Outbreak of Aflatoxin Poisoning --- Eastern and Central Provinces, Kenya

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Outbreak of Aflatoxin Poisoning --- Eastern and Central Provinces,

Kenya, January--July 2004

In May 2004, CDC Kenya, trainees of the CDC-supported Field

Epidemiology and Laboratory Training Program (FELTP) in Kenya, the

World Health Organization, and CDC were invited by the Kenya

Ministry of Health (KMOH) to participate in the investigation of an

outbreak of jaundice with a high case-fatality rate (CFR) in the

districts of Makueni and Kitui, Eastern Province. Preliminary

laboratory testing of food collected from the affected area revealed

high levels of aflatoxin, suggesting that the outbreak was caused by

aflatoxin poisoning, as was a previous outbreak in the same area in

1981 (1). In the United States, aflatoxin concentrations are limited

to 20 parts per billion (ppb), a level also adopted by Kenyan

authorities. The 2004 outbreak resulted from widespread aflatoxin

contamination of locally grown maize, which occurred during storage

of the maize under damp conditions. Urgent replacement of the

aflatoxin-contaminated maize with noncontaminated maize proved to be

a critical intervention; however, as of July 21, a limited number of

new cases continued to be detected. This report summarizes the

preliminary results of the outbreak investigation. Aflatoxin

poisoning likely will continue to be a public health problem until

culturally appropriate storage methods for dry maize are implemented

by the local population. In addition, enhanced surveillance for

human aflatoxin poisoning and testing of commercially sold maize for

aflatoxin levels will lead to long-term improvements in public

health.

Joint KMOH and CDC teams conducted patient interviews and reviewed

medical records dating back to January 1, in three health facilities

in the Makueni and Kitui districts. Additional case finding was

conducted through similar patient interviews and retrospective

record reviews in seven health facilities in adjacent districts of

Eastern Province (Machakos, Embu, Mbeere, and Mwingi districts) and

Central Province (Thika district) and at Kenyatta National Hospital

in Nairobi (Figure 1). Large-scale active surveillance occurred from

early May to late June. As of July 21, three health facilities in

Makueni and Kitui districts continued to be monitored for new cases.

A convenience sample of 20 patient households was visited to assess

the occurrence of jaundice in nonhospitalized household members and

to inspect food quality and storage. In this investigation, a case

of suspected aflatoxin poisoning was defined as a case of acute

jaundice that occurred after January 1, in a resident of Eastern or

Central Province or a case diagnosed at Kenyatta National Hospital

in a patient who was not known to have chronic liver disease or any

other cause of jaundice.

As of July 20, a total of 317 cases had been reported, with 125

deaths (CFR = 39%). An increase in case reports began in the third

week of April, with new cases continuing to occur through mid-July

(Figure 2). Of the 308 patients for whom age data were available, 68

(22.1%) were aged <5 years; 90 (29.2%) were aged 5--14 years, and

150 (48.7%) were aged >15 years. Of the 317 total patients, 178

(56.2%) were male, and 280 (88.3%) resided in four districts:

Makueni (148 [46.7%]), Kitui (101 [31.8%]), Machakos (19 [6.0%]),

and Thika (12 [3.8%]). The remaining 37 (11.7%) patients had

aflatoxicosis diagnosed at Kenyatta National Hospital in Nairobi or

at health facilities in Embu, Mbeere, or Mwingi districts. CFR was

significantly higher in Makueni district (CFR = 49.3%) than in Kitui

district (CFR = 23.7%) (CFR ratio = 2.1; 95% confidence interval

[CI] = 1.4--3.1).

Preliminary results from a case-control study that compared 40 case-

patients with 80 well controls matched by village in Makueni and

Kitui districts demonstrated a statistically significant association

between the development of jaundice and several risk factors or

markers, including 1) reported consumption of cooked maize kernels

(odds ratio [OR] = 8.0; 95% CI = 1.7--37.1), 2) reported possession

of homegrown maize that was discolored or visibly contaminated with

mold (OR = 5.9; 95% CI = 1.9--18.2), 3) consumption of homegrown

maize (OR = 3.0; 95% CI = 1.0--8.8), 3) storage of damp maize (OR =

3.5; 95% CI = 1.2--10.3), 4) inside storage of maize rather than

outside granary storage (OR = 12.0; 95% CI = 1.5--95.7), and 5)

reported deaths of dogs or livestock (OR = 3.3; 95% CI = 1.2--9.1).

