The global dimensions of cholera
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The global dimensions of cholera
Cholera remains among the most feared infectious diseases. The first six pandemics of cholera, beginning in 1817, were
major public health emergencies, inflicting high morbidity and mortality across the world. Today we continue to battle
with the seventh pandemic that began in 1961 and shows no sign of abating. Of particular concern is the spatially and
temporally different epidemiological pattern of Vibrio cholerae O1 biotype El Tor cholera. Accompanying these worry-
ing signs is the emergence and spread of V. cholerae O139 Bengal in parts of Asia since the early 1990s. Cholera is
behaving differently and is serving as a barometer of the unhealthy global changes around us.
Kelley Lee
Centre on Globalisation, Environmental Change and Health
London School of Hygiene & Tropical Medicine
Keppel Street, London WC1E 7HT U.K.
e-mail kelley.lee@lshtm.ac.uk
of the disease goes back much further (based on
C
holera remains one of the most feared infectious
diseases in public health. It is an acute bac- references to deaths from dehydrating diarrhoea
terial infection of the intestine caused by by Hippocrates and Sanskrit writings). From the
the ingestion of food or water contaminated by nineteenth century onward, cholera spread to other
certain strains of the Vibrio cholerae organism. V. parts of the world in seven pandemic waves. The
cholerae produces enterotoxins (toxins which act fi rst six pandemics of “classical” cholera left in their
in the gastrointestinal tract) whose actions on the wake high levels of morbidity and mortality, along
mucosal epithelium is responsible for the character- with much social and political upheaval.[1,2] Each
istic symptoms of the disease, namely acute watery time, however, cholera retreated back to South Asia
diarrhoea and vomiting. In the most severe cases, where it remains endemic to the present day. In
cholera is one of the most rapidly fatal illnesses 1961, a different strain of cholera, El Tor, spread
known, due to severe dehydration or water loss. If from Southeast Asia to become the seventh pan-
left untreated, mortality from “classical” cholera demic. Today, we continue to battle with this sev-
can be 50%. A healthy person may become hypo- enth pandemic which shows no sign of abating.
tensive within an hour of the onset of symptoms An eighth pandemic may be waiting in the wings,
and may die within 2-3 hours although more usu- again a new strain of cholera known as V. cholerae
ally death may come within a day or so. Death in O139 Bengal that is slowly spreading across parts of
this way prompted the French to call cholera mort Asia.
de chien (the dog’s death). With effective treatment, Since the isolation of the infectious agent by
through fluid and electrolytes replacement, mortal- Robert Koch in 1883, we have continued to stead-
ity can be reduced to less than 1%. Affected indi- ily advance our knowledge of the disease. We have
viduals are highly infectious, contaminating water mapped the entire DNA sequence of Vibrio chol-
and food sources that they come into contact with. erae [3] , learned how the O1 strain evolved to become
Therefore, the appearance of epidemic forms of lethal, and improved treatment, including use of
cholera is treated as a public health emergency. antibiotics, despite growing antimicrobial resist-
Until 1817, cholera largely remained a disease ance.[4]
of South Asia. Epidemics of cholera-like diseases The continuing challenges of cholera in the early
on the Indian subcontinent have been recorded twenty-fi rst century are integrally linked to the
from the early sixteenth century, and the history nature of the global changes around us. Processes
GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001) 6 © Kluwer Academic Publishers
feature
of globalisation, and how these processes are affect- diseases (along with plague, yellow fever, smallpox
ing the broader determinants of health including and louse-borne typhus) regulated under the fi rst
our social and natural environments, are core fac- International Sanitary Regulations (known today as
tors in the way cholera itself has changed. Global the International Health Regulations). Thus, his-
technological, economic, political and environmen- torical records allow us to analyse trends over a rel-
tal changes are invariably intertwined and cannot atively long time period and compare them with
be separated from the epidemiology of the disease. more recent trends in incidence and mortality.
