Am. J. Trop. Med. Hyg., 77(4), 2007, pp. 705–713
Copyright © 2007 by The American Society of Tropical Medicine and Hygiene
Cholera: A New Homeland in Africa?
Nicholas H. Gaffga,* Robert V. Tauxe, and Eric D. Mintz
Enteric Disease Epidemiology Branch, Division of Foodborne, Mycotic, and Enteric Diseases, National Center for Zoonotic,
Vectorborne, and Enteric Diseases, Coordinating Center for Infectious Diseases, Centers for Disease Control and Prevention,
Atlanta, GA
Abstract. Cholera was largely eliminated from industrialized countries by water and sewage treatment over a century
ago. Today it remains a significant cause of morbidity and mortality in developing countries, where it is a marker for
inadequate drinking water and sanitation infrastructure. Death from cholera can be prevented through simple treatment—oral, or in severe cases, intravenous rehydration. The cholera case-fatality rate therefore reflects access to basic
health care. We reviewed World Health Organization (WHO) data on cholera cases and deaths reported between 1960
and 2005. In the 1960s, at the beginning of the seventh and current cholera pandemic, cholera had an exclusively Asian
focus. In 1970, the pandemic reached sub-Saharan Africa, where it has remained entrenched. In 1991, the seventh
pandemic reached Latin America, resulting in nearly 1 million reported cases from the region within 3 years. In contrast
to the persisting situation in Africa, cholera was largely eliminated from Latin America within a decade. In 2005, 31
(78%) of the 40 countries that reported indigenous cases of cholera to WHO were in sub-Saharan Africa. The reported
incidence of indigenous cholera in sub-Saharan Africa in 2005 (166 cases/million population) was 95 times higher than
the reported incidence in Asia (1.74 cases/million population) and 16,600 times higher than the reported incidence in
Latin America (0.01 cases/million population). In that same year, the cholera case fatality rate in sub-Saharan Africa
(1.8%) was 3 times higher than that in Asia (0.6%); no cholera deaths were reported in Latin America. The persistence
or control of cholera in Africa will be a key indicator of global efforts to reach the Millennium Development Goals and
of recent commitments by leaders of the G-8 countries to increase development aid to the region.
principles—ensuring universal access to potable water and
the separation of human fecal wastes from food and water
sources—is sufficient to prevent widespread cholera transmission. Through these measures, epidemic cholera was eliminated from Europe and the United States over a century ago.
Although isolated cases and small, self-contained outbreaks
of cholera still occur in developed nations, sustained cholera
transmission, even under extraordinary conditions, generally
does not occur.
Cholera surveillance. Cholera was the first disease for
which modern public health surveillance and reporting was
carried out in an organized way.6 Because of the challenges of
conducting cholera surveillance in the developing world and
the concern in some countries about economic and social
ramifications of reporting cases of cholera, the cases reported
to the World Health organization (WHO) greatly underestimate the true number of cholera illnesses that occur.6 Despite
its imperfections, the WHO passive cholera surveillance system provides relatively consistent national and regional profiles of cholera over time, and reflects the success and failure
of efforts toward its prevention and control.
INTRODUCTION
Clinical features of cholera. Cholera is an acute, diarrheal
illness caused by infection of the intestine with the toxigenic
bacterium Vibrio cholerae serogroup O1 or O139. Infection
can be asymptomatic, mild, or severe: approximately 1 in 20
infected persons has severe disease characterized by profuse
watery diarrhea, vomiting, and leg cramps. In these persons,
rapid loss of body fluids leads to dehydration, electrolyte disturbances, and hypovolemic shock. Without treatment, death
can occur within hours.1 With simple and inexpensive treatment—vigorous oral or intravenous fluid and electrolyte replacement—recovery in a matter of days is routine, and overall mortality can be reduced from as much as 50% to less than
1%, even in makeshift rural treatment centers.2
Epidemiologic history of cholera. Toxigenic Vibrio cholerae O1, the causal agent of epidemic cholera, can persist
indefinitely in marine, estuarine, and riverine environments.
Since 1817, it has emerged from endemic areas in Asia in
seven pandemic waves that have involved much of the
world.3,4 The seventh and current pandemic, which began in
1961, is the first pandemic known to be caused by the El Tor
biotype of Vibrio cholerae O1.5 This most recent pandemic
has lasted longer, spread further, and infected more persons
than any of its predecessors, and is the first to have established a persistent presence outside of Asia.
