-term
expedient to deal with the present situation. Strategies to prevent further epidemics and address
micronutrient deficiency should be started as soon as possible to prevent a fourth epidemic from
occurring next year.
Immediate Actions to Reduce Morbidity and Mortality
Revising the general and supplementary rations: Food baskets should include niacin rich foods.
Improvement in the amount of niacin could be achieved either by increasing the quantities of blended
food (such as CSB/CSM or ICSM) purchased and distributed and/or by purchasing and distributing
groundnuts in the general distribution. While groundnuts are high in pre-formed niacin and will help
prevent pellagra specifically, this intervention alone will not impact on the mortality rate which is
almost certainly due to widespread micronutrient deficiency. Thus a modest increase in the amount
of blended foods (at least to last years levels) together with a small amount of groundnuts is
preferred.
In particular, the ration given to pellagra patients needs to be revised so that they are not given
additional maize, beans and oil. Pellagra patients do not require additional energy but rather
micronutrinet rich foods. Thus ration should be comprised of a modest amount of blended foods
alone (120g/person/day). The families of those admitted to TFC’s should also have a diet particularly
rich in micronutrients as kwashiorkor is the dominant form of severe malnutrition and is also
associated with a diet of poor quality.
ii
Executive Summary
Interventions to address those not receiving a ration: In order to address the needs of residents and
those who do not receive a general ration, additional actions will be required. While the overall
distribution of niacin rich foods will improve the situation in the IDP camps, there will also need to
be a measure of redistribution. Diet diversification should be encouraged through trading and the
promotion of simple, feasible education messages. It is recommended that direct market
interventions should be explored to assess the feasibility of providing relatively low price niacin rich
foods through the market. The possibility of monetization of blended foods and other micronutrient
rich foods should be further investigated.
Since the traditional way of cooking in Angola involves adding a sauce to the staple, it is also
suggested that UNICEF purchase a small consignment of micronutrient fortified condiment mix
(such as “QB mix” made by Nutriset, France). The QB mix could be sold through the market at cost.
This would need to be tried and tested to assess acceptability and viability and cost-effectiveness. If it
proves successful, it would be a cheap and effective strategy that would limit the need for blended
foods.
Seed diversity and small animal production. Annual crops that could be usefully grown in Bie
province include groundnuts, soya beans, sunflower, sesame and chilli pepper. This would result in a
diet that is adequate and balanced. However, it is doubtful that there will be a major impact from
seed distribution without more land being available. Re-establishment of local production of small
animals such as chickens or guinea pigs should be encouraged. This should be tried on a small scale
to test the feasibility, particularly given the limitations of providing animal feed in an already food
deficit area. FAO should take the lead on this.
Strategies to Prevent Further Epidemics and Address the Micronutrient Problem
Milling and fortification: Imported maize should be milled and fortified. All the maize imported into
Kuito should be milled in Lobito (the port of entry) and fortified with a micronutrient mix that
includes niacin, riboflavin, pyrodoxine, iron, zinc, vitamin C and antioxidants (such as vitamin E and
selinium). Milling and fortification is a feasible, viable and sustainable option and would address the
current problem in Bie as well as building national capacity to meet the nutritional needs of the
population. Once established, this would negate the need for expensive short-term interventions.
Technical experts in food technology, milling and fortification will need to conduct a field
assessment and a cost analysis. The Government of Angola should take the lead on the milling with
technical assistance from WFP and from UNICEF on micronutrient fortification.
Land allocation: In order to ensure food security and diet diversity in the longer term, additional land
should be made available to the displaced population to grow a variety of crops. An extra 60,000
hectares of land needs to be brought into cultivation in the Kuito area. Where possible, land provision
to families should be increased from the present 0.5 hectares, to close to 3 hectares. It is
recommended that a multi-agency high level delegation should negotiate such a distribution with
government officials.
A number of other recommendations are made and these include; conducting a survey to determine
the true prevalence of pellagra, analyzing the nutritional content of the distributed food, overhauling
the organization of the general distribution with particular emphasis on effective food basket
monitoring, effective tracking of the micronutrient content of distributed food and training and
raising awareness of micronutrient deficiency among key program staff and decision makers.
iii
Introduction
1. INTRODUCTION
1.1. Overview of Pellagra
Pellagra is a disease caused by consumption of a diet of poor quality. It is not due to insufficient
total food (energy) intake or to other diseases such as diarrhea or infection. It is caused by an
insufficiency of the vitamin niacin in the body. Clinically pellagra causes dermatitis (skin lesions),
diarrhea and a neurological condition similar to dementia (known as the 3 D’s). The dermatitis can
occur anywhere on the body that is exposed to damage, but it is only characteristic of pellagra when
it is symmetrical and on those parts of the body that are exposed to the sunlight; the face, neck, arms
and sometimes the backs of the legs.1 When the dermatitis occurs elsewhere it is more likely to be
due to other causes (such as kwashiorkor) and is not recognised as pellagra, even though some of
these cases may in fact be due to pellagra.2 Likewise there are no characteristic features of the
diarrhea caused by pellagra and most cases of diarrhea are due to other causes.3 The true nature of
the neurological symptoms is not normally discerned. Patients that are not significantly exposed to
sunlight are likely to remain undiagnosed.4 Thus those who are not exposed to direct sunlight (and
hence do not develop the classical distribution of skin lesions) might suffer from diarrhea and
neurological illness that is incorrectly ascribed to infective or psychological conditions. It is
unknown whether this occurs under field conditions. Typically, between 4% and 10% of patients
with classical skin lesions have their nervous systems affected.
In mild cases, pellagra is associated with decreased resistance to disease and increased susceptibility
to damage from infection and toxins. Symptomatic patients often have iron deficient anaemia. In
severe cases, pellagra can cause death, either directly from diarrhea/coma or from the decreased
resistance to other diseases. Deaths due to pellagra are often incorrectly diagnosed, even in the
presence of an epidemic of pellagra.
1
The lesions resemble sunburn. There is redness with itching and a burning sensation, followed by drying and cracking of the
skin to form shiny areas. In long-standing lesions there can be hyperkeratosis with swelling of the underlying tissues. The
overlying skin then cracks to form fissures which become secondarily infected, but there is little acute inflammation, the skin
typically becomes very dark, even in light-skinned people. There is usually a sharp demarcation between the skin that shows the
lesion and the rest of the skin. Thus, although the whole body is functionally niacin deficient, one area of skin is quite different
from an area a short distance away, which appears normal. It is unclear why only some of the areas exposed to the sun develop
the lesions. One can speculate that it may relate to additional trauma in the affected area, for example from rubbing or scratching.
2
Skin lesions of kwashiorkor are almost identical to those of pellagra except for their distribution on the body. This is probably
because both pellagra and kwashiorkor share a biochemical lesion in having inadequate amounts of reduced NADH and NADPH.
However, in kwashiorkor this is because of an increased rate of oxidation of the NADPH to NADP, whereas in pellagra it is
because of a decreased absolute level of NAD(H) and NADP(H)). Both diseases are caused by a diet of poor quality.
3
Patients may complain of nausea and a burning sensation in the upper abdomen. They may salivate excessively with
inflammation of the mouth (stomatitis), lips and tongue (glossitis). There is usually a marked reduction in gastric acid production
with growth bacteria in the stomach. Gastroenteritis is characteristic. The diarrhea is sometimes bloody.
4
Early symptoms are non-specific and include lethargy, tiredness, apathy, anxiety, depression, forgetfulness, headache and
irritability. These can then progress to tremors and an encephalopathy with coma and death. The brain lesions may be related to
inadequate levels of the neurotransmitter serotonin, which is made in the brain from the tryptophan. Pellagrins in Hyderabad
with depression had a much lower serotonin level in their platelets than pellagrins without depression. Many of the patients have
reduced or absent tendon reflexes, however, it is unclear if this is primarily due to the niacin deficiency or a feature of
accompanying deficiencies of other vitamins essential for nerve function.
1
Introduction
As with most nutritional deficiencies, there are many mild cases for each severe clinical
manifestation (the iceberg effect). Without treatment or changes to the diet, the mild cases will
deteriorate to become moderate or severe. Thus as with widespread mild and sub-clinical iron,
iodine or vitamin A deficiency, mild pellagra may contribute to significant increases in morbidity and
mortality in a population.
To satisfy the body’s requirement, niacin is taken pre-formed as well as synthesised in the body from
the amino acid tryptophan. This synthesis is not efficient, it requires adequate tryptophan containing
protein as well as pyridoxine (vitamin B6), riboflavin (vitamin B2), iron and possibly zinc in
adequate amounts. If any of these components are deficient there will not be sufficient endogenous
synthesis of niacin and pellagra can result. Appendix 1 outlines the metabolic pathway for the
biosynthesis of niacin in the body and the nutrients involved. In essence, clinical pellagra is a
multiple deficiency syndrome that only occurs when there is a very restricted diet consisting mainly
of a staple that is intrinsically low in niacin.
Pellagra is especially associated with maize as the staple. This is for three reasons. First, both the
level of pre-formed niacin and of tryptophan is low in maize. Second, at least two-thirds of the
niacin in maize is bound to protein. This niacin is not available unless it is released during cooking.
This only happens when the maize is alkalinised. For example, traditional practices in Mexico and
central America use lime or plant ash which when dissolved in the water give an alkaline solution in
which maize meal is then cooked. Typically this is not the culinary practice in areas where pellagra
is, or was endemic.5 6 Extensive enquires were made in Kuito to find if there was any culture of
using plant ash in cooking or for soap making (native soap is made from boiling alkaline ash extract
with lipid). In contrast to other areas in Africa, there was no home-made soap in the markets and
none of the resident key-informants had seen or heard of native soap being prepared in this area.
Samples of ash were collected from cooking fires during the visit to Kuito and the pH of the
dissolved ash was about 8.6, which is probably insufficient. Nevertheless, as there is no culture of
using ash in this area, it is likely that a campaign to persuade families to add cooking fire ash to their
food would not be particularly successful at this point. Third, poor people who subsist upon maize
for much of their energy needs often have a precarious status of iron, zinc, vitamin A, vitamin E,
Introduction
riboflavin, vitamin C and pyridoxine. Pellagra also occurs, for similar reasons, in populations
that
subsist upon sorghum, although this is much less common.
Pellagra was endemic in much of the “corn belt” of the USA in the early part of last century, and in
Italy, southern France, Bulgaria and Romania where maize was the staple food. In all these
countries, maize meal is now routinely fortified with niacin and the rise in living standards has led to
diet diversification.7 Pellagra is currently endemic in much of southern Africa with sporadic cases
5
Maize was domesticated as a Central American crop. Native peoples evolved culinary methods to alkalinise the maize-meal and
prevent pellagra. In Mexico, where carboniferous rocks are common, they added considerable quantities of lime to the maize
meal. Further north, where limestone is less common, the Native Americans burnt particular plants and added the ash to the
maize meal during cooking. Anthropologists have recorded how the old women add handfuls of the ash until the (white) maize
reaches a certain colour before they cook it.
6
Where maize is normally eaten without addition of strong alkali, its content of niacin should be reduced by two thirds when
computing the niacin in the diet. This has been done in the calculations used for this report.
7
USA has fortified both wheat and maize flour with niacin, thiamine and riboflavin since 1941 with 55mg niacin /kg. Niacin is
also added in Australia (15mg/kg), Chile (13mg/kg), Dominican Republic (44mg/kg), Kenya (44mg/kg), Mexico (35-70mg/kg),
Nigeria (50mg/kg), Philippines (44mg/kg), Switzerland (50mg/kg) and UK (16mg/kg).
