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1 figure omitted
Zambia experienced widespread cholera epidemics in 1991 (13,154 cases),
1992 (11,659), and 1999 (11,327).1 In response
to the large outbreak in 1999, the Zambian Ministry of Health (ZMOH) urged
use of in-home chlorination with the locally produced solution, Clorin®,
and the practice increased substantially Clorin® had been introduced in
Zambia in 1998 as part of the Safe Water System (SWS), a point-of-use water
disinfection and safe-water storage strategy* launched by the Society for
Family Health, in partnership with ZMOH, the U.S. Agency for International
Development, and CDC. Although no outbreaks were reported during 2000-2002,
cholera remained endemic. Epidemic cholera returned to Zambia in November
2003, when cases of toxigenic Vibrio cholerae O1, serotype Ogawa, biotype
El Tor were confirmed in the capital city, Lusaka. During November 28, 2003–January
4, 2004, an estimated 2,529 cholera cases and 128 cholera deaths (case-fatality
rate [CFR]=5.1%) occurred in Lusaka. In February 2004, the Lusaka District
Health Management Team (LDHMT) invited CDC to assist in an investigation of
the epidemic. This report summarizes the results of that investigation, which
implicated foodborne transmission via raw vegetables and demonstrated a protective
role for hand washing with soap. The results underscore the importance of
hygiene, clean water, and sanitary food handling for cholera prevention.
In response to increasing cases, Zambian authorities began opening designated
cholera-treatment centers (CTCs) in Lusaka in December 2003. All seven CTCs
were functional by early January 2004, and all patients with suspected cholera
were referred to these facilities. During January 5–March 1, an additional
2,101 cases and 25 deaths from cholera (CFR=1.2%) were recorded at CTCs in
Lusaka. Investigators conducted a matched case-control study to identify risk
factors for cholera. A case was defined as watery diarrhea in a person aged ≥5
years, who was admitted to the Chawama (Figure) or Kanyama CTC during February
11-22. Stool cultures were performed for all eligible patients. Homes of enrolled
patients were visited, and one age-, sex-, and neighborhood-matched control
per case was selected systematically from neighboring households.
A total of 71 case-control pairs were enrolled in the study. V. cholerae
O1 was identified in stool cultures from 52 (74%) patients. Both bivariate
and multivariate analyses were performed, comparing all cases with culture-confirmed
cases; because data were comparable for the two groups, results are reported
for all cases in aggregate. The median age of patients was 27 years (range:
5-75 years); 58% were male. Common symptoms, in addition to diarrhea, included
vomiting (61 [86%]) and leg cramps (44 [62%]).
Bivariate analysis indicated that consumption of raw vegetables was
associated with cholera (matched odds ratio [MOR]=3.9; 95% confidence interval
[CI]=1.7-9.6; p=0.0004). Hand soap was observed in 41 (58%) case homes and
64 (90%) control homes. Presence of hand soap was considered a proxy for actual
hand washing and was determined to be protective (MOR=0.14; 95% CI=0.05-0.40;
p=0.0001). Consumption of kapenta, a local sardine-like dietary staple, also
was protective (MOR=0.35; 95% CI=0.2-0.8; p=0.005). Drinking untreated water
was reported by 48 (67%) case-patients and 37 (52%) controls, but the association
with disease did not reach statistical significance (MOR=1.9; 95% CI=0.9-3.9;
p=0.06). In-home chlorination of drinking water with Clorin® was reported
by 48 (67%) controls and 47 (66%) case-patients. Free chlorine residuals were
detected in stored water in 19 (27%) case homes and 14 (20%) control homes
(MOR=1.5; 95% CI=0.7-3.3; p=0.21).
Kapenta, raw vegetables, presence of soap, and in-home water treatment
were included in a multivariate model. Water treatment, either by boiling
or home chlorination, was not significantly protective. Consumption of raw
vegetables remained significantly associated with cholera (adjusted odds ratio
[AOR]=4.7; 95% CI=1.7-13.0). The presence of hand soap remained significantly
protective against cholera (AOR=0.1; 95% CI=0.04-0.40), as did consumption
of kapenta (AOR=0.3; 95% CI=0.1-0.7).
On the basis of these results, the Zambian Central Board of Health and
LDHMT enhanced cholera-prevention efforts by reinforcing hand-washing promotion
messages and recommending that vegetables be cooked or washed in treated water.
Plans were created to improve hygiene and increase availability of latrines
at Lusaka’s major market to minimize cross-contamination of produce.