Cholera in the environment. Epidemic cholera is spread by
the fecal–oral route. In developing nations, this occurs most
often through consumption of contaminated water. Because
Vibrio cholerae has adapted to long-term survival in surface
waters, often in association with zooplankton, plants, and
crustaceans, eradication is not considered a realistic goal.1
However, the application of well-established public health
METHODS
Sources of cholera data. To better characterize the current
global cholera problem, we reviewed data from selected
WHO summaries of reported cholera incidence and mortality
between 1960 and 2005 and from a WHO multi-year summary
of cholera incidence and mortality.6 Cholera incidence data
were obtained from the following sources: 1960–1969 data
came from summaries published in 1961, 1962, 1964, and
19707–10; 1970–1998 data came from a WHO multi-year summary6; and 1999–2005 data came from annual summaries published in 2000 through 2006.11–17 Cholera mortality data were
obtained from the following sources: 1960–1963 data came
from annual reports8,9; 1964–1969 data came from a summation of all of the cholera deaths reported in the individual
Weekly Epidemiologic Reviews that contained information
* Address correspondence to Nicholas Gaffga, Centers for Disease
Control and Prevention, 1600 Clifton Road, NE, Mailstop A-38, Atlanta, GA 30333. E-mail: [email protected]
705
*
*
100%
(435,758)
100%
(117,192)
26.9%
*
*
*
sub-Saharan African % of
world reported deaths (#)
African CFR
Asian % of world reported
cases (#)
Asian % of world reported
deaths (#)
Asian CFR
Latin American % of world
reported cases (#)
Latin American % of world
reported deaths (#)
Latin American CFR
*
*
*
77.4%
(63,580)
8.9%
79.5%
(713,514)
22.4%
(18,398)
10.4%
19.7%
(176,849)
9.1%
82,095
897,340
1970–1979
*
*
*
18.1%
(4,939)
2.5%
40.0%
(200,991)
81.8%
(22,298)
7.5%
59.4%
(298,295)
5.4%
27,256
502,075
1980–1989
*, no reported cases or deaths, †, no reported deaths.
Table includes indigenous and imported cases reported from Latin America, Asia, and Africa.
26.9%
*
sub-Saharan African % of
world reported cases (#)
117,192
Reported global deaths from
cholera
Global CFR
435,758
Reported global cases of
cholera
1960–1969
1.0%
14.1%
(12,030)
42.9%
(1,261,629)
8.8%
(7,480)
1.7%
14.7%
(432,278)
77.1%
(65,914)
5.3%
42.2%
(1,240,277)
2.9%
85,445
2,939,020
1990–1999
1.1%
0.2%
(40)
0.5%
(3,687)
2.4%
(449)
1.1%
5.2%
(42,046)
97.2%
(18,196)
2.4%
93.9%
(758,866)
2.3%
18,711
808,594
2000–2005
1.3%
0.8%
(40)
2.3%
(3,091)
4.7%
(232)
2.1%
8.2%
(11,246)
93.9%
(4,610)
3.9%
86.8%
(118,932)
3.6%
4,908
137,071
2000
0.0%
0.0%
†
0.3%
(525)
5.1%
(138)
1.3%
5.6%
(10,340)
94.9%
(2,590)
1.5%
94.1%
(173,359)
1.5%
2,728
184,311
2001
0.0%
0.0%
†
0.0%
(17)
0.3%
(13)
0.3%
3.1%
(4,409)
99.7%
(4,551)
3.3%
96.9%
(137,866)
3.2%
4,564
142,311
2002
0.0%
0.0%
†
0.0%
(26)
0.5%
(10)
0.3%
3.1%
(3,463)
99.5%
(1,884)
1.7%
96.9%
(108,067)
1.7%
1,894
111,575
2003
TABLE 1
Cholera cases, deaths, and case fatality rate reported to WHO by region (World, Africa, Asia, Latin America), 1960–2005
0.0%
0.0%
†
0.0%
(28)
0.6%
(14)
0.2%
5.7%
(5,764)
99.4%
(2,331)
2.4%
94.3%
(95,560)
2.3%
2,345
101,383
2004
0.0%
0.0%
†
0.0%
(5)
1.8%
(82)
0.6%
5.2%
(6,824)
98.2%
(2,230)
1.8%
94.8%
(125,082)
1.7%
2,272
131,943
2005
706
GAFFGA AND OTHERS
CHOLERA: A NEW HOMELAND IN AFRICA?
707
FIGURE 1. Number of cases of cholera reported to WHO by region (Africa, Asia, Latin America) and year, 1960–2005. *Includes both
indigenous and imported cases of cholera.
on deaths for those years; 1970–1998 data came from the
WHO multi-year summary6; and 1999–2005 data came from
annual summaries published in 2000 through 2006.11–17 Data
on the number of countries reporting cholera were obtained
from the following sources: 1960–1969 data came from annual
summaries published in 1962, 1964, and 19718,9,18; 1970–1998
data came from a WHO multi-year summary6; and 1999–2005
data came from annual summaries published in 2000 through
2006.11–17 Except where noted, all data exclude cases that
were reported as imported cases.