2
Introduction
occurring among the poor wherever maize is the staple food. For example, a pediatrician in Maputo,
Mozambique sees about one case per week on a routine basis. A recent survey in three rural areas of
Tanzania showed the prevalence of pellagra between 0.4% and 9.4% of the population.8
1.2. Background - Bie Province
Bie province lies in the central plateau of Angola at an altitude of about 1800m. Despite being in the
tropics the temperature frequently falls sharply at night. Kuito is the provincial capital. Kuito was
the scene of intense fighting between the government forces and UNITA during the early 1990s. For
fifteen months, the main street of Kuito was the front line and the surrounding countryside was
largely under UNITA control. The government forces were effectively besieged and much of central
Kuito destroyed. Kuito has been under government control since November 1993 and the road to
Kunje opened by March 1994.
The attempt by the government to regain control of Andulo and Bailundo in December 1998
triggered the intensification of fighting throughout Angola including Bie province. Many residents
left for Luanda and there was an influx of about 50,000 people fleeing the fighting. From March
1999 until the present time, there have been successive waves of people displaced by the fighting in
Bie province that have arrived in Kuito. In June 1999, 13 camps were established to the north, south
and east of the town. They have been expanded and extended since that time. By the end of August
1999, the first cases of pellagra were identified. The numbers of Internally Displaced Persons (IDPs)
registered by MINARS (official government statistics) in Kuito is shown in figure 1. The resident
population of Kuito is about 80,000. The IDP population is now about twice the resident population.
About 80km to the east, the municipality of Camacupa came under government control in early 2000
and neighbouring Cuemba municipality came under FAA (Angolan army) control in July 2000.
Fighting continues in many parts of Bie Province and has intensified since November 2000 as the
Government extends its control. Most of the population in the areas that have recently come under
government control have been under UNITA control for many years, they are historically areas from
which UNITA has had general support from the population. Most of the displaced are women and
children with some elderly and disabled. The men are presumed to have been conscripted into the
UNITA forces or to be hiding from the government forces. Naturally, the FAA is concerned about
the loyalties of the displaced families of the men who are still in UNITA territory. Young men in
government held territory might be conscripted into the FAA. Government successes have led to a
steady stream of IDPs seeking support and security in the main population centres. These IDPs have
mostly arrived within the past two years, but particularly over the last six months. They are almost
entirely dependent on the humanitarian community for food.
8
Rikimaru T, Dirangw I and Jeje B. “Prevalence of Pellagra and Food Consumption Pattern in Maize Producing Areas in
Tanzania.” Ppresented at the World Nutrition Congress, Vienna, August 2001. The villages were Iringa (9.8%), Ruvuma (3.3%)
and Singida (0.4%) in each district 3 villages were sampled. A total of 261 households were sampled. The patients with pellagra
had a lower educational level, consumed fewer protein rich foods with less frequency and did not take milk.
3
Introduction
IDP Population of Kuito (Minars)
180,000
160,000
140,000
120,000
100,000
80,000
60,000
40,000
20,000
0
Oct98
Jan99
Apr99
Jul99
Oct99
Jan00
Apr00
Jul00
Oct00
Jan01
Apr01
Figure 1: Total numbers of IDPs registered in Kuito since 1998
Note: Data froFigure 1m MINARS. Official government data is not reliable, but is used by the Office for
the Coordination of Humanitarian Assistance (OCHA). The drop in December of about 40,000 was the result of a
re-validation exercise.
4
Methods
2. METHODS
The report is based upon the following sources of information:
•
Meetings to gather secondary and background information: Meetings were held with the
following: MSF(B) Nutrition Co-ordinator, MSF(B) Head of Mission, MSF(B) Medical Co-ordinator,
Epicentre Consultant, WFP-Luanda Program Officer, WFP-Kuito Program Officer, the WFP
Nutrition Officer for Angola, UNICEF-Nutrition Officer, UNICEF-Field Officer, Kuito SCF(UK)
Head of Mission, SCF(UK) Consultant, CARE-Luanda Health Co-ordinator, CARE-Kuito Officer in
Charge, CARE-Kuito Seeds and Tools Officer, ICRC-Kuito Seeds and Tools Officer, Concern
Medical Co-ordinator, Concern-Camacupa Nurse inCcharge, Concern Seeds and Tools Co-ordinator.
AFRICARE Seeds and Tools Officer, Head of OCHA Kuito. Padre-Camacupa, Professor Luis
Bernadino.
•
Databases and records: MSF(B), databases, files and records were the source of most of the
quantitative data about pellagra patients, TFC, SFC and health post activities. WFP-Kuito provided
data on monthly planned and distributed rations for the past year.
•
Key informant interviews: Interviews were held in Kuito. Informants on the cultural practices of
the Kuito area were mainly employees of WFP, Africare and ICRC who were born and raised in Bie
province and had farmed land in the area. Data obtained were in the form of an unstructured
interview concerning farming practice, land use and local dishes and recipes. The data were
compared with that obtained from similar interviews with employees who were born and raised in
other provinces of Angola.
•
Transect walks: Walks were made through camps in Kuito and Camacupa. The head of household
was interviewed about rations received, family structure and health, diet, land holdings, crops, work
availability and the prices paid for goods and received for labour. The ration cards were examined.
Clinical examinations of the sunlight-exposed skin surfaces of the people encountered during the
walk were made and an estimate of the total numbers of people examined made in order to estimate
the prevalence of pellagra. A sample of the subjects encountered had their Mid-Upper Arm
Circumference (MUAC) taken. It should be noted that this methodology is imprecise because a
random sample was not taken and likely to be an underestimate of the true prevalence.
•
Observation of clinic admissions: The clinician in charge of admitting new patients with pellagra
was observed during her examination and interview of the patients presenting at the clinic. New
patients presenting to the weekly “pellagra clinic” at the hospital and past patients who attended the
supplementary feeding center were examined. The Mid Upper Arm Circumference (MUAC) of these
patients was measured by standard methods.
•
Ward rounds: Ward rounds were conducted in the TFCs of both Concern and MSF-B and also in the
hospital. This was primarily to determine if any of the malnourished patients or their caretakers had
pellagra. However, it provided an opportunity to comment upon the clinical state of the malnourished
patients and current practice in the centers.
•
Markets: The markets in Kuito, Catabola, Camacupa and in the Kuito Camps were examined to
determine the relative amounts and spectrum of foodstuff on sale. Particular attention was paid to the
sale of groundnuts, Corn Soy Blend (CSB) and dried fish.
5
Findings
3. FINDINGS
3.1. Pellagra Diagnosis and Evolution of the Epidemic
Pellagra is endemic in Kuito and Campacupa in both the resident and IDP populations. Historically
pellagra seems to have been endemic and sporadic, but not epidemic. Hard data from before the
recent outbreaks does not exist. This is the third year that a confirmed epidemic has been reported.
The true extent of the “epidemic” cannot be determined from clinic data alone since this
represents a small proportion of the number of cases. A formal survey will be needed to
gather this information.
The first task was to determine whether the diagnosis of pellagra was being appropriately made. This
would have a direct bearing on the reliability of the statistics gathered by MSF-B. The clinician in
charge of the newly diagnosed cases of pellagra was audited as she was making the diagnosis on 80
cases. There was concordance in the diagnosis of 96%. This is about as high a concordance between
two clinicians as is found in any clinical practice. The conclusion from these data is that the clinical
data, as reported from the clinics treating pellagra should be accepted as accurately reflecting the
disease as it presents to the clinic.
This is the third year that there has been an outbreak of overt pellagra. It is clear from the graph
below (figure 2) that from its first recognition as a problem in the Kuito area in 1999, cases of
pellagra have been diagnosed each month at the clinic. The disease is thus endemic in this
population in both the resident and IDP populations.
Figure 2: New cases of pellagra presenting at Kuito hospital clinic: June 99-July 01
New cases of Pellagra: Kuito Hospital Clinic (1999-2001)
350
350
Residents
IDPs
Total
300
250
250
200
200
150
150
100
100
50
50
0
total number of cases
number of cases by origin
300
0
J-99 J-99 A-99 S-99 O-99 N-99 D-99 J-00 F-00 M-00 A-00 M-00 J-00 J-00 A-00 S-00 O-00 N-00 D-00 J-01 F-01 M-01 A-01 M-01 J-01 J-01
Note: The dotted line shows the total caseload. Black arrows show times of B complex tablet distribution.
6
Findings
There have been three major exacerbations of the outbreak. The exacerbation is largely due to lack
of access to foods other than maize at affordable prices and a lack of diversity in the diet due to the
conflict in this area. Outbreaks have occurred from June to October each year for the past three years.
Historically all pellagra outbreaks are seasonal, this was the case in the USA, Europe and India. It is
also seen seasonally in Africa. It is related to the climate (exposure to sunlight) and to the harvest
when the maize crop becomes the major item in the diet. When maize is relatively cheap and
abundant, people increase their consumption of maize and decrease consumption of other foods. In
2001, this seasonal trend coincided with a change in the niacin in the food basket. This is discussed
further below.
The black arrows in figure 2 show the times of distribution of vitamin B-complex tablets (another
was due to take place in July 2001). The original distribution was targeted to women aged 15-45.
This was not accepted by most of the population as targeting of tablets to the fecund female
population exclusively could have been confused with attempts to control fertility. Nevertheless, the
clinic admission rate fell by the time of the second distribution in February 2000. The epidemic in
the summer of 2000 was smaller and appeared to be aborted by the tablet distribution. The current
epidemic is larger than the preceding outbreaks.9 Since January 2000, there have been more residents
than IDPs presenting with pellagra. During the present outbreak there have been about two resident
cases for each IDP case. Figure 3 shows the ratio of resident to IDP cases. Caution should be
exercised in interpreting this data.
Figure 3: The ratio of resident to IDP cases of Pellagra presenting at Kuito hospital clinic
number of new cases (n)
250
New cases of Pellagra: Kuito Hospital Clinic (1999-2001)
300
250
Residents
IDPs
Res/IDP%
100%
200
200
150
150
100
100
50
50
0
total number of cases
300
0
Oct- Nov- Dec- Jan- Feb- Mar- Apr- May- Jun99
99
99
00
00
00
00
00
00
Jul- Aug- Sep- Oct- Nov- Dec- Jan- Feb- Mar- Apr- May- Jun00
00
00
00
00
00
01
01
01
01
01
01
9
Jul01
Meteorological data was unavailable. It would be interesting to examine whether there is a relationship between hours of
sunlight and the presentation of overt pellagra. However, experience derived from investigation of rickets (vitamin D deficiency)
in northern Africa shows that atmospheric dust has a very major effect upon incident UV-light at ground level.
7
Findings
It is important to note that several factors should be considered when interpreting these data. The data
only record patients that voluntarily presented at the clinic. This self-selection of the patients could
be for a number of reasons:
•
Knowledge about the existence of the clinic is more likely for the residents and the long-term
IDPs than for the new arrivals.
•
Those who have other symptoms of pellagra aside from the skin lesions, such as skin
irritation/itching, diarrhea or neurological symptoms, are more likely to seek assistance.
•
The patients that have been diagnosed as having pellagra are enrolled in the supplementary
feeding program and their families are given a family ration. This represents a substantial
income in the present circumstances of Kuito. There is a marked incentive for those who think
that they may have pellagra to present at the clinic. There were some who presented with selfinflicted excoriation on their arms who were clearly seeking to gain access to food by this means.
