Water System Publications
Cholera in the New World: Translating Field Epidemiology into New Prevention Strategies
Tauxe R, Mintz E and
a devastating diarrheal disease, has swept through the world in recurrent pandemics
since 1817. The seventh and ongoing pandemic began in 1961 when the El Tor biotype
of Vibrio cholerae O1 emerged in Indonesia. This pandemic spread through
Asia and Africa and finally reached Latin America early in 1991 1.
After explosive epidemics in coastal Peru, it spread rapidly and continues throughout
Latin America (Figure 1). Because of underreporting, the more than
1,000,000 cholera cases and 10,000 deaths reported from Latin America through
1994 (Table 1) 2 represent only a small fraction of the
actual number of infections. Molecular characterization of V. cholerae
O1 strains from Peru has shown that they do not match strains from anywhere else
in the world; therefore, the source of the Peruvian epidemic strains remains unknown
3. Moreover, other strains have since appeared in Latin America. At
least one of these, a strain resistant to multiple antimicrobial drugs, was first
identified in Mexico and elsewhere in the world in mid-1991 and has since spread
widely throughout Central America 4. The introduction of strains into
new areas illustrates the rapid global transfer of pathogens. V. cholerae
O139 Bengal, which emerged as a new cause of epidemic cholera in Asia in 1992,
could also appear in Latin America 5.
1. Geographic extent of the Latin American cholera epidemic over time. Lines
represent the advancing front of the epidemic at different dates. As of mid-1995,
all Latin American countries except Uruguay have reported cases; no cases have
been reported from the Caribbean.
1. Cholera cases by country, as reported to the Pan American Health Organization,
1991 through 1994
a NR = no reports received.
| Country|| Date
of first report|| 1991|| 1992||Number
of reported cases|
introductions are not easy to prevent, because they may follow the arrival of
travelers who are not aware of their infection or of ships carrying contaminated
ballast water. The key to controlling epidemic cholera lies in limiting its spread
by using measures that prevent sustained transmission. One measure might be using
an inexpensive and effective vaccine to provide lasting protection; however, no
such vaccine yet exists, although progress in vaccine development is being made
6-8. Another measure is interrupting transmission so that the causative
organism never reaches the human host. This approach to prevention successfully
controlled many epidemic diseases in the industrialized world, including cholera,
typhoid fever, plague, and malaria, before vaccines or antibiotics were developed.
Over the last century, a large engineering infrastructure, built in industrialized
nations, has provided safe water and sewage treatment for nearly all people in
these nations and has made sustained transmission of cholera in those countries
extremely unlikely. Despite sporadic cases along the U.S. Gulf Coast and repeated
introduction of the epidemic organisms by travelers, epidemic cholera has not
occurred in the United States since the nineteenth century 9,10.
2. Mechanisms of transmission of epidemic cholera in Latin America, as determined
in eight epidemiologic - investigations, 1991-1993a
| || ||Peru|| || || || || || |
Urban 3/91 (15)||Piura
Urban 3/91 (16)||Iquitos
Urban 7/91 (17)||Ecuador
Guayaquil Urban |
Salvador Rural |
Saipina Rural |
Fortaleza Rural |
6/93 + b
City Urban 7/93 (21)
|Waterborne|| || || || || || || || |
water||+||+|| ||+|| || || || |
water|| || ||+|| ||+||+||+|| |
hands in water vessel||+||+|| || || || || || |
|Foodborne|| || || || || || || || |
vendors' foods|| ||+|| || || || || || |
vendors' beverages|| ||+|| ||+|| || ||+|| |
vendors' ice/ices|| ||+|| || || || || ||+|
|Leftover rice|| ||+||+|| || || || ||+|
| || ||+|| || || || ||+|
|Seafood|| || || || || || || || |
seafood|| || || ||+|| || || || |
seafood|| || || ||+||+|| || || |
prevent cholera by interrupting transmission of the organism to the host, it is
important to understand precisely how the bacteria are transmitted. John Snow
demonstrated waterborne transmission of cholera during a large epidemic in London
in 1856 11. He and many others since have suspected that other routes
of transmission are also important. Epidemiologic investigations during the seventh
pandemic have documented a variety of specific food and water pathways by which
the bacteria reach the host, some of which were new and unsuspected 12.
The El Tor biotype of V. cholerae O1, for example, multiplies rapidly in
moist foods of neutral acidity 13. This bacterium also persists in
the estuarine environment in niches that are poorly understood but may involve
the plankton on which shellfish feed. This means that raw seafood can be contaminated
naturally before it is harvested. Understanding these pathways of transmission
in detail has been central to devising successful control measures to block them.