Food samples collected from household visits during May 10--19

included maize flour, maize grains, dry maize cobs, muthokoi (i.e.,

maize in which the outer hulls have been removed), millet, sorghum,

and beans. A total of 31 samples were tested by the Kenya National

Public Health Laboratory Services, and 15 had >20 ppb aflatoxin B1

(range: 20--8,000 ppb).

A representative survey of maize products from agricultural markets

and outlets (Figure 3) in Makueni, Kitui, Thika, and Machakos

districts was conducted to assess the extent and magnitude of

aflatoxin contamination in the sampled maize. Preliminary results

indicated widespread, high-level aflatoxin contamination. A total of

182 (53.2%) of 342 samples had >20 ppb of aflatoxin. In addition, a

substantial percentage of samples from each district had aflatoxin

levels >1,000 ppb: Makueni (12.1%), Kitui (9.6%), Thika (3.9%), and

Machakos (2.9%).

The government of Kenya is providing replacement food in the most

heavily affected districts: Makueni district (population: 771,545)

and Kitui district (population: 515,422). Residents of affected

districts have been advised to avoid consumption of maize or other

foods suspected to be moldy or appearing discolored. In addition,

food inspections by public health authorities are being conducted,

and suspect food is being seized, destroyed, and replaced.

Surveillance for possible aflatoxin poisoning in humans has been

extended to other parts of Kenya by MOH, and aflatoxin screening of

maize has been increased.

Reported by: J Nyikal, A Misore, C Nzioka, C Njuguna, E Muchiri, J

Njau, S Maingi, J Njoroge, J Mutiso, J Onteri, A Langat, IK Kilei, J

Nyamongo, G Ogana, B Muture, Aflatoxin Task Force, Kenya Ministry of

Health; P Tukei, C Onyango, W Ochieng, Kenya Medical Research

Institute; C Tetteh, S Likimani, P Nguku, T Galgalo, S Kibet, A

Manya, A Dahiye, J Mwihia, I Mugoya, Kenya Field Epidemiology and

Laboratory Training Program/Kenya Ministry of Health. J Onsongo, A

Ngindu, World Health Organization Kenya Country Office. KM DeCock, K

Lindblade, L Slutsker, P Amornkul, D Rosen, D Feiken, T , CDC

Kenya. P Mensah, N Eseko, A Nejjar, World Health Organization

Regional Office for Africa. M Onsongo, F Kessel, Foreign

Agricultural Svc, U.S. Dept of Agriculture. H Njapau, DL Park,

Center for Food Safety and Applied Nutrition, Food and Drug

Administration. Div of International Health, Epidemiology Program

Office; L , G Luber, H , L Backer, C Rubin, National

Center for Environmental Health; KE Gieseker, E Azziz-Baumgartner, W

Chege, A Bowen, EIS officers, CDC.

Editorial Note:

Evidence that this outbreak resulted from aflatoxin poisoning

included 1) high levels of aflatoxin (up to 8,000 ppb) in maize

samples collected from patient households, 2) a clinical illness

consistent with acute aflatoxin poisoning, 3) clustering of cases

among residents of the same household, and 4) reports of deaths

among animals known to have eaten the same maize as the patients

during the same period. Serum specimens from a convenience sample of

seven patients were tested for differential viral etiologies. All

seven patients had negative serologic tests for yellow fever,

dengue, West Nile virus, Rift Valley fever, Chikungunya and

Bunyamwera viruses, acute hepatitis A, acute hepatitis B, and

hepatitis C.

Aflatoxins are a group of metabolic products formed by two species

of fungus, Aspergillus flavus and A. parasiticus, in several

agricultural commodities, including corn or maize. Two structural

types of aflatoxins are known (B and G types), of which aflatoxin B1

is considered the most toxic and was the type most commonly found in

Kenya during this outbreak. Exposure to aflatoxins occurs primarily

through ingestion of contaminated foods (2) and can cause hepatic

and gastrointestinal injury and have immunosuppressive, teratogenic,

and oncogenic effects. Chronic low-level aflatoxin exposure can

increase the risk for hepatocellular carcinoma (3). Severe, acute

liver injury with high morbidity and mortality has been associated

with high-dose exposures to aflatoxins (4). Ingestion of 2--6 mg/day

of aflatoxin for a month can cause acute hepatitis and death (5,6).