Long-term prevention measures under discussion by local authorities include
improving the quality and quantity of municipal water supplies. In April,
cholera cases declined dramatically, and LDHMT closed the CTCs.
M Sinkala, MD, M Makasa, MD, F Mwanza, P Mulenga, Lusaka District Health
Management Team, Zambia. P Kalluri, MD, R Quick, MD, E Mintz, MD, RM Hoekstra,
PhD, Div of Bacterial and Mycotic Diseases, National Center for Infectious
Diseases; A DuBois, MD, EIS Officer, CDC.
This month marks the 150th anniversary of the removal of the famed Broad
Street pump handle after John Snow’s classic study of epidemic cholera
in London. Cholera is caused by toxigenic V. cholerae, serogroup O1 or O139.
Infection can result in rapidly progressive, profuse, dehydrating diarrhea,
with CFRs ≥22% when treatment is delayed.2 Cholera,
which is still propagated by many of the same vehicles described by John Snow
in the mid-1800s,3 remains a public health
threat in sub-Saharan Africa and certain Asian countries. In 2003, the World
Health Organization reported a total of 111,575 cholera cases and 1,894 deaths
(CFR=1.7%) in 45 countries; 97% of reported cases occurred in sub- Saharan
Africa.4 In recent decades, the CFR of cholera
has decreased because of dramatic improvements in oral and intravenous rehydration
In this epidemic of cholera, the primary mode of transmission was foodborne
rather than waterborne, a possibility recognized by Snow.3 The
implication of vegetables as a vehicle of transmission in this epidemic emphasizes
the need for further assessment of produce hygiene during transport, delivery,
and use in the home.
This investigation also documented the widespread acceptance of the
SWS in cholera-affected communities in Lusaka. Implemented as a pilot project
in Zambia in 1998, SWS has been determined to reduce the risk for diarrhea
by ≥40%.7 The SWS consists of Clorin®,
a dilute solution of locally produced sodium hypochlorite bleach, packaged
and marketed for disinfection of water in the home, and promotion of plastic
20-liter jerricans for safe storage of treated water. The demand for Clorin®
escalated during the 1999 cholera epidemic, and sales increased steadily in
subsequent years. In 2003, approximately 1.7 million bottles of Clorin®
were sold in Zambia. Findings of this investigation suggest that, 5 years
after introduction of the SWS in Zambia, >20% of persons residing in Lusaka’s
shantytown purchase Clorin® solution and add it to their water.
The presence of soap in the home, which serves as a proxy for improved
hygiene, was protective against cholera during this investigation. This finding
is consistent with other studies that suggest hand washing reduces the risk
for diarrhea by >40%8 and echoes the work of
Snow, who implicated poor hand hygiene in cholera transmission.
Approximately 50% of Zambia’s 10 million residents live in cities.
An estimated 60% of the 2 million residents of Lusaka reside in shantytowns
without municipal water supplies or sewer systems.9 Snow’s
London of 1854 resembles numerous cities in the developing world today, where
inadequate water and sanitation services and overcrowding contribute to a
high burden of preventable diseases such as cholera. An estimated 1.1 billion
persons in the world live without access to improved water supplies such as
piped municipal systems; hundreds of millions more use inadequate systems,
which routinely provide water that is contaminated and unsafe. Waterborne
transmission of enteric pathogens contributes to the estimated 2 million diarrheal
deaths that occur among children aged <5 years each year.10 In
recognition of this continuing problem, member states of the United Nations
established a Millennium Development Goal for Water to reduce by half the
proportion of persons without sustainable access to safe drinking water by
2015. To achieve this goal, an estimated 300,000 persons must gain access
to safe drinking water each day for the next 11 years. Even if this challenge
is met, more than half a billion persons will still lack access to safe drinking
water. As in Snow’s day, field epidemiology and practical prevention
strategies remain critical to meeting public health challenges in the modern
The findings in this report are based in part on contributions by S
Leuschner, C Robinson, P Kalenga, Society for Family Health, Lusaka; M Tembo,
PhD, Tropical Diseases Research Center, Ndola; V Mukonka, MD, V Mtonga, MMED,
Central Board of Health, Zambia. M Roulet, MD, J Vincent, World Health Organization,
Geneva, Switzerland. S Sasaki, Japan International Cooperation Agency, Tokyo,
*Detailed information available at http://www.cdc.gov/safewater.
Cholera Epidemic Associated With Raw Vegetables—Lusaka, Zambia, 2003-2004. JAMA. 2004;292(17):2077–2078. doi:https://doi.org/10.1001/jama.292.17.2077
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