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Cholera: A New Homeland in Africa?

ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION LIMITATIONS CONCLUSIONS REFERENCES

 
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.

INTRODUCTION

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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 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.

METHODS

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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 1970^7–10; 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 reports^8,9; 1964–1969 data came from a summation of all of the cholera deaths reported in the individual Weekly Epidemiologic Reviews that contained information 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 1971^8,9,18; 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

RESULTS

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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).

View larger version (17K): [in this window] [in a new window]       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.

View larger version (17K): [in this window] [in a new window]       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.

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 sub-Saharan 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

View larger version (38K): [in this window] [in a new window]       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.

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.

View larger version (13K): [in this window] [in a new window]       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.

View larger version (35K): [in this window] [in a new window]       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.

DISCUSSION

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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 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 was brought quickly under control, and overall diarrhea-related 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 cope-pods, nor has it been tested in Africa with locally available cloth.

Access to adequate health care. The persistently high case-fatality 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 one-tenth 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 case-fatality rate of at least 6%.^44,45

During the epidemic in Latin America, cumulative cholera incidence was strongly correlated with low scores on several socioeconomic 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 sub-Saharan 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

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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. Surveillance 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

CONCLUSIONS

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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.

Received May 25, 2007. Accepted for publication July 9, 2007.

Acknowledgments: We thank Mike Hoekstra for guidance with biostatistics issues and Tracy Ayers for help with construction of figures for this manuscript.

^* Address correspondence to Nicholas Gaffga, Centers for Disease Control and Prevention, 1600 Clifton Road, NE, Mailstop A-38, Atlanta, GA 30333. E-mail: ngaffga{at}cdc.gov

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.

Reprint requests: Nicholas Gaffga, Centers for Disease Control and Prevention, 1600 Clifton Road, NE, Mailstop A-38, Atlanta, GA 30333. E-mail: ngaffga{at}cdc.gov.

REFERENCES

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