This raises clear implications for how we think about Cholera was confi ned to the riverine areas of
infectious disease control amidst globalisation, and the Indian subcontinent since at least the early six-
the actions needed to put the protection of public teenth century. There were occasional outbreaks
health more centrally at the heart of global govern- along China’s coastal communities from contact
ance.[5,6] with trading ships from South Asia, and in the
Middle East among pilgrims travelling to Mecca.
Cholera in historical context: a barometer of inequity It was a much feared disease and its devastating
Cholera, particularly, lends itself to historical anal- impact led to the creation of an Indian goddess of
yses because it is the fi rst disease for which modern cholera, Sheetola.[7]
public health surveillance, monitoring and report- In 1817, cholera began to spread worldwide and
ing was undertaken in an organised way. As a highly over the next one hundred years, there were six
infectious and, in the nineteenth century, extremely pandemics (Table 1). Medical historians attribute
lethal disease, it was included as one of a handful of this change to the colonisation of the region by
Figure 1 Boy washing dishes in polluted irrigation canal in the Philippines (Source: M/MC Photoshare, www.jhuccp.org/mmc).
© Kluwer Academic Publishers
7 GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001)
The global dimensions of cholera
Table 1 Dates of the first six cholera pandemics Table 2 Cholera cases and fatalities reported in PAHO region,
1991-1999
pandemic year
year number of number of number of
1 (6 years) 1817-1823 cases deaths countries
2 (12 years) 1826-1838 affected
3 (16 years) 1839-1855
4 (11 years) 1863-1874 1991 391 751 ~ 4 000 16
5 (15 years) 1881-1896 1992 352 300 1 692 20
6 (24 years) 1899-1923 1993 204 543 2 362
1994 195 574 1321
1995 85 802 837 14
1996 ~21 000 ~266
European powers, resulting in intensified migra- 1997 17 760 225
tion, socioeconomic restructuring of local commu- 1998 57 106 558 16
nities, and alterations to the natural environment. 1999 8 126 103 12
More specifically, under the impact of the Industrial
Revolution, the character of European imperialism Source Compiled from Pan American Health Organization,
changed. Early European imperialism focused on a 1996; Tauxe R. et al. Epidemic Cholera in the New World:
search for the riches of the Orient, and the estab- Translating Field Epidemiology into New Prevention Strategies.
lishment of trading stations and strategic outposts Emerging Infectious Diseases, 1995; 1(4):
in Asia and Africa to protect them. In the nine-
teenth century, however, the enforced opening of
the world to European (notably British) commerce
was enacted. This occurred in Turkey and Egypt the ensuing scandal famously led to the organiza-
(1838), Persia (1841), China (1842) and Japan tion of proper military nursing services by Florence
(1858). Hence, the movement of traders, military Nightingale.[9] A substantial proportion of the pop-
personnel, camp followers and immigrants between ulation living in the industrial slums of large cities
Europe and Asia increased substantially from the or affected by military confl ict, lived in squalid con-
early nineteenth century. In South Asia, this inte- ditions with poor access to clean water and san-
gration of the region into the British empire led to itation. As a water-borne disease spread by the
the construction of poor draining irrigation canals oral-faecal route, cholera became a regular visitor,
to raise cash crops (e.g. tea, opium), impoverish- resulting in hundreds of thousands of deaths during
ment of local peoples by land reforms and taxa- each pandemic. Mortality associated with “classi-
tion, and mass migration as a result of economic cal” cholera was approximately 50%. The lack of
hardship. Cholera became endemic throughout the scientific understanding of how the disease spread,
region, and then to spread beyond the region to the poorly developed public health systems and,
Europe, Africa and eventually the Americas.[8] perhaps most importantly, prevailing social atti-
In Europe, cholera found hospitable conditions tudes and complacency towards the conditions of
for spreading far afield. European societies were poor and vulnerable populations allowed cholera to
undergoing significant social and economic transi- return time and again.
tion, including growing levels of human migration, Effective public health response to the disease
urbanisation, socioeconomic inequality, and inad- was slow in coming. Even John Snow’s famous
equate water and sanitation facilities. Military con- removal of the Broad Street pump in 1854 did
fl ict and social upheaval resulted in soldiers living in not defi nitively change the prevailing attitude that
appalling, crowded conditions. They became effec- cholera was due to immorality and lack of “proper
tive vectors of a variety of diseases including syph- habits”.[8] It was not until thirty years later, with
ilis, tuberculosis, typhus and typhoid fever. The Koch’s important work in isolating the bacillus
Crimean War (1853-1856), in particular, resulted Vibrio cholerae as the causative agent of cholera,
in such high numbers of deaths from disease that that the inertia of government policy began to shift.
GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001) 8 © Kluwer Academic PublishersThe global dimensions of cholera
The development of public health infrastructure, the Sinai peninsula where it was fi rst isolated in
and the growing use of epidemiological methods to 1905 from the intestines of pilgrims returning from
understand diseases such as cholera, were together Mecca). There is uncertainty as to why El Tor
underpinned by wider social reforms to improve assumed pandemic form when it did, and why it has
housing, nutrition and sanitation. subsequently spread worldwide to replace the clas-
Cholera traveled to the Americas via intensi- sical biotype. One theory from evolutionary biology
fying migration to the New World. The speed of argues that, when sanitation improves, selection
spread was dependent on contemporary modes of acts against V. cholerae O1 classical in favour of the
transport. The advent of the steamship and rail- more benign El Tor biotype. The more virulent and
way, in particular, sped the transmission of cholera lethal classical biotype kills the host more quickly
across larger distances. Consequently, each subse- and, in doing so, shortens the period, reducing the
quent pandemic encompassed a larger area than opportunity for infection of other potential hosts.
the previous. Coinciding with these spatial pat- The lower virulence of El Tor results in less severely
terns were burgeoning trade, migration, political ill, thus more mobile, hosts capable of infecting
and cultural links across the world, what Robert- others over a longer period of time.[11] By 1964,
son describes as the Incipient (mid eighteenth cen- El Tor cholera had reached South Asia, become
tury to 1870) and Take Off (1870 to the mid 1920s) endemic in the region and largely replaced V. chol-
phases of globalisation.[10] The fi rst saw the begin- erae O1 classical.
nings of the admission of non-European societies The behaviour of El Tor cholera over the next
to “international society”, while the second saw a forty years t has been distinct from the fi rst six
sharp increase in global forms of transportation pandemics in a number of ways.[12] First, the sev-
and communication technologies. With intensifying enth pandemic has behaved differently along the
(frequency) and extensifying (geographical reach) spatial dimension of globalisation. The pandemic
links among societies on many continents, cholera has affected a more widespread and greater geo-
and other infectious diseases were spread more graphical area, including regions which had always,
quickly and farther afield. Indeed, it was cholera’s or for a significant period, been cholera free. The
clearly crossborder nature that made it a keen sub- number of countries affected continues to increase,
ject of negotiation at the periodic International San- and it is becoming endemic in an increasing number
itary Conferences held between 1851-1911. Focused of areas. Furthermore, the pattern of spread across
narrowly on minimising the impact of certain infec- geographical areas has not been linear, (spreading
tious diseases on flourishing international trade, from country to country), but in some cases, has
standard practices for shared surveillance, monitor- “hopped continents”, showing up unexpectedly in
ing and reporting of outbreaks were agreed upon by different regions of the world. Some of the major
the leading powers of the day. outbreaks over the past four decades have occurred
Eventually, major welfare reforms, improve- in Peru in 1991, Soviet Union from 1961 onwards,
ments in basic living conditions, such as housing, and South Africa from August 2000.