For these reasons, it was anticipated that the clinic data would represent most of the cases in
Kuito. Upon visiting the camps, this was found not to be the case. There is thus a discrepancy
between the expected high attendance rate at the clinic and the large numbers of patients seen at
the camps (see below) who were not enrolled in the pellagra clinic.
It is difficult to know the extent to which each of these factors affects the clinic-derived data. There
were very few cases of patients complaining of pellagra recorded in the records of the health posts in
the camps. These health posts could not enroll patients to receive additional food. It may be that the
families in the camps were already receiving general rations, but the old IDPs and the residents who
were not receiving any food assistance were presenting at the hospital. This could account for the
discrepancy between the resident and IDP populations. Unfortunately, the data collected from the
IDPs do not differentiate between old IDPs who are not receiving general distributions and the new
IDPs who have cards and are receiving the general distribution. Nevertheless, this is not an entirely
satisfactory explanation. Figure 4 shows the proportion of residents to IDPs presenting to the clinic
in Kuito and Camacupa. The proportion of IDPs to residents is almost identical in the two sites, yet
there is a marked difference in the registration and delivery of the general distribution.
Figure 4: Proportion of residents/ IDPs in Kuito and Camacupa presenting with pellagra
Status-Camacupa
Status-Kuito
IDP
35%
IDPs
30%
Res
70%
Res
65%
8
Findings
3.2. Pellagra Cases
Clinical signs differ in Kuito and Camacupa. This is partly due to ascertainment bias. All the cases were
self-presenting at the clinic. There has been no attempt to survey either the camps or the towns to determine
the true prevalence. Many of the patients in Kuito appeared to be recent cases with a relatively short
history. In contrast, more than half the patients in Camacupa had symptoms for over two months. Most
cases are adults and adolescents. The high proportion of females presenting with pellagra is partly due to
metabolic differences. It is also likely to be due to the higher proportion of females in the camps and town.
The true sex ratio will only be ascertained from a pellagra survey. The clinic-derived data should be taken
as tentative and not used alone to determine an intervention strategy.
Clinical data were obtained from 640 cases of diagnosed pellagra from Kuito and a further 70 cases
from Camacupa. The overwhelming majority of the patients were adults with only 1% over 65 years
old and 8% between 51 and 65 years. Fifteen percent were below 18 years. The numbers were
similar in Camacupa where 24% were below 18 years. The majority of the patients in both areas
were female. This distribution is similar to the age/gender ratios seen in other outbreaks in Africa
and India (see figure 5). However, a large number of the subjects seen with pellagra in the camps
were adolescents and the question arises as to whether the adults are more likely to present at the
clinic for treatment. Females out-number males in the camps very markedly. Indeed, in the
Camacupa camps, no able-bodied adult males were seen. Thus, the general population from which
the clinic population is drawn is overwhelmingly female. Again the clinic data is subject to
ascertainment bias and should be related to the age/sex distribution of the at-risk population before
any conclusions can be drawn about the propensity for development of pellagra in Kuito. Only a
stratified survey will reveal the true age:sex distribution.
Age of Pellagrins
(Kuito)65+
1%
51-65
8%
Sex-ratio - Kuito
Sex-ratio - Camacupa
<10
7%
10-18
8%
19-50
76%
Adolescent
14%
Male
28%
Male
13%
Child
10%
Female
72%
Female
63%
Figure 5: Age of patients in Kuito and sex distribution of patients in Kuito and Camacupa
Prevalence of diarrhea among pellagra cases presenting at clinics in Kuito and Camacupa was
assessed. Marked differences were found. Fifty-five percent of the patients in Camacupa had
diarrhea. This is to be expected and denotes moderate to severe classical pellagra in most of these
patients. The very low prevalence of diarrhea in the Kuito cases is not a usual finding, and suggests
that these cases are much milder than the ones in Camacupa. The likely explanation is that the Kuito
cases are presenting at a much earlier stage because of anticipated supplementary feeding enrollment
and family ration.
The vast majority of the patients were diagnosed and had lesions on the forearms or face. Only half
the patients had neck lesions that are reproduced in all the text books as the classical feature of
9
Findings
pellagra. Virtually all the patients with the classical neck lesions also had typical skin lesions
elsewhere. About a third of the patients had neurological complaints. These were mainly of a mild
and relatively non-specific nature. There would need to be a control group to ascertain the
proportion of these complaints that were due to the circumstances under which the patients lived.
Clearly all subjects are stressed in Kuito.
The question arises as to the length of time that the symptoms were present when the patients
presented. This is the time of interest in relation to the aetiological factors, rather than the time of
presentation to the clinic. Such data were collected from the 70 patients in Camacupa (see figure 6).
In most of the cases the length of history was less than two months. For about 10% of the patients it
was more than one year. Clearly, in Camacupa, some of the patients have very long-standing chronic
pellagra. This reinforces the data, which shows that pellagra is an endemic disease of Bie province
and that the disease is also prevalent in the UNITA held areas. Similar data are not available for the
patients in Kuito. However, the patients interviewed in Kuito had a much shorter history, except for
some of the newly arrived IDPs. This is likely due to the presence of pellagra services in Kuito for
some years.
Figure 6: Length of history of pellagra
Percent cases (%)
Length of History of Pellagra (Months)
1
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
0
0
10
20
30
40
Note: Cumulative distribution of the time from onset of symptoms to presentation at the
clinic. The proportion of cases can be read on the y axis against the length of time on the x
axis. Thus 50% of the cases presented within 2.5 months of the onset of symptoms.
10
50
Findings
3.3. Pellagra Prevalence
Pellagra prevalence is estimated at 10% in Kuito and 30% in Camacupa. While on the surface this seems low,
it is noted that initial reports suggested a prevalence of 0.35%. While 10% have clinical pellagra, almost
everyone will have sub-clinical niacin deficiency. Those affected by pellagra were of normal weight or
overweight thus indicating that the quality of food eaten and not the quantity is a critical issue. These findings
were surprising and significant. The most likely explanation for a high prevalence of pellagra in Bie province
in particular is partly related to case-recognition and partly to the cultural practices of the local population.
Transect walks were undertaken in four camps in Kuito. Of the approximately 300 people examined
in these walks, approximately 10% had skin lesions characteristic of pellagra. The prevalence
appeared to be similar in each of the camps. The majority of the subjects seen with pellagra were
youths and adolescents, with about equal numbers of boys and girls represented. There were fewer
adult females examined during the walks - again about 10% of these had pellagra. There were too
few adult males examined to reach any judgement. Similar transect walks in three camps in
Camacupa showed a much higher prevalence. Of about 200 people examined, 30% had lesions of
pellagra. Again, most of the subjects examined were adolescents and school-age children. These
people were the survivors who had managed to reach Camacupa. They had been living for most of
their lives in UNITA held territory. They were remarkably stunted.10 During the walks, several
experienced nurses, doctors and nutritionists assisted in assessing the situation. Initially none of
these professionals noticed the clinical signs of pellagra since they were looking for classical severe
cases (such as the cassal’s necklace). A great many patients showed more subtle, but nevertheless,
unequivocal lesions that would not have been recognised by the vast majority of professionals. Thus,
even experienced reputable NGOs may not recognize the more subtle signs.
In summary, firstly, it is almost certain that the cases of pellagra presenting at the clinic represent a
very small proportion of the true number cases in the Kuito area. Secondly, the condition is endemic
in the Bie area, as it is in many areas of Africa where maize is the principle staple, and thirdly, it is
only now being recognised as a major problem in the Bie area because the clinicians and population
have been sensitized to the problem.
Why is pellagra apparently confined to Bie province?
A major corollary of the failure of accompanying professionals to recognise pellagra is that endemic
pellagra may well be present in other areas of Angola, but is as yet unrecognised. The only evidence
that pellagra does not occur in other areas where maize is widely eaten such as Huambo, for example,
is that overt cases have not been reported from that area. To resolve the question of why cases are
reported from Bie, but not from other areas, it would be necessary for an experienced clinician to
visit other areas and examine people for the lesions. In some corn eating populations such as
Benguela and Huila, it would be important to examine pellagra prevalence. It is interesting to note
that Benguela is coastal and there is much more marine food available, however, there is a high
prevalence of kwashiorkor in Benguela and Huila indicating that the diet is of poor quality.
It is recommended that an experienced MSF-B clinician visit other places to determine if pellagra
does or does not exist.11
10
On examination it was found that stunted individuals with the height of 4 and 5-year-old children were found to have the full
dentition of adolescents.
11
Findings
Areas where the population is entirely dependent upon humanitarian aid consisting of un-milled
maize, beans, oil and salt will also develop cases of pellagra. In Bie province the local produce
consists mainly of local maize and beans so there is less opportunity for diet diversification than
elsewhere. Nevertheless, it was from Bie province that the cases of pellagra were reported previously
and where it is presently overt. Even if cases do occur elsewhere, it is likely that Bie province is the
epicentre and has more extensive or severe pellagra than elsewhere.
What are the possible explanations?
First, the farmers interviewed were asked about the crops that they chose to plant. They concurred
that about 70% of their land would be used for maize, 20% for beans and 10% for all other crops
(mainly green leafy vegetables and tomatoes). Although groundnuts grow well in Bie province, none
of the farmers said spontaneously that they would grow groundnuts. When asked directly they said
that they might plant a “few” groundnuts.
Second, people were asked about local dishes and recipes. None of the typical local dishes contained
groundnuts or other major sources of niacin. When asked directly how groundnuts were used, the
respondents all said that they were salted and roasted and taken as a snack and not as part of the
meal. Groundnuts are not used to produce oil (although some people said that sesame seed was used
for oil production). These responses were in marked contrast to those who were born and raised
outside Bie province where there was oil production from groundnuts, the residue being moulded
into a sort of cake that was sliced and eaten. They also made a paste from groundnuts and used it as
a spread. Lastly, groundnuts were frequently added to other dishes, particularly cassava leaf sauce.
Before the war, the diet of the population contained a lot of chicken and other animal products,
including wild meat. It seems that the people in Bie province traditionally had a diet with sufficient
meat to supply their dietary needs for tryptophan, pyridoxine, riboflavin and niacin. With the onset
of the war, the supply of animal products ended but the cultural practices of the people did not adapt
to secure an alternative supply of these nutirents in sufficient amounts. In other areas where there
was traditionally less meat supply, the population may have developed cultural practices, such as
planting and eating groundnuts, which supplied sufficient nutrients to prevent pellagra. Such
anthropological and cultural differences between regions would be a satisfactory and sufficient
reason for the difference in the prevalence of pellagra within the maize consuming
areas of Angola.12
There maybe alternative explanations for which there is no substantive evidence. The local variety of
maize, Umbundo maize, which is favored by the population, is a drought resistant variety with a
lower yield than most varieties. It has neither been analyzed for its niacin content nor for the
proportion of its niacin that is covalently bound to protein and unavailable.13 The soil upon which the
11
A report by UNICEF-Angola in 1992 states: “Pellagra has been reported in the province of Bie, in the villages of Kunje,
Mucumba, Sanono and Camacupa. It is very likely that this nutritional deficiency is very widespread but very seldom diagnosed.
This must be especially so in the areas of concentration of displaced and returnees and the areas which remained isolated during
long periods of time during the war.” See Food Security and Nutrition in Angola. UNICEF-ESARO, UNICEF internal document,
May 1992
12
Historical data was sought from libraries in Lisbon, Portugal, where the records of the Portuguese Colonial medical service are
stored. To date there has been no response to these requests.