Calculation of indices. We used national data reported to
WHO from 2000 through 2005 to calculate indices of cholera
“endemicity” and “density” in each African country during
this 6-year period. We defined the cholera endemicity index
as the number of years during 2000–2005 in which a country
reported cholera cases (from 0–6). We defined the cholera
density index as the median number of cases reported annually by a country during 2000–2005 divided by the country’s
population as estimated for 2005.19 For each country, we
calculated the mean case-fatality rate (CFR) for the 6-year
period (the total number of deaths reported divided by the
total number of cases reported divided by 6). We use the term
Latin America to refer to countries in South and Central
America (including Mexico) but not the Caribbean. Cases
and deaths reported from Europe, Canada, the United States,
and Oceania were included in the world totals only. Population data, when not provided directly in source references, and definition of geopolitical areas and regions, were
derived from the United Nations 2004 World Population
Prospects.19
FIGURE 2. Number of countries that reported cholera cases to WHO by region (Africa, Asia, Latin America) and year, 1968–2005. *Includes
countries reporting both indigenous and imported cases of cholera. Does not depict countries in Europe or Oceania that reported cases of cholera.
708
GAFFGA AND OTHERS
FIGURE 3. Cholera density: endemicity and median incidence of cholera reported to WHO by country, Africa, 2000–2005. The number
appearing over each country represents the number of years between 2000 and 2005 in which the country reported cases of cholera.
RESULTS
The seventh pandemic entered Africa in 1970, where it
remains an ongoing source of morbidity and mortality (Table
1, Figures 1 and 2). The pandemic reached the Americas in
1991, causing nearly 400,000 cases that year for a total of
nearly 1 million cases over a 10-year period. However, the
number of Latin American countries reporting cholera and
the number of cases reported has since diminished sharply,
and in 2005, only one Latin American country (Brazil) reported cholera (5 cases).
The number of Asian countries reporting cholera cases (indigenous or imported) decreased from a mean of 18 during
the period 1970–1979 to a mean of 11 during the period 2000–
2005. In 2005, 9 Asian countries reported a total of just 6,824
indigenous or imported cholera cases to WHO.
However, each year since 1991, more than 100,000 indigenous or imported cases and 1,800 cholera deaths have been
reported by between 45 and 92 member nations (Table 1,
Figures 1 and 2).6,11–17,20 Although cholera incidence and the
number of countries reporting cholera has decreased in Asia
and Latin America over the past decade, the number of countries in sub-Saharan Africa reporting cholera has increased,
and the incidence has remained largely unchanged. In subSaharan Africa, between 1971 and 1993, a mean of 17 countries reported indigenous or imported cholera each year, increasing to 28 countries between 1994 and 2005. With 11.6%
of the world’s population, sub-Saharan Africa has reported
more than 94% of the total global cholera cases since 2001
(Table 1, Figure 1). In 2005, 94.8% of the 131,943 reported
cases of cholera and 98.2% of the 2,272 reported cholera
deaths occurred in Africa (Table 1).
Cholera endemicity within Africa. In recent years, the pandemic has been sustained in several African regions (Table 2,
Figure 3). Among the 39 African countries that reported
cases of cholera in any year from 2000 through 2005, 18 (46%)
reported cases in all 6 years: Benin, Burundi, Cameroon,
Democratic Republic of the Congo, Ghana, Guinea, Liberia,
Malawi, Mozambique, Niger, Nigeria, South Africa, Swaziland, Togo, Uganda, United Republic of Tanzania, Zambia,
and Zimbabwe. Countries with such high endemicity are
found in East, Southern, Central, and West Africa (Figure 3).
During that 6-year period, no cholera cases were reported by
11 (28%) countries in sub-Saharan Africa: Angola, Botswana,
Cape Verde, Eritrea, Lesotho, Mauritius, Namibia, Reunion,
St. Helena, Seychelles, and Sudan. The absence of reported
cases may reflect a real lack of detectable cholera, or the
national Health Ministries’ inability to recognize or unwillingness to report cholera cases. It is noteworthy that three
countries that did not report cholera in 2000–2004 experienced cholera outbreaks in 2005: Gambia, 214 cases and 13
deaths (CFR 6.1%); Mauritania 4,132 cases and 70 deaths
(CFR 1.7%); Sao Tome, 1,966 cases and 33 deaths (CFR
1.7%). Similarly, in 2006, two countries that did not report
cholera in the preceding 5 years had dramatic cholera epidemics: Angola, 43,076 cases and 1,642 deaths (CFR 3.8%) as
of June 6, 200621; and Sudan, 8,923 cases and 238 deaths (CFR
2.7%) as of March 20, 2006.22
Cholera density within Africa. The cholera density is highest in Eastern and Southern Africa (Figure 3). During this
period from 2000–2005, four countries in Africa had a cholera
density greater than 200 cases per 1,000,000 people: Mozambique (793/million), Liberia (594/million), Somalia (441/
million), and the Democratic Republic of the Congo (242/
709
CHOLERA: A NEW HOMELAND IN AFRICA?