For example, advice to drink only boiled or bottled water would be of little use
in outbreaks where the source was actually contaminated food, such as shellfish
or leftover rice. On at least one occasion, such advice actually worsened the
situation because the bottled water was itself contaminated 14.
epidemic cholera appeared in Latin America, after an absence of more than 100
years, we conducted a series of eight rapid field investigations in collaboration
with national public health authorities and the Pan-American Health Organization
to define the pathways of disease transmission and the priorities for prevention.
Conducted in various settings between February 1991 and August 1993, these investigations
guided the initial emergency prevention efforts and the development of sustained
prevention measures (Table 2) 15-21.
same case-control method was used for each investigation. We first interviewed
a few patients in great detail about what they had ingested in the 3 days before
they became ill, probing for known or potential vehicles of cholera. We then constructed
a standardized interview questionnaire that asked about possible exposures. Using
this questionnaire, we interviewed patients recovering from cholera as well as
healthy persons of the same age and sex who lived in the same neighborhood. By
comparing the frequency of positive and negative responses among the ill and well
persons, we could identify the exposures most strongly associated with disease.
For example, if 25 of 35 patients, but only 5 of 35 matched controls, reported
eating sliced mango from street vendors in the 3 days before the illness began,
the probability of observing this difference in proportions by chance alone is
0.000045, and the ratio of the odds of exposure is 15, a measure of the strong
association between disease and consuming sliced mangos. When disease is statistically
associated with more than one exposure, multivariate analysis can identify truly
independent risk factors. In the above example, "eating food from a street vendor"
would not be independent from "eating sliced mango" if one usually got sliced
mango from a street vendor. This case-control method can be rapidly carried out
in the field at low cost.
showed that cholera was being transmitted by several distinct mechanisms. The
predominant route of transmission in a given setting depends largely on the degree
of sanitation already achieved. Therefore, a multifaceted approach to prevention
is needed. Emergency measures, such as advice to boil drinking water or to heat
all foods from street vendors, are difficult to sustain because of their inconvenience
and high cost. Moreover, the cost of building large-scale water treatment and
sanitation systems is extraordinary, estimated at $200 billion for all of Latin
America 22. The challenge of cholera prevention lies in devising low-cost
alternatives that are both effective and sustainable.
transmission was identified in seven of the eight investigations. In three of
these, the implicated water came from municipal systems or from tanker trucks
that reportedly obtained water from municipal systems. Water delivered through
poorly maintained municipal water systems can be contaminated by sewage because
of leaky pipes, frequent pressure drops, and the lack of residual chlorine disinfectant
in the water. In developing countries, water is rarely available 24 hours a day
so it is usually stored in the home, where further contamination can easily occur.
For example, when we measured the increase in contamination of the water as it
was distributed and stored in Trujillo, Peru, fecal coliform counts, an index
of sewage contamination, were 1/100 ml in water collected at the source well,
2/100 ml at public taps, and 20/100 ml in water stored in the home 13.
In four investigations, the implicated water was collected from rivers or ponds,
where direct sewage contamination was likely. Specific protective practices were
also noted in these investigations, including treating water in the home by boiling
it or by adding chlorine bleach, using a small-mouthed vessel to store water,
pouring water out of the storage vessel rather than scooping it out with a cup,
and having hand soap in the home. In one investigation on the Amazon, we found
that the local common practice of adding citrus juice to water to improve its
taste was protective because the acid in the fruit killed Vibrio bacteria
14. This observation gave local authorities a new, inexpensive, and
immediately available emergency control measure.
first stage of prevention, then, is providing safe drinking water. As a result
of the above findings, we have developed and are testing simple and inexpensive
methods of domestic water disinfection and storage that would also prevent other
diseases transmitted by the same route. A pilot trial in a periurban area of Bolivia
showed that disinfecting household water with a calcium hypochlorite solution
and storing it safely in a special narrow-mouthed container was acceptable to
a community of Aymara Indians 20. Compliance, as measured by chlorine
residuals in stored water, was high among families using the intervention. The
concentration of Escherichia coli bacteria in the stored water, a measure
of fecal contamination, was significantly lower in households that used the intervention
than in neighboring households that used traditional water handling methods 23.