13
Four samples of Umbundo maize were secured if such an analysis were to be desired.
12
Findings
maize is grown could conceivably affect the nutrient composition of the seed. Certainly, the soil is
known to be iodine deficient and probably selenium deficient as well (Bie province also has a much
higher prevalence of goitre than elsewhere in Angola).14 The geochemistry of the Kuito region is
very complex with many different soil types in the area. It is unlikely that this could provide a
satisfactory explanation.
3.4. Nutritional Status of Pellagra Patients
Pellagra is not related to the quantity of food taken. It is related to diet quality. Data
demonstrate that normal and overweight individuals can and do get pellagra, in fact they
appear to be more at risk than those who are thin and wasted. Nutrients deficient in pellagra
are type 1 nutrients (niacin, riboflavin, pyridoxine) and do not give rise to wasting unless
there is overt disease that makes the individual sick or anorexic. The prevalence of wasting is
not useful in assessing type 1 micronutrient deficiency. Individuals with pellagra do not
require additional maize rations but micronutrient rich foodstuffs
Kuito has been besieged and from time to time there has been a high prevalence of wasting in the
population. The vast majority of the food eaten by the population is brought in by air. Commodities
consist mainly of maize, beans, oil, sugar, salt, fish and Corn Soy Blend (CSB). Without this food
the population would starve. In Camacupa, where the prevalence of pellagra appears to be much
higher, there is also a very high prevalence of moderate and severe wasting in children and in adults,
particularly in the displaced camps and new arrivals. Wasting (low weight-for-height or muac) is
used as the main criterion for targeting supplemental food rations to individuals and their families.
The prevalence of wasting is also used to call alert to the overall nutritional status of the population.
However, the prevalence of wasting is not very high in Kuito compared to other emergencies. Thus it
is questionable whether the method of targeting of food is appropriate to prevent pellagra and other
conditions arising from a diet of poor quality. To address this question, 209 patients with pellagra
were examined (125 adult females, 49 adult males, 26 children and 9 elderly). The results may seem
surprising. None of the patients with pellagra were wasted or edematous, indeed, many were obese
despite their coming from a besieged city in a war zone (see figure 7 below). Muac values were also
taken from 48 patients with pellagra that were seen in Camacupa during the transect walks. They
confirmed the results from Kuito.
14
Dr David Bernadino, Medical Journal of Angola, and UNICEF Goitre Prevalence Surveys.
13
Findings
Figure 7: Cumulative distribution of MUAC in adult pellagra patients
C u m u la tiv e d is trib u tio n o f M U A C in P e lla g ra
1 00
90
80
Percent of cases
70
60
50
40
30
A d u lt F e m a le
A d u lt m a le
20
10
0
1 80
20 0
220
2 40
26 0
M UA C (m m )
280
3 00
32 0
Note: The percent of patients with values below those shown on the x- axis is
given on the y-axis. None had values below 180mm. Half the cases had a
value of 240 mm (normal +). Some patients were obese.
Collated data emphasise that pellagra is not a disease related in any way to the quantity of food taken.
It is related to diet quality. Data demonstrate that normal weight and overweight people can and do
get pellagra, indeed it would appear that normal-overweight individuals are more at risk of pellagra
that those who are thin and wasted. The nutrients deficient in pellagra (niacin, riboflavin and
pyridoxine) are type 1 nutrients. Deficiency of type 1 nutrients does not cause wasting (or stunting)
unless there is overt disease that makes the individual sick and/or anorexic.15
Pellagra patients do not require additional maize. Indeed additional maize, oil or sugar could
aggravate their condition by displacing more balanced food from their diet. Provision of maize as an
economic transfer is an inefficient way of improving the diet and inspection of markets revealed that
aside from oil and maize there is little other produce available.
15
Certain types of nutrient deficiencies cause the body to respond in different ways. The first response (type 1) is to keep
growing and use up the nutrient in the body, at which point the specific metabolic function that depends on the nutrient declines
and the person becomes ill. The illness has characteristic symptoms, so that a deficient nutrient can be identified and remedied.
Examples of type I nutrients include iron, ascorbic acid, vitamin A, vitamin D, riboflavin, niacin. The second response (type II)
is for the body to stop growing or break down its own tissue to conserve the nutrient in the body. Other type II nutrients are lost
in the process. Examples of type II or “growth nutrients” include potassium, sodium, magnesium, zinc, phosphorous, protein.
Deficiency of one of the type II nutrients gives rise to wasting or stunting.
14
Findings
3.5. Pellagra and Malnutrition
Evidence shows that co-incidentally with the outbreak of pellagra amongst the adults there has been an
increase in the incidence of kwashiorkor in the same population, together with a dramatic increase in deaths
occurring at home. Both kwashiorkor and pellagra are diseases of diet quality. A high prevalence of
edematous malnutrition in an area of operations should trigger an investigation of micronutrient deficiencies.
Since the characteristic skin lesions appear to affect those who are relatively overweight, and both
pellagra and kwashiorkor (the main form of malnutrition in Kuito) are due to consumption of a diet
of poor quality, the relationship between the prevalence of malnutrition and the pellagra outbreak
was examined.
Figure 8: Wasting (WFH <-2 Z) and Pellagra, Kuito
W a s tin g W /H %
(c a m p s c re e n )
16
W a s tin g a n d p e lla g ra , K u ito
case s of
P e lla g ra
100
90
14
p e lla gra-re s ide nt s
80
p e lla gra ID P
12
w a s t in g - o ld ID P
70
W a s tin g - ne w a rriva ls
10
60
50
8
40
6
30
4
20
2
10
0
0
1
2
3
4
5
6
7
8
9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28
W e e k in 2 0 0 1
Note: Prevalence of wasting each week in the established IDPs and newly arrived IDPs. Data form MSF(B)
screening teams. Dark bars show cases of pellagra from Kuito hospital clinic.
There was a sharp peak of wasting in the old IDPs in February and March 2000. This occurred at a
time when there were very few pellagra cases. Wasting is more common in the new IDPs. There was
a marked peak in late April and May 2001. The two groups of IDPs showed quite a different pattern
of wasting. However, in July there was a sudden deterioration in both groups, indicating a general
deterioration in the situation. These data show that there is no clear relationship between pellagra and
wasting. This confirms the earlier finding that wasting (usually due to a type II deficiency) cannot
be used to predict or identify when a population has significant type I nutrient deficiency, such as
pellagra, that gives rise to a major degree of morbidity and may dramatically increase mortality.
Such considerations explain discrepancies between the global acute malnutrition rate and the
15
Findings
mortality rate. It is clear that the prevalence of edematous malnutrition should be reported separately in
surveys in addition to the overall severe malnutrition rate. A high prevalence of edematous malnutrition
should alert the responsible agencies to the probability of widespread type I nutrient deficiency and lead
to programs specifically aimed at improving the quality of the diet rather than simply supplying sufficient
energy and protein. A high prevalence of edematous malnutrition in an area should also lead to
investigation of the presence of pellagra, beriberi, scurvy and other micronutrient deficiencies in that
theatre of operations. Indeed many of those admitted to Therapeutic Feeding Centers (TFCs) in Kuito
showed signs of chronic vitamin C deficiency.
Figures 9.1 and 9.2 show the proportion of cases admitted to the MSF-B TFCs in Kuito by residence and
those due to kwashiorkor. It is clear that the majority of the cases with severe malnutrition in the Bie area
have kwashiorkor. This is the case for both children and adults. The recent deterioration of nutritional
status and increasing deaths occurring at home is primarily due to an increase in the prevalence of
edematous malnutrition. Indeed, between 70% and 80% of all TFC admissions are for kwashiorkor.
These data are total admissions to the TFCs and could not be broken down to tease out admissions from
Kuito IDPs, Kuito residents and those transported from outside the area.
Figures 9.1. and 9.2. Admissions to MSF-B Therapeutic Feeding Centers
TFC admissions, Kuito (MSF(B))
1200
Total Admissions
Kuito Residents
IDP camps
From outside Kuito area
Numbers of patients /month
1000
800
600
400
200
0
Apr-99
Jul-99
Oct-99
Jan-00
Apr-00
Jul-00
Oct-00
Jan-01
Apr-01
Proportion of oedematous cases (TFC) vs pellagra
0.8
100
pellagra cases
TFC- %oedema
90
80
0.7
60
0.6
50
40
30
0.5
20
10
0.4
0
1
3
5
7
9
11
13
15
17
Week 2001
16
19
21
23
25
27
29
Pellagra cases
proportion oedema
70
Findings
Soon after the resumption of hostilities and the opening of the TFC in 1999 there was a high
admission rate. There were a large number of admissions during the first pellagra epidemic in
1999 and this affected both the residents and the IDPs. However during the smaller epidemic in
the summer of 2000, there were very few admissions. Recently there has been a massive
increase in the numbers of patients admitted. This has been mainly due to transfer of patients
from outside the Kuito area, or new IDPs arriving with severe malnutrition. The total admission
data for recent months is thus distorted. There has also been an increase in the admissions from
the other groups, mainly the IDPs.
3.6. Pellagra and Nutrition and Mortality Survey Data
Data support the thesis that there is excess mortality due to widespread micronutrient deficiency of a type
that does not give rise to wasting but which is associated with the edematous form of severe malnutrition.
Nutrition survey data confirm high levels of excess severe malnutrition.
Figure 10 shows the prevalence of moderate and severe malnutrition in the Kuito camps and Kuito
residents in relation to the two standard mortality rate indicators. Data are taken from MSF-B, ICRC
and Concern surveys.
Figure 10: Prevalence of global acute malnutrition (<-2Z) and under -5 mortality rate
G lo b a l A c u t e M a ln u t r it io n ( < -2 Z ) & M o r t a lit y in K u it o
20
14
C am p
T ow n
< 5 M o r t a lit y R a t e
C r u d e M o r t a lit y R a t e
18
12
10
Global m alnutriton %
14
12
8
10
6
8
6
4
4
2
2
0
0
M a r -9 9
J u n -9 9
S e p-9 9
D e c -9 9
M a r -0 0
J u n -0 0
17
S e p-0 0
D e c -0 0
M a r -0 1
J u n -0 1
Mortality rate (/10,000/d)
16
Findings
Figure 11: Prevalence of severe malnutrition and the retrospective crude mortality rate
S e v e re M a lnut rit io n ( < - 3 Z: o e de m a ) & M o rt a lit y - K uit o
5
14
Camp
T ow n
< 5 M orta lity ra te
C rude M orta lity R a te
Se ve re M alnutrition %
4
12
10
3.5
3
8
2.5
6
2
1.5
4
M ortality rate (/10,000/d)
4.5
1
2
0.5
0
0
M ar -9 9
J u n -9 9
S e p-9 9
D e c -9 9
M ar -0 0
J u n -0 0
S e p-0 0
D e c -0 0
M ar -0 1
J u n -0 1
In March 1999, there was a relatively low prevalence of global malnutrition (3% < -2Z), but 1.3%
severe malnutrition. This was unusual. It was mainly due to high prevalence of kwashiorkor. This
was the first indication that there was a particular problem with habitual diet quality in this area of
Angola. Data show an excess of severe malnutrition in all the surveys conducted in 1999. Survey
reports from 2000 and March 2001 reveal that the observed severe malnutrition rate was close to the
theoretical rate. The survey of July 2001, however, again shows an excess of severe malnutrition.