TABLE 2
Continued
TABLE 2
Cholera endemicity, density, and lethality in Africa, 2000–2005
Number of
years
reporting
cholera
Median
incidence
per million
persons
2000–2005
Mean
case-fatality
rate
2000–2005*
Burundi
Malawi
Mozambique
Tanzania
Uganda
Zambia
Zimbabwe
Comoros
Kenya
Rwanda
Somalia
Madagascar
Djibouti
Ethiopia
Eritrea
Seychelles
6
6
6
6
6
6
6
5
5
5
5
4
1
1
0
0
121
186
793
100
98
165
64
177
25
14
441
1
31
0
0
0
2.0
1.6
1.1
3.4
3.6
3.7
5.0
1.2
3.3
0.3
3.5
1.9
0.3
0
0
0
Median for region
5
81
1.8
Region of Africa
Eastern Africa
Cameroon
Congo, (Democratic Republic
of the)
Chad
Equatorial Guinea
Gabon
Central African Republic
Congo (Repbulic of the)
Sao Tome & Principe
Angola
6
14
10.2
6
4
2
2
1
1
1
0
242
7
0
0
0
0
0
0
4.1
6.3
0.4
0
2.5
3.7
0.3
0
Median for region
2
0
2.5
Northern Africa
Algeria
Egypt
Libya
Morocco
Sudan
Tunisia
Western Sahara
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
Median for region
0
0
0
Southern Africa
South Africa
Swaziland
Botswana
Lesotho
Namibia
6
6
0
0
0
147
133
0
0
0
0.7
9.5
0
0
0
Median for region
0
0
0
Western Africa
6
6
6
6
6
6
6
5
5
4
66
151
48
594
19
23
119
31
50
18
Median
incidence
per million
persons
2000–2005
Mean
case-fatality
rate
2000–2005
Guinea-Bissau
Mauritania
Senegal
Sierra Leone
The Gambia
Cape Verde
4
3
2
2
1
0
140
6
0
0
0
0
0.8
4.2
0.4
1.4
1.0
0
Median for region
5
27
2.2
Region of Africa
* Rounded to the nearest tenth.
Middle Africa
Benin
Ghana
Guinea
Liberia
Niger
Nigeria
Togo
Cote d’Ivory
Mali
Burkina Faso
Number of
years
reporting
cholera
2.4
2.0
9.6
0.6
7.9
3.9
4.8
6.2
7.7
0.9
million). Three (Mozambique, Liberia, and the Democratic
Republic of the Congo) of these four countries also reported
cases of cholera in all 6 years (Table 2, Figure 3), indicating
highly endemic cholera as well.
Cholera mortality within Africa. The discovery and widespread adoption of oral rehydration therapy in the past 40
years revolutionized cholera treatment,23 resulting in a reduction of the global CFR from 9.1% in the 1970s to 1.7% in 2005
(Table 1, Figure 4). The CFR decreased in Africa as well—
from 10.4% in the 1970s to 1.8% in 2005—but it lags behind
other areas of the world (Table 1, Figure 4). From 2000–2005,
the mean CFR was greater than 5% in eight countries: Cameroon (10.2%), Guinea (9.6%), Swaziland (9.5%), Niger
(7.9%), Mali (7.7%), Chad (6.3%), Cote d’Ivoire (6.2%), and
Zimbabwe (5.02%) (Table 2, Figure 5). Most of these countries are in Western or Middle Africa. The 2.4% overall CFR
seen in Africa from 2000–2005 was similar to that achieved in
Asia by the 1980s. The CFR for all parts of the world outside
of Africa has been below 1.4% since 2001 and below 0.4%
since 2002; the CFR for Africa has never been below 1.5%
(Table 1, Figure 4). If the CFR in Africa in 2005 had been as
low as it was in the rest of the world in 2005 (0.6%), 1,480
fewer persons would have died of cholera.
DISCUSSION
In the twenty-first century, sub-Saharan Africa bears the
brunt of reported global cholera morbidity and mortality. The
region is broadly affected by cholera, and intense epidemic
activity coexists with a high level of endemicity across the
continent. Though they have decreased since previous decades, reported case-fatality rates for cholera remain higher
in Africa than elsewhere. Many countries face the dual challenges of improving both cholera treatment and prevention.
The successful control of the pandemic in Latin America in
the past decade suggests that strategic interventions could
reduce Africa’s cholera burden in the future.
Water and sanitation infrastructure. Past epidemiologic
studies have demonstrated the central role of waterborne and
foodborne transmission as well as hygiene for cholera in the
African setting.5,24 The potential for epidemic cholera is large
where adequate water and sanitation infrastructure is lacking,
as is the case in much of sub-Saharan Africa.25 In 2002, only
58% of the population of sub-Saharan Africa had access to
improved water sources—up from 49% in 1990—but substantially lower than all four Asian regions, northern Africa, and
710
GAFFGA AND OTHERS
FIGURE 4. Cholera case-fatality rate reported to WHO by region (World, Africa, Asia, Latin America) and year, 1960–2005. *Includes
indigenous and imported cases of cholera. Does not depict cholera trends in Europe or Oceania.
Latin America (coverage rates between 78% and 90%),26 and
the number of Africans without access to improved water
sources increased by 23% from 1990–2004.27 Despite modest
improvements in access to improved sanitation, sub-Saharan
Africa fell by this measure from fourth place in 1990 (32%
coverage) to last place in 2002 (36% coverage).26 In 2004,
over 30% more Africans lacked access to sanitation than in
1990. Sub-Saharan Africa remains the region where the Millennium Development Goal to halve the proportion of persons without access to safe drinking water and sanitation by
2015 is least likely to be met.