The largest reported outbreak of aflatoxicosis to date occurred in

western India in 1974, resulting in 397 recognized cases and 106

deaths (6). The ongoing epidemic in Kenya already has resulted in

125 recognized deaths. Because of the remoteness of villages in the

affected districts in Kenya and the large geographic area involved,

case finding has been limited to medical facilities. In addition,

because some persons might not have been able to reach health-care

facilities for diagnosis and treatment, the true magnitude of this

outbreak is likely to be considerably greater than reported.

An outbreak of acute aflatoxicosis (20 cases; CFR = 60%) was

reported previously in Makueni district, Eastern Province, Kenya, in

1981 (1). Patients were clustered in family groups that shared meals

consisting of aflatoxin-contaminated maize (1,600--12,000 ppb).

Acute hepatitis associated with consumption of moldy grains also has

been reported in other areas in Africa, Western India, and Malaysia

(6--8), where affected persons came from areas prone to drought and

malnutrition and unseasonable rains forced the harvest of grains

before adequate drying had occurred. Typically, increased reports of

jaundice and hepatitis followed within weeks of such harvests (6--

8). Locally produced maize associated with this outbreak was

harvested in February during peak rains, and the first illnesses

were reported in Makueni district in late March and early April.

For every symptomatic case of aflatoxicosis identified, several

other persons likely were exposed to unsafe levels of aflatoxin and

might face future adverse health consequences. In addition,

individual cases or clusters of aflatoxin poisoning likely occur

regularly but are not recognized. Efforts should focus on the

prevention of aflatoxin exposure by implementing extensive food

replacement, without which, the epidemic can be expected to

continue. Longer-term requirements include strengthened

surveillance; increased food inspections to ensure food safety; and

local education and assistance to ensure that maize is harvested

correctly, dried completely, and stored properly.

This report describes the first investigation by the Kenya FELTP, a

partnership of CDC, KMOH, and Jomo Kenyatta University of

Agriculture and Technology intended to build public health,

epidemiologic, and laboratory capacity in Kenya. This investigation

provided field experience to these Kenyan public health workers in

training and exemplified collaboration between different national

and international agencies and among various sectors and

disciplines, including health, agriculture, food safety, nutrition,

and humanitarian relief. Increased collaboration between the health

sector and others involved in food security and safety could enable

early warning of high levels of aflatoxins.

As a result of widespread drought, Kenya faces an acute food

shortage, with nearly 1.8 million persons in 26 districts vulnerable

to food insecurity (9), including persons in the area most heavily

affected by the aflatoxicosis outbreak. Because an estimated 166,000

metric tons of food will be required to meet the requirements of

emergency and school feeding programs during August 2004--January

2005, public health officials should be vigilant to a possible wider

aflatoxicosis outbreak resulting from the large-scale storage and

distribution of certain emergency food supplies.

Acknowledgments

The findings in this report are based, in part, on contributions by

Makindu Sub-District Hospital, Makueni district, Mutomo Mission

Hospital, Kitui district, other health facilities, staff at the

National Public Health Laboratory Svcs, Kenya.

References

Ngindu A, Kenya PR, Ocheng DM, et al. Outbreak of acute hepatitis by

aflatoxin poisoning in Kenya. Lancet 1982;319:1346--8.

Fung F, RF. Health effects of mycotoxins: a toxicological

overview. J Toxicol Clin Toxicol 2004;42:217--34.

Peraica M, Radic B, Lucic A, Pavlovic M. Toxic effects of mycotoxins

in humans. Bull World Health Organ 1999;77:754--66.

Chao TC, Maxwell SM, Wong SY. An outbreak of aflatoxicosis and boric

acid poisoning in Malaysia: a clinicopathological study. J Pathol

1991;164:225--33.

Patten RC. Aflatoxins and disease. Am J Trop Med Hyg 1981;30:422--5.

Krishnamachari KA, Nagaarajan V, Bhat RV, Tilak TB. Hepatitis due to

aflatoxicosis---an outbreak in Western India. Lancet 1975;305:1061--

3.

Krishnamachari KA, Bhat RV, Nagarajan V, Tilak TBG. Investigations

into an outbreak of hepatitis in parts of Western India. Indian J

Med Res 1975;63:1036--49.

Lye MS, Ghazali AA, Mohan J, Alwin N, Nair RC. An outbreak of acute

hepatic encephalopathy due to severe aflatoxicosis in Malaysia. Am J

Trop Med Hyg 1995;53:68--72.

USAID Famine Early Warning Systems Network (Kenya), World Food

Program, Kenya Ministry of Agriculture. Kenya food security report---

August 9, 2004. Available at

http://www.fews.net/centers/files/Kenya_200407en.pdf.

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