The relationship between the malnutrition and mortality rates is not simple. At all times the mortality
rate has been much higher than expected from the nutrition survey data. Indeed, although the
wasting rate in 2000 did not give cause for alarm, the under 5 mortality rate remained at about
4/10,000/day and the crude mortality at about half this figure. Something other than wasting was
related to these excess deaths. The data from the July 2001 survey shows a crisis situation with
respect to mortality while at the same time showing a relatively modest increase in the wasting rate.
3.7. Pellagra, Morbidity and Mortality
Data from screening teams and health posts show an increasing mortality rate at a time when the
pellagra epidemic was becoming overt. Mortality data show rates that are much higher than one
would expect from the wasting rate. Excess mortality is not attributable to outbreaks of infectious
disease, but there has been an increase in deaths directly ascribed to malnutrition. Thus the pellagra
epidemic is symptomatic of serious nutrient deficiencies in Kuito. In the midst of a confirmed
pellagra epidemic, where case confirmation is confined to characteristic dermatitis, it is reasonable to
suppose that pellagra might be contributing to diarrhea and to the depression and psychological
hardships that accompany the circumstances of IDPs. To investigate this possibility the data from the
MSF-B health posts and screening teams in the camps were examined and compared temporarily
with the onset of the pellagra epidemic of confirmed cases presenting at the hospital.
18
Findings
Figure 12: Total number of consultations at health posts in Kuito
C o n s u lt a t io n s
2500
P e lla g r a
100
O t h e r c o n s u lt a t io n s
C a m p H e a lt h p o s t
p e lla g ra
90
2000
80
70
1500
60
50
1000
40
30
500
20
10
0
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
0
week 2001
Figure 12 shows the weekly total consultations at the health posts in the camps, in relation to the
confirmation of pellagra cases in the hospital. It is clear that there was no increase in the frequency
of IDPs seeking help at the health posts (for whatever reason) with the major increase in the pellagra
cases. Even if the onset of the pellagra was up to two months before the cases presented at the clinic,
there is no relationship. If one assumes that pellagra is causing widespread neurological complaints
or diarrhea one might reasonably have expected there to be an increase in consultations, particularly
as many of the cases had neurological complaints in Kuito. This was not the case. Thus, unless the
depression inhibited the sufferers from seeking help, it would appear that widespread neurological
illness was not a major feature of this outbreak. Attempts were made to obtain data on suicide rates
in the Kuito area as suicide may be a feature of widespread depression. It appears that suicide is
uncommon in the area, but hard data was not obtained.
Figure 13 shows the percentage of consultations for diarrhea in children and adults, for pellagra and
also the hospital cases originating from the same IDP camps, by time. The time frame includes the
end of the 2000 epidemic and the present epidemic.
19
Findings
Figure 13: Morbidity at IDP health centers
Morbidity at IDP he alth ce ntre s
IDP Pellagra (hosp)
Diar <5y
Diar 5+y
pellagra
% consultations
6
120
100
5
80
4
60
3
40
2
IDP pe llagra cas e s (hos p)
7
20
1
0
0
Sep-00
Oct-00 Nov-00 Dec-00
Jan-01
Feb-01 M ar-01 A pr-01 M ay-01 Jun-01
These data are surprising. First, the percent of consultations for diarrhea was surprisingly low,
between 3% and 5% in children and 1% and 3% in adults. The total number of consultations did not
change appreciably during this time so that the absolute number of cases of diarrhea follows the same
pattern as the data presented. The causes of diarrhea in children are much more varied than in adults.
Second, the consultation rate at the health posts in the camps for pellagra is remarkably low, less than
20 in the highest month out of more than 10,000 total consultations. It would appear that the
widespread pellagrous skin lesions are not leading to consultation with the health staff in the camps.
This may be because most of the IDPs consider that these skin lesions are a “part of life”, and not
considered as indicating the presence of an easily curable disease. Most of the IDPs examined did
not consider that they were abnormal in any way, and most were surprised by an interest in their skin
appearance. Third, there is no relationship between the rate of diarrhea consultation and either the
presentation of pellagra at the health posts or at the hospital. Figure 14 shows deaths in the camps by
cause. During the time shown there was an average of 118 deaths per month. However, there has
been a steady increase in the total number of deaths per month in the camps from about 60 in
September 2000 to 180 in June 2001.
20
Findings
Figure 14: Deaths in IDP camps by cause
De ath of IDPs in Camps
% De ath in camp by cause
30
% M alnutritio n de ath
% Diarrho e a de ath
180
to tal re po rte d de ath
160
25
140
120
20
100
15
80
60
10
40
Total re porte d de aths (n)
200
35
5
20
0
0
Sep -00
Oct-00 No v -00 Dec-00 Jan -01
Feb -01 M ar-01 A p r-01 M ay -01 Ju n -01
Changes in the camp population could not account for the increase in reported deaths. The
population of the camps surveyed by MSF-B is about 80,000 so that the observed Crude Mortality
Rate (CMR) is now about 0.75 deaths/10,000/80,000/day. The survey derived CMR for March 2001
was about 1.4/10,000/day and for July 2001 had risen to 4.0/10,000/day. There is almost certainly
under-reporting of deaths to the health posts and over-reporting in the retrospective data collected
during the survey. Nevertheless, it is clear that there has been a steady worsening of the nutritional
status of IDPs since September 2000. The proportion of deaths from diarrhea has risen slightly from
about 10% to 15% of deaths. There was a striking increase in deaths due to malnutrition (increasing
from zero at the end of 2000 to 25% of all deaths by June 2001). While the type of malnutrition
causing death is not formally recorded, it is assumed to be mainly kwashiorkor for two reasons.
First, as noted earlier, 80% of the admissions to the therapeutic feeding centers have kwashiorkor as
the primary diagnosis. Second, deaths due to wasting are usually ascribed, by the relatives and health
workers, to the associated or precipitating conditions such as diarrhea and TB. Indeed, it is likely
that the increment in deaths ascribed to diarrhea may actually be due to the wasting form of severe
malnutrition.
In the camps, kwashiorkor is now the leading cause of death. This deterioration has happened at the
same time as the development of the pellagra epidemic and also with the change in the diet resulting
from the break in the CSB pipeline to Kuito. Both pellagra and kwashiorkor are caused by a very
poor quality diet. It would appear that there is now widespread micronutrient deficiency in Kuito and
that this is leading directly to these deaths. However, the pellagra itself does not seem to be of
sufficient severity to increase the rate of consultation at the health posts. It is unlikely that there are
large numbers of cases suffering from diarrhea or neurological problems without the skin lesions of
pellagra. At the moment, most cases of pellagra are mild. It is unclear why there has been a steady
increase in death rate without there also being an increase in the consultations at the health posts.
This discordance within the camp health data sets indicates that we should examine other sources of
data to support or refute these findings.
21
Findings
In summary, there are three relatively independent lines of evidence that point to a major problem
with the quality of the diet in Kuito.
1. The data from the screening teams and health posts show an increasing mortality rate at a time
when the pellagra epidemic was becoming overt.
2. The TFCs show a marked increase in the rate of edematous malnutrition, which is related to
pellagra in that are both caused by a very poor quality diet.
3. The survey data show an excess of severe malnutrition and mortality rates that are far higher than
one would expect from the rate of wasting. There have not been outbreaks of malaria, cholera,
shigellosis or other major infectious disease epidemics to account for the high mortality rate.
There does not seem to have been a change in the rate of diarrhea during the increase in mortality
rate, but there has been an increase in deaths directly ascribed to malnutrition.
Thus, the pellagra epidemic is symptomatic of serious nutrient deficiencies in Kuito.
3.8. Food Distribution
It is clear from direct sampling of the population that not all the families that should have received a general
and/or supplementary ration did so. There has been an increasing reliance on maize and a decrease in the
amount of blended food and beans in the ration resulting in a poor quality diet. Problems occurred with the
distribution at several levels resulting in a lack of transparency and cooperation and hampering operations.
There are a substantial number of beneficiaries in Kuito. This is shown in figure 15. Figure 16 shows
the official IDP numbers in relation to the beneficiary numbers receiving food from the general
ration. The reduction in the numbers of IDPs in December 2000 is related to the re-validation
exercise that took place at that time. It is expected that the present re-validation exercise will also
reduce the numbers of IDPs by about 40,000. During 2001, about 60% of the IDPs should have been
receiving rations. Although for various reasons it is likely that the distribution was highly uneven in
practice. The “old IDPs” do not receive a general distribution and account for the difference. It is
unclear how they get sufficient food.
A great many families receive food from the special programs for vulnerable groups, these include
Kuito residents. By far the largest group is the families of those in special need (accompanying
family members). A substantial number of moderately malnourished also receive food. Of interest
has been the increasing numbers of children in the Infant Program Centers (PICs) that have been
benefiting from food distributions over the past year (from 3,000 in June 2,000 to 15,000 at present).
The PICs program targets preschool children in the community and is directed mainly at the resident
population.
22
Findings
Data analyzed are from actual reported distributions and not the planning figures. Pipeline breaks
were reported by WFP, although it is not clear why this occurred. However, what is relevant is what
was actually distributed and the relationship to the outbreak of pellagra. 16
There are assumed to be about 80,000 Kuito residents and that this figure is relatively stable. If we
add the 80,000 to the IDP figure to get the total population of Kuito and add the number of
beneficiaries of vulnerable group programs to the recipients of the general rations, we can derive the
data given in figure 17 further below.
Figure 15: Total number of beneficiaries of humanitarian aid
180000
160000
140000
B eneficiaries
vulnerable
IDP-new
IDP-old
all
120000
100000
80000
60000
40000
20000
0
Apr- May- Jun00
00
00
Jul00
Aug- Sep- O ct- N ov- Dec- Jan00
00
00
00
00
01
16
Feb- Mar- Apr- May01
01
01
01
It would be useful to have data going back for 3 years in order to see if the same change in the actual distributed food occurred
at the same time as the other outbreaks.
23
Findings
Figure 16: IDP general distribution (MINARS data)
IDP population
200,000
% rations
100
IDP General Distribution
90
80
160,000
70
60
120,000
50
40
80,000
s
30
20
40,000
IDP population
IDP general
% Receiving
Apr- May- Jun00
00
00
Jul00
Aug- Sep- Oct- Nov- Dec- Jan00
00
00
00
00
01
10
-
Feb- Mar- Apr- May01
01
01
01
Figure 17: Total food distribution
Total population
% rations
Total food Distribution
100
250,000
90
80
200,000
70
60
150,000
50
40
100,000
30
total population
Total rations (IDP+Vul gps)
% pop potentially fed
50,000
20
10
-
Apr- May- Jun- Jul-00 Aug- Sep- Oct- Nov- Dec- Jan00
00
00
00
00
00
00
00
01
24
Feb- Mar- Apr- May01
01
01
01
Findings
Assuming the official figures are correct, there are sufficient rations being distributed to feed about
60% of the total population (residents and IDPs). If the official population figures are inflated (this
is likely to be the case mainly because families that move away are not de-registered) then a higher
proportion of the population is being fed (approx 66%). The food that is being distributed to the
targeted groups is finding its way to the general population and the residents of Kuito, much of it
through the market. As such, a high proportion of the residents of Kuito are receiving food derived
from WFP and it is clear that the quality of that ration will impact directly upon the whole
population. The actual distribution to the families has been assessed by MSF-B. The data for the
coverage among families present in the camps is given in the following table.