The impact of specific improvements in drinking water and
sanitation on the Latin American epidemic has been documented in at least two countries. In Santiago, Chile, construction of a long-planned sewage treatment plant was stimulated
by the first cases of cholera in 1991. After this intervention,
cholera cases stopped occurring, cases of hepatitis A decreased by 64%, and cases of typhoid fever decreased by 83%
within 2 years.28 In Mexico, the response to epidemic cholera
in the 1990s included major nationwide investments in drinking water and sanitation infrastructure, leading to an increase
in the percent of municipalities with potable water from 55%
in 1990 to 91% in 1998.29 After these interventions and efforts
to improve access to proper oral rehydration therapy, cholera
FIGURE 5. Cholera mortality: endemicity and mean case-fatality rate of cholera reported to WHO by country, Africa, 2000–2005. The number
appearing over each country represents the number of years between 2000 and 2005 in which the country reported cases of cholera.
711
CHOLERA: A NEW HOMELAND IN AFRICA?
was brought quickly under control, and overall diarrhearelated mortality dropped by an average of nearly 18% per
year from 1990–1993.29
Although universal access to piped treated water is essential for the long-term prevention and control of cholera and
other waterborne diseases, it will be many years before this is
available throughout Africa. In the interim, practical and inexpensive approaches such as household water treatment programs, can greatly reduce the risk of cholera transmission and
other waterborne diseases.30 Programs developed by the Pan
American Health Organization and the Centers for Disease
Control and Prevention to locally produce and promote sodium hypochlorite bleach for household water treatment and
safe vessels for household water storage were successful components of cholera prevention and control programs in many
Latin American countries, including Mexico.29,31 Within the
past 5 years, household water treatment and safe storage programs have been launched in 13 countries in sub-Saharan
Africa: Burundi, Cameroon, Ethiopia, Guinea, Kenya, Madagascar, Malawi, Mozambique, Nigeria, Rwanda, Tanzania,
Uganda, and Zambia.32 Their value in cholera prevention has
been demonstrated in Madagascar.33 Other approaches to
treatment of drinking water at the point of use have also been
shown to successfully reduce cholera transmission. Solar disinfection has been used in Kenya to prevent cholera in children.34 In rural Bangladesh, the use of sari cloth, folded several times, as a filter reduced cholera transmission and incidence through the removal of the copepods to which most
Vibrio cholerae are attached.35 It is unknown whether this
method would have as great an impact on other waterborne
illnesses caused by microorganisms that do not attach to copepods, nor has it been tested in Africa with locally available
cloth.
Access to adequate health care. The persistently high casefatality rate in sub-Saharan Africa may reflect more general
problems in access to effective health care. The average
health care bed/population ratio in sub-Saharan Africa is onetenth the average for developed countries and half the average seen in other developing countries.36 With only 2.3 health
workers per 100,000 people, Africa also has a smaller health
workforce than any other region.37 Access to health facilities
also depends on readily available transportation for patients
too ill to walk. In 1999, a median of only 12% of roads in
Africa were paved compared with 20% of roads in Latin
America and 75% of roads in Asia, respectively.38 The relative paucity of healthcare beds, personnel, and paved roads
suggests that access to lifesaving rehydration therapy is more
limited in Africa than in other regions. The quality of care
that patients with cholera receive after they arrive in health
facilities also influences the outcome of the illness. Use of oral
rehydration therapy and proper case management of diarrhea
in Africa is suboptimal,39 and recent data from Demographic
and Health Surveys conducted in Africa from 1988–2003 indicate that the proportion of children under 5 years old with
diarrhea who did not receive oral rehydration solution or
increased fluids during diarrhea episodes actually rose in nine
of ten African countries.40
Social disruption and poverty. Social disruption and poverty contribute to the spread and lethality of epidemic cholera. Since 1980, 28 (56%) of the 50 nations in sub-Saharan
Africa have been at war.41 Resulting migrations disrupt access to clean water, waste disposal, and health care.42 Large
internally displaced and refugee populations in Africa have
suffered highly lethal cholera epidemics.43 For example, the
large epidemic in Goma in 1994 resulted in an estimated
58,000 to 80,000 cases of cholera within 1 month and a casefatality rate of at least 6%.44,45
During the epidemic in Latin America, cumulative cholera
incidence was strongly correlated with low scores on several
socio-economic development indices, and particularly with a
high infant mortality ratio (IMR), which may reflect exposure
to fecally contaminated water and food among the population.46 Cumulative incidence decreased in countries with IMR
of less than 40 per 1,000 live births. In 2001, the mean IMR of
sub-Saharan African countries was 91, and 42 (95%) of 44
countries in that region had an IMR above 40.47
Malnutrition and other health conditions. Underlying malnutrition may also increase the risk of cholera mortality. Undernourished infants, particularly those suffering from deficiencies of zinc and vitamin A, appear to be more susceptible
to death from diarrheal disease.48,49 Children in many subSaharan countries are likely to suffer from malnutrition and
micronutrient deficiency; vitamin A deficiency is particularly
prevalent in sub-Saharan Africa and southern Asia.50,51 Although we are unaware of any direct association between
cholera susceptibility or severity and either malaria or HIV/
AIDS—two infections that are prevalent in Africa—it is possible that co-infection could result in poorer cholera outcomes.