A field trial in rural Bolivia showed that villagers could generate their own
disinfectant solution by using a simple electrolytic apparatus 24;
with the disinfectant and the special water container the villagers provided clean
water in their homes. Households using this intervention had 40% fewer diarrheal
episodes than randomly selected neighboring families who used traditional water-handling
methods. The combination of point-of-use disinfection and safer water storage
containers could have broad effects, including local empowerment for production
of potable water, safer infant foods, and new microindustries for the production
of disinfectant solutions and water vessels 25. Cost-benefit analysis
indicates that this strategy is cost saving if it prevents more than 20% of diarrheal
illnesses 26. Inexpensive disinfectant generators are now being manufactured
for this purpose in Ecuador. In Colombia, the number of cholera cases has dropped
dramatically since late 1992 when chlorine disinfectant tablets were distributed
for treating household water.
second major route of cholera transmission is food contaminated in the market
or home. This includes food and beverages sold by street vendors, leftover rice,
and unwashed fruits and vegetables. This was an important route in four of the
eight investigated areas, including Guatemala City, where there was no evidence
of waterborne transmission 21. Foods and beverages sold by street vendors
are a fixture of urban life throughout the developing world; they are often prepared
in unhygienic ways and then held at ambient temperatures for hours, which permits
rapid bacterial multiplication. Other problems associated with food and beverages
from street vendors included using unsafe ice to chill beverages and selling homemade
frozen drinks. Leftover rice is an excellent growth medium for V. cholerae
O1 and eating leftover rice without reheating it was associated with illness in
three investigations. In one investigation, illness was associated with eating
unwashed produce that was probably splashed with river water while being transported
to market in small boats.
the second stage of cholera prevention is to improve food handling, particularly
for foods and beverages sold by street vendors. Many countries in Latin America
have begun educating street vendors in fundamental food safety and linking this
education to licensing 27. By itself, however, education may not improve
food safety if clean water to prepare foods and beverages is not available and
handwashing and dishwashing with soap and water are not routine. We are field
testing a combined strategy of point-of-use disinfection, handwashing with soap,
and use of a special water/beverage container to improve the microbial quality
of beverages sold by street vendors. Because street vendors are responsive to
customer demand, teaching consumers to look for street vendors that are visibly
practicing better hygiene may reinforce more hygienic conditions. In addition
to these efforts to improve food sold on the street, health authorities should
advise the public to reheat leftover rice and wash fruits and vegetables before
eating. In Santiago, Chile, suspicion that cholera was caused by vegetables irrigated
with fresh sewage led to a ban on this practice; the ban not only prevented cholera
transmission by this route, but also decreased the incidence of typhoid fever
and hepatitis A dramatically 28.
through seafood (identified in two of the eight investigations) is a third major
route of cholera transmission, distinct from other foodborne mechanisms, because
it requires different prevention strategies. One investigation implicated both
uncooked seafood and cooked crab, and another implicated cooked seafood eaten
without reheating. Contaminated seafood also caused three outbreaks of travel-associated
cholera in the United States. In the most dramatic, at least 75 persons contracted
cholera after taking a flight from Latin America to California 29;
illness was associated with eating cold seafood salad that was loaded onto the
plane in Lima, Peru. Two other outbreaks followed the informal transport of cooked
crabs from Ecuador to the United States in travelers' suitcases 30,31.
Marine creatures may harbor V. cholerae O1 before they are harvested or
may be contaminated by seawater used in seaside processing plants. In areas where
raw and undercooked seafood are popular, seafood-associated cholera may occur
even if the general level of sanitation and hygiene is high 32. Vibrios
survive light cooking and can subsequently grow if the seafood is held for many
hours before eating 33.
seafood-associated cholera in the long term will depend on maintaining sewage-free
harvest beds and improving sanitation in processing plants. In coastal areas where
the organism persists in the environment, even in the absence of sewage contamination,
education to discourage the consumption of raw or undercooked shellfish is also
needed. Thorough cooking provides the greatest security, but it is sometimes resisted
by local populations for cultural reasons. "Ceviche," a popular Latin American
dish prepared from seafood that is marinated in citrus juice for variable lengths
of time, is a case in point. Prolonged marination in acidic liquid is likely to
inactivate vibrios if the acid can penetrate throughout the flesh and deep organs
of the fish or shellfish (34). Further evaluation of this approach is needed,
but for the present, encouraging the use of ceviche recipes that provide sufficient
marination time may be a practical intervention.
Latin America, as in other parts of the world, epidemiologic field investigations
of cholera have defined the local routes of transmission, identified unsuspected
and correctable control points, and quantified the effects of emergency measures.
The results of investigations also have generated specific control strategies
targeted to blocking the predominant routes. While this multistage portrait of
transmission is complex, it is being translated into action and change. The longstanding
deficits in basic urban infrastructure and the need for new efforts to correct
them have never been more apparent 35,36. Workable prevention strategies
include better domestic water storage containers, point-of-use water disinfection,
attention to the education and hygiene of street vendors, and simple modifications
of traditional recipes. Many other diseases are transmitted by these same waterborne
and foodborne routes, so these control measures may prevent other infections in
addition to cholera. If it becomes a catalyst for long overdue improvements in
the safety of water and food, epidemic cholera can have a far-reaching impact
on the public health of Latin America.
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