Table 1: Families receiving general ration (MSF-B data)
Jan-01
Feb-01
Mar-01
Apr-01
May-01
Jun-01
Jul-01
sampled
168
187
198
206
213
217
220
targeted
153
168
187
198
206
213
217
new arrivals
15
19
11
8
7
4
3
receiving
105
134
166
178
153
71
153
coverage
69%
80%
89%
90%
74%
33%
71%
Note: Figures cited represent families.
Figure 18 shows the tonnage of foodstuff that has been distributed in Kuito. From July 2000 to
February 2001, about 2000 MT have been distributed each month. This dropped to about 1500 MT
from March to May 2001. Although there have been problems with the runway and air transport, the
vast majority of the food transported into Kuito is cereal maize. The percentage of the transport
capacity that has been used for non-maize foodstuffs has decreased from over 30% before June 2000
to about 17% in April/May 2001. This may be due to ruptures in supply of other commodities further
back in the pipeline, but transport capacity cannot be cited as the reason for the poor diet quality.
Although the proportion of maize to non-maize items has fallen steadily, the quality and quantity of
micronutrients in the non-maize commodities is clearly of importance (see figure 19).
Of note is the reduction in the delivery of CSB from more than 250 MT per month to about 50 MT
per month from November 2000. CSB is a rich source of anti-pellagra nutrients. There was a partial
replacement with dried fish, but the quantities will not compensate for the loss of CSB. Dried salted
fish was purchased by WFP and distributed. However, problems with the distribution are such that
much of the fish does not reach the beneficiaries and often runs out fast. Very few families received
the amount of fish written on their cards. The fish does not contain pre-formed niacin, but ‘niacin
equivalents.’ To date the fish has not been analyzed, thus there is no reason to suppose that the fish is
high in niacin.17 From
17
The Angolan government provided funds to WFP which were used to purchase dried salted dish. Niacin in fish is as ‘niacin
equivalents’ not pre-formed niacin. Without addressing the other micronutrient deficiencies, this will not necessarily give rise to
actual niacin in the body. The fish are sun dried which destroys riboflavin. The fish are of a species that have not been analyzed,
as such there is no basis for suggesting that the fish are high in niacin.
25
Findings
April, about two months before the onset of the present epidemic there has also been a dramatic
reduction in the distribution of beans. It is quite clear from these figures that the beneficiary
population has been receiving a higher and higher proportion of their diet from cereal maize and a
much smaller proportion from richer sources of micronutrients.
Figure 18: Total food distributed in Kuito by commodity and proportion of non-maize items.
M T food pr odu c t
T o ta l fo o d d is trib u te d , K u ito (M T )
% N on -M ai z e
3000
35
2500
30
25
2000
20
1500
15
c
1000
10
500
5
0
0
A p r- M a y 00
00
Ju n 00
M a i ze
J u l-00 A u g 00
b e a ns
Sep 00
O c t00
Nov00
o il
Dec00
Ja n 01
Feb 01
csb
M a r01
A p r- M a y 01
01
fi s h
%
Figure 19: Quantities of non-maize items that have been distributed in Kuito.
MT food produ ct
N on-M aize food distribute d, K uito(M T )
3 00
b eans
o il
csb
fish
2 50
2 00
1 50
1 00
50
0
A p r-00
M ay 00
Ju n -00
Ju l-00 A u g -00 Se p -00 O c t-00 N o v -00 D e c -00 Ja n -01 Fe b -01 M a r-01 A p r-01
26
M ay 01
Findings
When the general distribution was observed, it was clear that there was a potential problem with both
the distribution itself and with the manner in which the official planning figures were derived. There
was no list of beneficiaries to receive the food ration. The family member receiving the food first
presented their card where the number was recorded and the amount that should be given written on
the card as if it had already been received. These sheets were then used to derive the official figures
returned to WFP. However, it was clear that there was an insufficient physical quantity of food for
the number of beneficiaries who gathered at the collection point. Whenever an item ran out the
remaining beneficiaries did not receive the item, even though their card was marked that they had
received the food. The data presented therefore represent the maximum that the beneficiaries
received, if there was fair and even distribution of the rations. There was no regular food-basked
monitoring (as is the normal standard practice). It is unclear how such a system of general food
distribution has been allowed to develop and persist, for it cannot be controlled or audited and it is
open to abuse at several levels. Furthermore, it was extremely difficult to get any meaningful
information from the local head of the NGO responsible for the general distribution and attempts to
observe distributions were hampered. Such lack of transparency is regrettable because of the
suspicion thrown, perhaps unfairly, on several people and agencies. It also hinders other agencies
work, since they cannot plan their own programs or interpret the data they are gathering in a
meaningful way. Without clear, complete and authoritative data that is made freely available in a
timely and comprehensible way anything is possible. Indeed, the different agencies are using
different names with different boundaries for the various IDP camps. There is sufficient mutual
suspicion and lack of cooperation to seriously hinder the humanitarian operation in Kuito.
When such a large proportion of the population is being fed, the whole town, residents and IDPs
alike, is clearly dependent upon this aid for their survival. There is insufficient local production to
feed more than a small proportion of the total population. It is likely that the poorer residents and old
IDPs, who are not eligible for the general distribution, are obtaining most of their food from the
imported humanitarian items, by one means or another. They are also likely to obtain the cheaper
food items to which they are accustomed, mainly maize and beans. Such a diet will lead directly to
pellagra.
3.9. Energy and Micronutrients in the Distributed Food Rations
Insufficient quantities of micronutrient rich foods were available in the general and supplementary rations.
Low levels of niacin in the ration and the overall quality of the ration were not adequately tracked to allow
for preventative action. Analysis shows that the pellagra epidemic is related directly to the quality of the
ration distributed to the beneficiaries in Kuito.
General rations: Figure 20 shows the actual (unverified) distribution of energy to the IDP camps by
month expressed in kcal per person per day. The target ration of 2100 kcal/person/day was met
between May 2000 and Feb 2001. There was then a shortfall and in March, April and May, 2001 the
average energy distributed was about 1500kcal/person/day. It is clear that there has been
considerable heterogeneity in the distribution that is hidden by the mean results. In March 2001, five
of the camps only received 500 kcal/person/day in the general distribution.
27
Findings
Figure 20: Energy in the general distribution by IDP camp
E n e rg y in G e n e ra l D is trib u tio n b y c a m p
2500
Kcal/pe rson/d
2000
1500
A n d u lo
Ca ma c u p a
Ca mb a n d u a
Ca t a b o la
Ch ic a la I
Ch ic a la II
Ch in g u a r
Ch ip e t a
Ch is s in g u i
K u e mb a
K u n h in g a
N h a re ia
T ru mb a
Ungundo
1000
500
0
A p r00
M a y - Ju n -00 Ju l-00 A u g 00
00
S e p - O c t -00 N o v 00
00
D e c - Ja n -01
00
Feb 01
M a r01
A p r01
M ay 01
The intake of niacin falls well below the recommended amount (figure 21). The heavy dotted line
shows the recommended intake derived from the Institute of Medicine (IOM) standards.18 The level
of niacin in the distributed rations never reached the IOM recommended amounts. Thus, it is
expected that the stores of niacin in the population would have been depleted and that the proportion
of the population with a requirement approaching the dietary recommended values and those with a
raised requirement due to disease or other stress, would have been subject to pellagra during this
time. Nevertheless, the general distribution was above the threshold of overt pellagra derived from
experimental subjects from April 2000 to October 2000. However from November 2000, the level
was very low and from April 2001, there was a further major deterioration in both the absolute
amount of niacin delivered and also the quality of the ration.
The graphs documenting the outbreaks of pellagra and the distributed commodities and levels of
niacin in the ration are presented separately to avoid confusing overlay; however, there is a clear
relationship. There is an expected delay of about two months between beginning a low niacin diet
and developing a clinical picture. For populations with low stores it will be quicker. There is also
typically a delay of about two months in patients presenting with illness. These factors combined
lead to the start of an epidemic shortly after a change in ration and reach a peak 2-4 months later.
These analyses show that an outbreak of pellagra occurred about two to four months after the
problem with the food basket. This could have been anticipated if ongoing analysis had taken place.
Preventive measures could then have been taken.
18
Data for each camp are available on request. They show heterogeneity of a similar magnitude to the energy distribution.
28
Findings
Figure 21: Niacin in the general distribution
n ia c in
m g /1 0 0 0 k c a l
8
B2 & B6
m g /1 0 0 0 k c a l
1 .2
N ia c in in g e n e r a l d is t r ib u t io n
7
1
6
0 .8
5
4
0 .6
3
0 .4
2
0 .2
1
0
N ia c in m g /1 0 0 0 k c a l
A p r- M a y00
00
Jun00
J u l00
A ug00
B 2 m g /1 0 0 0 k c a l
S ep00
O c t00
N o v- D e c 00
00
B 6 m g /1 0 0 0 k c a l
Ja n01
F eb01
M a r01
0
A p r- M a y01
01
Supplementary rations: A large proportion of the population was receiving supplementary food
rations. The food basket given in these programs was not the same as the general distribution.
Figures 22 to 24 show the energy and niacin in these rations in a similar format to the data given for
the general distribution. The energy given to the vulnerable groups has never reached the target
amount of 2100 kcal. For most of the past 6 months, it has averaged about 1500kcal. Figure 23
shows the intake of niacin and other micronutrients in the vulnerable groups. It is clear that the
intake of niacin fell dramatically in November 2000 and has not recovered since. One might have
expected that the ration given to the vulnerable groups would have been of a much higher quality
than the general distribution. This was not the case with respect to niacin. Indeed, the quality of the
ration given to the vulnerable groups is of the same order as that given to experimental subjects
designed to study the effects of niacin deficiency. These vulnerable group rations, unlike the general
distribution rations, are distributed throughout the Kuito area to feeding centres, the elderly, orphans,
and TB patients. Figure 24 shows the rations that have been given to the families of patients with
pellagra specifically. The intake for these vulnerable families does not even reach the recommended
allowances for normal people.19 They are quite inadequate to provide sufficient amounts to replete
the body stores of niacin or to treat incipient pellagra. The niacin density in the ration should be
7.2mg/1000kcal, in fact it was always below 6mg/1000kcal, and in November 2000, there was the
situation where a frankly pellagragenic ration was given to families who were already at very high
risk of pellagra.20 This may have been detrimental. There are no data from the pellagra clinic to
determine if more than one member of a family was enrolled in the clinic.
19
Healthy experimental subjects in the USA taking clearly defined experimental diets developed signs of pellagra in about 2-3
month when a diet of less than 4mg/1000kcal or 8 mg absolute was taken.
20
Nutrient density is expressed as amount of nutrient required per 1000kcal of diet. This analysis is quite straightforward and
could easily be programmed into Excel or other spreadsheet to give an ongoing picture for most of micronutrients. This is not
done anywhere in the world, even where there are recurrent outbreaks of micronutrient deficiency.