Cholera vaccines. Recent studies have documented that licensed vaccines against cholera can be used safely in Africa in
refugee populations52 and in adults with HIV infection.53 In
addition, a recent mass vaccination campaign in a cholera
endemic area of Mozambique showed that the two-dose recombinant cholera-toxin B subunit, killed whole cell vaccine
was highly effective against clinically significant cholera in an
urban sub-Saharan African population with a high prevalence
of HIV infection.54 Although cholera vaccines are not yet
appropriate tools for long-term cholera prevention and control in Africa because of their high cost and short duration of
protection, they may have a useful role to play in specific
situations, such as the temporary protection of populations at
high risk.55,56 WHO does not routinely collect data on the
age of patients with cholera or cholera fatalities, and the
data presented here are insufficient to assess the potential
value of interventions, such as cholera immunization, which
could be targeted to specific age groups. Currently available
cholera vaccines are not licensed for use in children under 2
years old.
LIMITATIONS
Although under the International Health Regulations notification of cholera cases and deaths to WHO is mandatory,
reporting of cholera cases and deaths is grossly incomplete
because of poorly functioning surveillance systems and political and economic concerns.6 WHO estimates that the officially reported cases represent only 5%–10% of actual cases
worldwide.57 Regional biases in reporting and differences in
cholera surveillance case definitions and capacity could
heighten or diminish the relative predominance of cholera in
Africa. Some countries bound by strong trade and travel relations to the Far East and the Middle East, where cholera is
rare and the likelihood of economic and social sanctions is
high, may be particularly reluctant to report cholera. Surveil-
712
GAFFGA AND OTHERS
lance for many diseases, including cholera, may have improved in Africa over recent years as a result of investments
in guinea-worm and polio eradication, measles elimination,
the control and prevention of HIV/AIDS, and general public
health infrastructure.
Another data source indicates the dominant role of Africa
in the global cholera picture. The Program for the Monitoring
of Emerging Diseases (ProMED) is an electronic information
system that reports morbidity and mortality data from a variety of official and unofficial sources58 and thus may be less
subject to the biases that affect national cholera reporting to
WHO. Between 1995 and 2005, Africa was the site of 417
(66%) of the 632 cholera outbreaks reported by ProMED and
of 88% of the total number of cases during this period.58
Under the new revised International Health Regulations
scheduled for implementation in 2007, reporting and verification of cholera outbreaks, cases, and deaths to WHO from
all regions may improve.59
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
CONCLUSIONS
24.
The sustained high incidence of cholera in sub-Saharan Africa for over 35 years indicates that it could persist indefinitely. However, the control of epidemic cholera in Latin
America repeats the historical lessons that improving water
and sanitation coverage and increasing access to health care
can control cholera transmission and death. Though lessons
from the epidemiology of cholera in other parts of the world
are important, solutions to the African cholera problem must
be workable in African communities. The impact of prevention efforts can be measured through basic surveillance data,
including the data reported annually to WHO, and corroborated by more detailed studies in the field. Cholera in Africa
is thus an indicator of progress toward the Millennium Development Goals,60 which lead directly to improved health
and quality of life across the African continent far into the
future.
31.
Received May 25, 2007. Accepted for publication July 9, 2007.
32.
25.
26.
27.
28.
29.
30.
Acknowledgments: We thank Mike Hoekstra for guidance with biostatistics issues and Tracy Ayers for help with construction of figures
for this manuscript.
Authors’ addresses: Nicholas Gaffga, Robert V. Tauxe, and Eric D.
Mintz, Centers for Disease Control and Prevention, 1600 Clifton
Road, NE, Mailstop A-38, Atlanta, GA 30333.
33.
Reprint requests: Nicholas Gaffga, Centers for Disease Control and
Prevention, 1600 Clifton Road, NE, Mailstop A-38, Atlanta, GA
30333. E-mail: [email protected].
34.
35.
REFERENCES
1. Sack DA, Sack RB, Nair GB, Siddique AK, 2004. Cholera. Lancet 363: 223–233.
2. Siddique AK, 1995. Failure of treatment centres to prevent cholera deaths in Goma. Lancet 346: 379.
3. Pollitzer R, 1959. Cholera. Geneva: World Health Organization.
4. Barua D, 1974. Cholera. Philadelphia, London, Toronto: WB
Saunders Co.
5. Wachsmuth I, Blake P, Olsvik O, 1994. Vibrio Cholerae and
Cholera–Molecular to Global Perspectives. Chapter 19–The
Epidemiology of Cholera in Africa. Swerlow DL, Isaacson M
(eds). Washington, DC: ASM Press.
6. WHO, 2000. WHO Report on Global Surveillance of Epidemic-
36.
37.
38.
39.
40.
Prone Infectious Diseases. Geneva: World Health Organization, 1-43.
WHO, 1961. Cholera in 1960. Wkly Epidemiol Rec 36: 150–151.
WHO, 1962. Cholera in 1961. Wkly Epidemiol Rec 37: 254–256.
WHO, 1964. Cholera in 1963. Wkly Epidemiol Rec 39: 478–486.
WHO, 1970. Cholera in 1969. Wkly Epidemiol Rec 45: 269–271.
WHO, 2000. Cholera, 1999. Wkly Epidemiol Rec 31: 249–256.
WHO, 2001. Cholera, 2000. Wkly Epidemiol Rec 76: 233–240.
WHO, 2002. Cholera, 2001. Wkly Epidemiol Rec 31: 257–268.
WHO, 2003. Cholera, 2002. Wkly Epidemiol Rec 78: 269–276.
WHO, 2004. Cholera, 2003. Wkly Epidemiol Rec 79: 281–288.
WHO, 2005. Cholera, 2004. Wkly Epidemiol Rec 80: 223–233.
WHO, 2006. Cholera 2005. Wkly Epidemiol Rec 81: 297–308.
WHO, 1971. Cholera in 1970. Wkly Epidemiol Rec 46: 325–336.
United Nations, 2004. The World Population Prospects, the 2004
Revision. United Nations Department of Education and Social
Affairs. New York: United Nations.
WHO, 1999. Cholera, 1998. Wkly Epidemiol Rec 31: 257–264.
WHO, 2006. Cholera, Angola-Update. Wkly Epidemiol Rec 81:
237–240.
WHO, 2006. Cholera, Southern Sudan-Update. Wkly Epidemiol
Rec 81: 118.
Guerrant RL, Carneiro-Filho BA, Dillingham RA, 2003. Cholera, diarrhea, and oral rehydration therapy: triumph and indictment. Clin Infect Dis 37: 398–405.
CDC, 2004. Cholera epidemic associated with raw vegetables–
Lusaka, Zambia, 2003–2004. MMWR Morb Mortal Wkly Rep
53: 783–786.
Moszynski P, 2006. Cholera outbreak highlights poor health services in southern Sudan. BMJ 332: 570.
WHO and UNICEF, 2005. Water for Life. Making it Happen.
Geneva: World Health Organization and UNICEF.
WHO and UNICEF, 2006. Meeting the MDG Drinking Water and
Sanitation Target: The Urban and Rural Challenge of the Decade. Geneva, New York: World Health Organization and
UNICEF.
Alcayaga S, Alcayaga J, Gassibe K, 1993. Changes in the morbidity profile of certain enteric infections after the cholera
epidemic. Rev Chile Infect 1: 5–10.
Sepulveda J, Valdespino JL, Garcia-Garcia L, 2006. Cholera in
Mexico: the paradoxical benefits of the last pandemic. Int J
Infect Dis 10: 4–13.
Mintz E, Bartram J, Lochery P, Wegelin M, 2001. Not just a drop
in the bucket: expanding access to point-of-use water treatment systems. Am J Public Health 91: 1565–1570.
Reiff FM, Roses M, Venczel L, Quick R, Witt VM, 1996. Lowcost safe water for the world: a practical interim solution. J
Public Health Policy 17: 389–408.
Lantagne D, Quick R, Mintz E, 2007. Household water treatment
and safe storage options in developing countries: a review of
current implementation practices. Water stories: expanding
opportunities in small-scale water and sanitation projects.
Woodrow Wilson International Center for Scholars, 17–38.
Reller ME, Mong YJ, Hoekstra RM, Quick RE, 2001. Cholera
prevention with traditional and novel water treatment methods: an outbreak investigation in Fort-Dauphin, Madagascar.
Am J Public Health 91: 1608–1610.
Conroy RM, Meegan ME, Joyce T, McGuigan K, Barnes J, 2001.
Solar disinfection of drinking water protects against cholera in
children under 6 years of age. Arch Dis Child 85: 293–295.
Colwell RR, Huq A, Sirajul Islam M, Aziz KMA, Yunus M,
Mahmud A, Sack RB, Nair GB, Chakraborty J, Sack DA,
Russek-Cohen E, 2003. Reduction of cholera in Bangladeshi
villages by simple filtration. Proc Natl Acad Sci USA 100:
1051–1055.
Van Lerberghe W, de Bethune X, De Brouwere V, 1997. Hospitals in sub-Saharan Africa: why we need more of what does
not work as it should. Trop Med Int Health 2: 799–808.
WHO, 2006. Health Workers: A Global Profile. The World
Health Report. Geneva: World Health Organization.
International Road Federation, 2001. World Road Statistics.
Geneva: International Road Federation.