29
Findings
Figure 22: Energy in supplementary rations
E n ergy g iven
2500
kcal /person/day
2000
1500
1000
p ellagra-fam
500
Vul gro up s
0
A p r-00 M a y - Ju n -00 Ju l-00
00
A u g - Se p -00 O c t-00
00
N o v - D e c -00 Ja n -01 Fe b -01 M a r00
01
A p r-01 M a y 01
Figure 23: Intakes of B2, B6 and Niacin mg/d in supplementary rations
B 2 & B 6 mg/d
2.5
N iacin mg/d
15
Inta k e Vulne ra ble g ro ups
13
2.0
11
9
1.5
7
1.0
5
3
0.5
1
B2-mg/d
B6-mg/d
Niacin mg/d
-1
0.0
A pr-00
M ay-00
Jun-00
Jul-00
A ug-00
S ep-00
O ct-00
30
N ov-00
D ec-00
Jan-01
F eb-01
M ar-01
A pr-01
M ay-01
Findings
Figure 24: Intake of B2, B6 and niacin mg/d in rations to families of pellagra patients
B2 & B6 mg/d
Niacin mg/d
Intake Pellagrin Families
15
2.5
13
2.0
11
9
1.5
7
1.0
5
3
0.5
1
B2 mg/d
B6 mg/d
Niacin mg/d
0.0
-1
Apr-00
May-00
Jun-00
Jul-00
Aug-00
Sep-00
Oct-00
Nov-00
Dec-00
Jan-01
Feb-01
Mar-01
Apr-01
May-01
3.10. Food Security and Agricultural Activity
Prevention of pellagra is achieved primarily through diet diversification using perishable or semiperishable food items. These can only be reasonably produced locally. Clearly the only way for the
population to regain food security is to cultivate sufficient land. Groundnuts are particularly valuable in
pellagra prevention and should be actively promoted. Until the total land under cultivation can be
increased, there will remain a need for continued humanitarian assistance.
Market prices: As people get poorer, the variety in the diet is restricted until little more than the
staple diet is eaten. The prices in the market are shown in figure 25. The household food economy
approach is useful to determine what choices are likely to be made in food purchase by the residents
and IDPs who are not eligible for direct aid. Most of the population is made up of the poor (Group 1)
and their income has not kept pace with the increasing costs. The following is extracted from a
recent report on food security in Kuito.21
“A population’s food security is linked to both availability and also to access which is
closely allied to the cost of those products. From the transect and detailed interviews
it is clear that income may have increased slightly for Groups 1 and 2, with
indications that Groups 3 and 4 are earning more than before.” But the food prices
have increased substantially in this time. So that: “In this environment, those
members of the lower income groups will inevitably find it more difficult to purchase
food now than they would have done six months ago which may, in part, account for
their increasingly poor nutritional status.”
It is likely that the families with a decreasing budget to devote to food have increased the proportion
of maize purchased and decreased the purchase of other items that will provide niacin. It is clear that
21
Food Security Assessment, Kuito (draft), 14-23 July 2001, Mark Wright, Save the Children (UK).
31
Findings
those who developed pellagra were obtaining sufficient maize to meet their energy needs as shown
by their normal or high body weight, but this has been at the expense of developing micronutrient
deficiency. Clearly the only way for the population to regain food security is to cultivate sufficient
land with a diversification of products that will ensure sufficient availability of all essential nutrients.
Those who do not cultivate enough themselves will need the ability to acquire the food by redistribution. Thus they must have the purchasing power.
The critical point is that the items, which can be stockpiled, warehoused and shipped, are limited to
non-perishable dry items such as cereal, beans, oil and dry food blends. Such a diet over time will
lead to micronutrient deficiency. Prevention is achieved by diet diversification using mainly
perishable or semi-perishable food items. These can only be realistically produced locally.
Therefore there needs to be sufficient land available for the crops to be grown in sufficient quantity
for the local market price to be low enough to ensure a reasonable exchange for non-perishable food
items. Data on market prices exists; however, no data on price elasticity was available to make the
sort of supply/demand price calculations necessary. FAO could undertake such an analysis.
Figure 25: Market prices in Kuito per 1000 kcal
M a rk e t P rice s K u ito p e r 10 00 ka l (2 00 0/2 00 1)
7
C orn f lou r
6
B ean s
O il
Kw aza p e r 1000kcal
5
S ugar
K w z :U S $ 0 . 1
4
3
2
1
0
Ja n
'0 0
F eb
Mar
Apr
May
Ju n
Ju l
Aug
Sept
O ct
No v
Dec
Ja n
'0 1
F eb
Mar
Apr
May
Ju n
Note: The prices of commodities in Kuito. Data are expressed as Kwanza to purchase 1000kcal (rather than as
weight). The average person will need to eat 2100 kcal/day. The exchange rate to US$0.1 is also given. The price
of 1000kcal from maize has remained at about US 8cents, rising in terms of the Kwanza with inflation. The other
commodities are more than twice the price of maize. There was very little fish in the markets.
Insufficient total land in production: For a total population of about 250,000, there is a requirement
of 145MT of food per day or 53,000MT per year. The yield of maize is about 0.5MT/hectar, beans
0.4MT/hectar, groundnuts 0.3MT/hectar, and millet/sorghum 0.6MT/hectar. These yields in Bie
province are lower than elsewhere (Huambo is achieving 0.7MT/hectar), but without considerable
agricultural input and extension the yield is unlikely to increase. There are no assessments available
for post-harvest losses which have not been factored into the calculation, but can be very substantial
(up to one third of a crop). Nevertheless, it is clear that there will need to be about 130,000 hectares
producing food in the Kuito area (assuming average yield of 0.4MT/hectar of mixed crops with 10%
32
Findings
post harvest losses) for the area to become self sufficient in a variety of crops. At the moment about
24,000MT of humanitarian aid is being flown into Kuito each year. This appears to be maintaining
the energy balance of the population, so that the local production can be assumed to be somewhere
around 30,000 MT per year (mainly of maize and beans and consumed by the growers). Thus, there
needs to be an increase in the food-producing land to make good this shortfall. This represents about
60,000 hectares of new land that has to be brought into cultivation. This can be through a mix of
larger scale units and family cultivation.
In terms of the ability of the poor to acquire the means of obtaining their own food, through paid
work, agricultural labour and growing their own crops it is important for the individual families to
have access to their own lands. In particular, the very large numbers of IDPs in the Kuito area will
remain dependent upon humanitarian aid until they have access to land and seeds. The average
family in Kuito has 1.8 adults and 3.6 children, and will require about 90kg of mixed food per month,
or 1.1MT per year. This would require cultivation of about 3 hectares per family. At the moment,
the average land allocation to IDPs is 0.5hectar, which will grow enough food for the typical family
for between 2 and 2.5 months. They need to rely on resources from elsewhere to feed themselves for
over 9 months per year. Until the total area under cultivation is increased and the land is distributed
more equitably, there will remain the need for continued humanitarian assistance on a large scale.
Military activity: The military activity of the FAA is displacing people from their land. It should be
recognised that this is the primary cause of the influx of IDPs arriving in the government held area.
The humanitarian community is feeding them. The military activity is likely to continue. It appears
that part of the strategy is to maintain an “empty area” of land around the government held area as a
cordon sanitaire. This makes sense militarily, however it deprives the swollen population of the
means of becoming self-sufficient in food. This has now reached the stage where pressure must be
brought to bear on the administrators of Bie province to release additional land.
Crop diversification: The seeds distributed last year (cropped this year) were dominated by maize
and beans. There has been almost no groundnut seed distribution and very little vegetable seed.
None of the seed and tools programs have consulted with nutritionists to determine what mix of
seeds would be appropriate to provide a reasonable balance to the diet, particularly in terms of
micronutrients. This lack of nutritional expertise within the decision making process of seeds and
tools programs is folly. It is difficult to address the question of the preventing pellagra when the
crops grown are largely confined to maize and beans, the same commodities that are being imported
as humanitarian aid. While these products dominate the markets, residents and IDPs will be equally
vulnerable to pellagra and other diseases of diet quality. CARE, Concern, Africare and ICRC
distributed seeds to about 38,000 families last year. This year there will be better diversification of
the seeds distributed. For example, Concern has ordered kalahari corn, caricoca bean, mucunde bean,
groundnut, pumpkin, headed cabbage, green-leaf cabbage, galecian cabbage, roma tomato, texas
onion, lettuce, sweet potato and cassava. These are all important and a vast improvement on maize
and beans. Other annual crops that could usefully be grown in Bie province include soya bean,
sunflower, sesame and chilli pepper. Most of the seeds that are distributed by NGOs are imported by
EUROAID. The results of seed diversification will take some time due to the time lag between seed
procurement and an edible crop. However it is unlikely that there will be much impact from the
change in the seed distribution without more land available to plant the seeds. Groundnuts are a
particularly valuable source of niacin and should be actively promoted.
33
Recommendations
4. RECOMMENDATIONS
4.1. Major Recommendations
It is recommended that there should be a comprehensive strategy to address the problem of
micronutrient deficiency in Bie province. Immediate actions will be relatively expensive, but will
reduce morbidity and mortality. These actions should be viewed as an expedient to deal with the
present situation. The subsequent strategies should be in place to prevent a fourth epidemic from
occurring next year. Once in place these strategies would negate the need for the more expensive
short-term interventions. Some solutions will take several years to fully implement, however, it is
critical that these strategies are started now in order to achieve a sustainable solution within several
years.
Immediate Actions to Reduce Morbidity and Mortality
Improve the quality of the general ration
The general food basket that is distributed by WFP should be changed to provide at least the
recommended allowance of niacin riboflavin, pyridoxine and tryptophan. In calculating the niacin in
the diet, a correction factor for the availability of niacin from maize should be made in the basic
calculation (only one third of maize niacin is available). Improvement in the amount of niacin in the
food basket could be achieved either by increasing the quantities of fortified blended foods (such as
CSB, ICSM or CSM) purchased and distributed and/or by purchasing and distributing groundnuts in
the general distribution. Groundnuts are grown widely in southern Africa, including within Angola
and regional provision should be possible. While groundnuts are high in pre-formed niacin and will
help prevent pellagra specifically, provision of groundnuts will not impact on the mortality rate
which is almost certainly due to widespread micronutrient deficiency. Thus a combination of a small
amount of fortified blended food and a small amount of groundnuts per person/day is preferable.
Since groundnuts are not widely eaten in Bie, there should be accompanying education campaign
providing advice on storage and preparation at household level.
Improve the quality of supplementary rations
The food basket for the vulnerable groups needs to be revised. In particular, the ration given to the
pellagra patients needs to be changed so that they are not given maize, beans and oil, but have most
of their ration composed of a modest amount of fortified blended food alone (120g/person/day). The
rationale for this is that pellagra patients do not need additional energy but require micronutrient rich
foods. The families of patients in therapeutic feeding centers should also have a diet particularly rich
in micronutrients as the dominant form of severe malnutrition is kwashiorkor, which is also a disease
caused by a diet of poor quality. The technical changes in the food basket should be made in
consultation with Dr Rita Bhatia, the head of nutrition WFP, Rome.
Encourage diet diversification
The above recommendations do not address the nutritional needs of the residents or old IDPs
directly. It is likely that an increase in the overall importation and distribution of niacin rich products
will improve the situation in the IDP camps, however, there will also need to be a measure of
34
Recommendations
“redistribution” through trading which may help the resident population. Such trading should not be
discouraged, since it can lead directly to diet diversification. In addition, education on diet
diversification is important. This could take place through existing health and feeding programs in
both IDP and resident communities. Simple, feasible, practical messages should be developed.
Where possible, collaboration with development programs (DAP programs) should be sought to
ensure harmony and promotion of messages.
Explore market interventions to address micronutrient deficiencies
Opportunities for direct market intervention in Kuito should be explored in order to assess the
feasibility of providing low price, niacin rich foods through the market to those who mainly purchase
food. The possibility of monetizing a portion of blended food and other micronutrient rich foods
should be further investigated.