Forsberg BC, Petzold MG, Tomson G, Allebeck P, 2007. Diarrhoea case management in low- and middle-income countries–
an unfinished agenda. Bull World Health Organ 85: 42–48.
Ram PK, Choi M, Blum LS, Wamae A, Mintz ED, Bartlett AV,
CHOLERA: A NEW HOMELAND IN AFRICA?
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
2007. 2006 Declines in diarrhoea case management. Bull World
Health Organ In press.
Luckham R, Ahmed I, Muggah R, White S, 2001. Conflict and
poverty in Sub-Saharan Africa: an assessment of the issues and
evidence. Institute of Development Studies Working Paper
128.
Swerdlow DM, Begkoyian G, Nyangulu G, Toole D, Waldman
RJ, Puhr DN, Tauxe RV, 1997. Epidemic cholera among refugees in Malawi, Africa: treatment and transmission. Epidemiol
Infect 118: 207–214.
WHO, 1994. Cholera in 1993. Wkly Epidemiol Rec 69: 205–212.
Siddique AK, Salam A, Islam MS, Akram K, Majumdar RN,
Zaman K, Fronczak N, Laston S, 1995. Why treatment centres
failed to prevent cholera deaths among Rwandan refugees in
Goma, Zaire. Lancet 345: 359–361.
Goma Epidemiology Group, 1995. Public health impact of
Rwandan refugee crisis: what happened in Goma, Zaire, in
July 1994? Lancet 339–344.
Ackers ML, Quick RE, Drasbek CJ, Hutwagner L, Tauxe RV,
1998. Are there national risk factors for epidemic cholera? The
correlation between socioeconomic and demographic indices
and cholera incidence in Latin America. Int J Epidemiol 27:
330–334.
United Nations Development Programme, 2003. Human Development Report 2003. New York: United Nations Development Programme. Available at: http://hdr.undp.org/
reports/global/2003/pdf/hdr03_HDI.pdf. Accessed August 15,
2007.
Rahmathullah L, Underwood BA, Thulasiraj RD, Milton RC,
Ramaswamy K, Rahmathullah R, Babu G, 1990. Reduced
mortality among children in southern India receiving a small
weekly dose of vitamin A [see comment]. N Engl J Med 323:
929–935.
Sommer A, Katz J, Tarwotjo I, 1984. Increased risk of respiratory
disease and diarrhea in children with preexisting mild vitamin
A deficiency. Am J Clin Nutr 40: 1090–1095.
WHO, 1995. The global prevalence of micronutrient deficiency.
Micronutrient Deficiency Information Systems Working Paper
51.
52.
53.
54.
55.
56.
57.
58.
59.
60.
713
2:WHO/NUT/95 3. Geneva. Available at: http://
whqlibdoc.who.int/publications/2004/9241546123.pdf. Accessed April 2007.
UNICEF, 2007. Vitamin A Deficiency: The Challenge UNICEF
Statistics. Available at: http://www.childinfo.org/areas/
vitamina/. Accessed April 2007.
Legros D, Paquet C, Perea W, Marty I, Kenya Mugisha N, Royer
H, Neira M, Ivanoff B, 1999. Mass vaccination with a two-dose
oral cholera vaccine in a refugee camp. Bull World Health
Organ 77: 837–842.
Perry RT, Plowe CV, Koumare B, Bougoudogo F, Kotloff KL,
Losonsky GA, Wasserman SS, Levine MM, 1998. A single
dose of live oral cholera vaccine CVD 103-HgR is safe and
immunogenic in HIV-infected and HIV-noninfected adults in
Mali. Bull World Health Organ 76: 63–71.
Lucas ME, Deen JL, von Seidlein L, Wang XY, Ampuero J, Puri
M, Ali M, Ansaruzzaman M, Amos J, Macuamule A, Cavailler
P, Guerin PJ, Mahoudeau C, Kahozi-Sangwa P, Chaignat CL,
Barreto A, Songane FF, Clemens JD, 2005. Effectiveness of
mass oral cholera vaccination in Beira, Mozambique. N Engl J
Med 352: 757–767.
Cookson ST, Stamboulian D, Demonte J, Quero L, Martinez de
Arquiza C, Aleman A, Lepetic A, Levine MM, 1997. A costbenefit analysis of programmatic use of CVD 103-HgR live
oral cholera vaccine in a high-risk population. Int J Epidemiol
26: 212–219.
WHO, 2001. Cholera vaccines. Wkly Epidemiol Rec 76: 117–124.
WHO, 2007. Cholera surveillance and number of cases. Available
at: http://www.who.int/topics/cholera/surveillance/en/
index.html. Accessed May 2007.
Griffith DC, Kelly-Hope LA, Miller MA, 2006. Review of reported cholera outbreaks worldwide, 1995-2005. Am J Trop
Med Hyg 75: 973–977.
WHO, 2005. International Health Regulations. Available at:
http://www.who.int/csr/ihr/en/index.html. Accessed August 15,
2007.
United Nations, 2005. The Millennium Development Goals Report, 2005. New York: United Nations, 1-48.