The traditional way of cooking in Angola, and most of Africa, is to cook a sauce and add it to the
staple at the time of serving. Rather than import a complete food, it would be more economical and
efficient to attempt to improve the quality of the sauce. This could be done by fortification of a
condiment (condiments are nearly always added to the sauces prepared at home, and food will be
traded in order to purchase condiment in the marketplace). There is a condiment, fortified with antipellagra nutrients, produced for this type of situation by Nutriset. The trade name for this condiment
mix is “QB-mix.” It will cost somewhere in the region of US$3/kilo. To improve the diet to a level
that prevents pellagra and other micronutrient deficiencies requires that an average of 3 to 5 grams of
the condiment be added to food consumed by one person each day. The cost of this condiment is
thus about one cent per person per day (without transport costs). It is recommended that UNICEF
purchase a consignment of about one metric ton of QB-mix. This should be sold through the market,
at cost, with the transport of the first test consignment to be met by UNICEF. The popularity,
acceptability and use of the condiment should be monitored carefully since this product is still in the
trial phase. The nutritional status of a sample of the population showing signs of mild pellagra as
well as those without pellagra should be followed. If this transpires to be a viable and cheap solution
to the micronutrient problem then the program should be extended and other manufacturers
(including local production) encouraged to produce similar products in order to achieve a minimum
price. The shelf life of the product is several years. If this proves successful, it would be a cheap and
effective strategy that would limit the need for blended foods.
Seeds and small animal production
Seeds that are ordered and distributed by agencies involved should result in a diet that is adequate
and balanced. Annual crops that could usefully be grown in Bie province include groundnuts, soya
beans, sunflower, sesame and chilli pepper. However it is doubtful that there will be a major impact
from seed distribution alone without more land being available on which to grow the seeds (see
below). There should be encouragement of re-establishment of local production of small animals
such as chickens or guinea pigs. While animal protein is culturally appropriate it should be noted that
the conversion of plant food into animal food is an inefficient process and requires a substantial
amount of grain. This is a challenge to be overcome in a region with an overall food deficit. Thus this
strategy should be further explored and tested for viability. FAO should take the lead on this.
35
Recommendations
Strategies to Prevent Further Epidemics and Address the Micronutrient Problem
Milling and fortification of maize
Imported maize should be milled and fortified before it is transported to Kuito. Such fortification of
a staple food that is eaten by virtually everyone is standard practice in many countries and is the only
sustainable way of ensuring adequate nutrition in the present situation. The milling and fortification
should take place in Lobito, the port of entry for shipments of maize. Milling capacity exists
according to an assessment made by the local WFP staff. The micronutrients that are used for the
fortification should not only prevent pellagra but also other micronutrient deficiencies that occur
under the conditions found in Bie province. The micronutrient mix should include niacin, riboflavin,
pyrodoxine, iron, zinc, vitamin C and antioxidants (such as vitamin E and selenium). Installation of
the fortification equipment and possible upgrading of the milling capacity in Lobito is not only as an
mechanism for addressing the immediate micronutrient deficiencies in Bie province, it is also
infrastructure support to Angola and supports national capacity building to respond to the nutritional
needs of the population. It is clear that the end of military activities in Bie province is not yet in sight
and that without a political settlement or military victory, humanitarian assistance will continue for
the foreseeable future. At some time in the future it is likely that some other area will also experience
military activity, insecurity and renewed displacement. A technical advisor, experienced in food
technology, milling and fortification, should conduct a feasibility assessment. A cost analysis
should also be made. This should be coordinated through the office of WFP in Rome where the
nutrition section has experience with implementation of a similar program to address the previous
pellagra epidemic among refugees from Mozambique in Malawi. A cost analysis should also be
undertaken. The Government of Angola should take the lead on the milling with technical assistance
from WFP and assistance from UNICEF on micronutrient fortification.
Land allocation
The allocation of additional land to the displaced population and the growing of a wide variety of
crops are critical to ensure food security and diet diversity in the longer-term. The quantity of locally
produced food will determine its market price and the ability of the poor to purchase a diversified
diet. Whilst the quantity produced is so much less than the need, the price will remain high and the
population will depend upon imported non-perishable food items that are associated with pellagra.
An additional 60,000 hectares should be brought into food production in the area immediately around
Kuito. This additional land should be mainly distributed in parcels of about 3 hectares to give a
viable land area to a family (at the moment the land distributed can only be viewed as “supplemental
gardening”). A multi-agency high level delegation should approach government officials to negotiate
such a distribution. It will be necessary to identify land that is not mined or has already been demined. It is clear that the fear of mines prevents much useful land from being used, whether or not it
is mined in reality. It is also the reason given for the non-distribution of land, whether or not this is
in fact the case. It is equally clear to military strategists that the maintenance of an empty area
around the secured territory is a military expedient. Further, there is a reluctance to allocate land to
families who may well have family members still active on the other side of the front and who could
give succour or resources to UNITA forces. Although this argument has weight from the
government’s point of view, it is being carried out to a level where the population is suffering major
and widespread nutritional disease, and the time has come for representation to be made to ease the
policy.
36
Recommendations
4.2. Further Recommendations
•
There should be a survey in the Kuito area to determine the true prevalence of pellagra. A survey
should be made in Huambo and other maize eating areas (such as Benguela and Huila) to determine if
pellagra is endemic in those areas as well as in Kuito.
•
The food being distributed through WFP should be analyzed. In particular the local dried and salt
fish has not been analyzed and is not listed in any food-composition tables. The nutrients in the fish
being distributed have been assumed. However, it is likely that the riboflavin content has been
overestimated as this vitamin is readily destroyed by sun drying. The Umbundo maize should be
analyzed.
•
The organization of the general distribution needs to be overhauled and tested methods and
management systems instituted. There must be transparency in the distribution of food and the data
freely and regularly distributed to all involved, including the other UN agencies, government, NGOs,
donors and their technical advisors. There should be regular food-basket monitoring of the general
and other distributions.
•
New software should be developed to allow immediate and ongoing monitoring of the distribution of
a range of essential nutrients in the food-basket and not just energy and protein, as is the case at the
moment. Nutrients should be expressed as nutrient density (amount of nutrient/1000 kcal). This
analysis could be easily programmed into a spreadsheet to give an ongoing picture for most of the
micronutrients. It is difficult to see how non-nutritionally trained technical officers, logisticians,
economists, managers and decision makers can formulate effective programs unless data is presented
in an easily consumed and digestible way. In order to create the graphs presented in this report many
detailed calculations had to be made (and some assumptions about nutrient composition of the
products in the absence of analytical data). Judgements could not be reached until these analyses had
been made, inspected and interpreted.
•
There should be training and a raising of awareness of micronutrient deficiency among WFP,
UNICEF, NGO, and MINARS staff. For example, targeting of food aid is frequently based on
anthropometric surveys, yet many are unaware that anthropometric surveys do not give any
information about the presence or absence of one or many type I nutrient deficiencies that will cause
disease and increased mortality rates. The level of type I malnutrition can be very high and cause
significant mortality (for example form pellagra, scurvy, folate, iron, iodine or vitamin A deficiency)
while the prevalence of moderate or severe wasting reported in surveys is modest and not cause for
alarm.
•
The names of the camps and their boundaries used by the different agencies should be harmonized
and there needs to be much more efficient co-operation and co-ordination.
•
A proper anthropological study could usefully be made in Bie province to determine if the qualitative
data collected on culinary practice and cropping preferences is accurate. This would also assist in
determining appropriate educational messages.
•
Data on edema (kwashiorkor) should be clearly reported, as well as data on wasting and total severe
malnutrition. It should be broken down by resident/newIDP/oldIDP/new arrival-not-yet-registered.
Kwashiorkor should be recognized as a type I micronutrient deficiency disease. No responsible
program officer should be unaware of the modern thinking about this disease and continue to hold
that it is due to protein deficiency.
37
Appendix 1
Appendix 1:
Metabolic Considerations in Niacin Metabolism
Figure App-1.1. shows the biochemical steps in the conversion of tryptophan into niacin. Although at
first it appears complex, it is this pathway that explains why pellagra is a multi-nutrient deficiency
disease.
Figure Appendix 1.1
The steps involved are conversion to kynurenine, which is hydroxylated to form 3-hydroxy-kyenurenic
acid (3-OH-Ky), in a riboflavin dependent step. Then alanine is removed to form 3-hydroxy-anthranilic
acid (3-OH-AA): this is a pyridoxine dependent step. The 3-OH-AA has its ring oxidatively opened with
an iron dependent oxygenase to give ACS. ACS is at a branch point in metabolism. It can either be
converted to niacin (with quinolinic acid as an intermediate), non-enzymatically converted to picolinic
acid or to acetyl-CoA via aminomuconic semialdehyde.
Riboflavin is the cofactor for the conversion of kynurenine to 3-OH-Ky. It is unclear in humans how
sensitive this step is to riboflavin deficiency.
Pyridoxine is involved at four points in this metabolic pathway. For the formation of 3-OH-A and also to
form the excretory products, kyenurenic acid, anthranilic acid and xanthuneric acid. However, the step
which forms 3-OH-AA is sensitive to dietary pyridoxine deficiency whereas the other steps are many
times less sensitive.
Iron is involved in the enzyme that converts 3-OH-AA to ACS. It is noteworthy that virtually all patients
with pellagra also have iron deficient anaemia.
38
Appendix 1
Zinc is also probably involved, possibly as an essential factor for pyridoxal phosphokinase. At any rate,
pellagra patients have a low plasma zinc status and zinc supplementation increased their excretion of
nicotinic acid metabolites.
Tryptophan itself can be limiting. This occurs classically with inborn errors of metabolism where there is
loss of this amino acid in the urine (Hartnup disease) or with excess tryptophan consumption for other
pathways (Carcinoid syndrome). Both these conditions can present with the typical features of pellagra,
even when the niacin intake is at the recommended daily allowance. This demonstrates that humans are
dependent upon the metabolic conversion of tryptophan into niacin to satisfy their metabolic
requirements.
The metabolic requirements for niacin are much higher than the dietary requirements. Thus, any
deficiency of pyridoxine, tryptophan or the other components can lead to niacin deficiency even when
there appears to be an adequate niacin intake.
The drug isoniazid, which is used widely for the treatment of tuberculosis, inhibits pyridoxyl phosphate
and can prevent the conversion of tryptophan to niacin.
When computing the “total niacin equivalents” of a diet, it is conventional to add the tryptophan intake,
divided by 60, to the preformed niacin intake. This convention has been followed in the calculations for
this report. However, where there are deficiencies of any of the essential cofactors, the conversion will be
much less efficient. There is another consideration. The conventional factor of 60 as the efficiency of
tryptophan to niacin conversion is actually the experimental average of tests in humans of the effect of
dietary tryptophan on the excretion of nicotinic acid metabolites. There was, however, a very wide
individual variation in the efficiency of this process in experimental individuals that were otherwise
nutritionally complete. The variation was plus or minus 30%. In any normally nourished population
therefore, there will be individuals who are much less efficient than the 60:1 ratio that has here been used.
These individuals will be particularly susceptible to pellagra. Such a variation could underlie why some
individuals succumb whereas others, ostensibly on the same diet, do not develop pellagra.
It has repeatedly been found that females of reproductive age are more at risk of pellagra in an epidemic
situation. This may be because of the effect of female sex hormones on the relative activities of the
enzymes leading from the metabolic branch point at ACS. Both enzymes appear to be more active in the
female, but PAC, the enzyme that converts ACS along the acetyl-choline pathway, is activated to a much
greater extent than the enzyme leading to niacin. Thus, it may be that there is less conversion because of
diversion at this metabolic branch point.
39