sanitation and dietary standards, led to the virtual The second important difference is that the sev-
disappearance of cholera from most industrialised enth pandemic has demonstrated temporal differ-
countries by the mid 1920s. ences both in the speed with which the disease has
spread and the duration of the pandemic. In the
Cholera and contemporary globalisation: nineteenth century, cholera transmission traveled
what is the seventh pandemic telling us? across countries and continents as quickly as people
After each of the fi rst six pandemics, V. cholerae moved via prevailing modes of transport. In the
O1 classical retreated to South Asia where it twentieth century, of faster modes, reduced costs,
remained endemic. Regular reports of cases con- and increased frequency of transport by airplanes,
tinued between 1923-1961, but pandemic cholera automobiles, shipping and high speed trains, have
disappeared for 38 years. The seventh pandemic led to the disease travelling much faster rate than
began in Sulawesi, Indonesia in 1961, this time earlier. The longest previous pandemic was the
caused by a different biotype, V. cholerae O1 El sixth pandemic that lasted 24 years (1899-1923). As
Tor (named after the El Tor quarantine camp on of 2001, the seventh pandemic has lasted forty years
© Kluwer Academic Publishers
9 GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001)The global dimensions of cholera
and shows no sign of abating. Despite the advent ation with certain aquatic plants and animals, so
of modern public health systems and effective treat- water is an important reservoir for infection.[14]
ments in many parts of the world, the number of The nature of the social and natural environ-
cholera cases continues to grow. In the late 1990s, mental changes being created by processes of glo-
there was a dramatic increase in the number of balisation plays an important role in the spatial
cholera cases worldwide, with an almost doubling and temporal differences of the seventh pandemic.
of cases between 1997 and 1998.[13] In particular, V. cholerae O1 El Tor has remained
An important determinant of the epidemiology closely associated with poverty and deprivation with
of the seventh pandemic is due to the differences in its poor sanitation and lack of access to clean water.
the V. cholerae biotypes. Although V. cholerae O1 El In the Celebes Islands of Indonesia, poor sanita-
Tor serotype Ibana is a less virulent strain than V. tion because of overpopulation of urban peripher-
cholerae O1 classical, it causes a higher proportion of ies, military operations, and other environmental
asymptomatic infections (1:30-100 compared with disturbances, combined with certain cultural prac-
1:2-4), and thus allows carriers to spread the dis- tices (e.g. use of night soil) contributed to the local
ease unknowingly through contamination of food cholera epidemic in the early 1960s.[15] An analysis
or water. The duration of carriage after infection of four cholera outbreaks during the current pan-
is longer for El Tor, the organism grows in many demic suggests that global changes are intimately
foods, survives longer in the natural environment linked to its continued public health challenge.
(it is one of the most resistant to adverse environ-
mental conditions), and shows a greater resistance
to antibiotics and chlorine. It also lives in associ-
Figure 2 Women and children bathing and washing clothes in a river in Bangladesh (Source: M/MC Photoshare, www.jhuccp.org/mmc).
GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001) 10 © Kluwer Academic PublishersThe global dimensions of cholera
Cholera returns to Latin America close trading relations with Asia. Nonetheless, the
Cholera arrived, as a vulture, in one of the bleakest peri- towns are extremely polluted with toxic and biolog-
ods of Peru’s contemporary history.[16] ical waste from the fishery industry. For example,
After disappearing from the western hemisphere Chimbote is described as one of the most polluted
for almost a century, cholera was simultaneously towns in Peru, with the fishery industry discharging
reported in January 1991 in three coastal towns 1570 metric tonnes of waste into the bay daily and
in Peru. The epidemic that ensued moved with other industries dumping another 100 metric tons
“unprecedented speed and intensity”, according to on adjacent lands daily.[16] Rapid population growth
WHO reports, with 12,000 confi rmed cases by mid in Lima and other coastal cities has also exerted
February. The disease then traveled two thousand stress on the local environment, with demand
kilometers along the coast to Ecuador, reaching exceeding the infrastructure’s capacity to supply
Colombia and Chile by March-April. By the end clean water and sanitation.
of 1991, there were nearly 400,000 cases and more There is extreme socioeconomic inequality in
than 4,000 deaths. By all accounts, the epidemic this region. Sixty percent of the Peruvian popula-
was a major public health emergency, with more tion (13 million people) live in poverty, with more
cases reported in one year than total reported than half living in “critical poverty” (unable to meet
during the previous five years. The cause of the ini- basic needs in housing, health and education) and
tial outbreak remains unclear and subject to some three million living in “extreme poverty” (unable to
speculation. Many believe that the disease was purchase minimum daily nutritional requirements
transported to the region by a Chinese grain ship, of calories and protein). The poorest 30% of pop-
the Feng Xian, which arrived in the Peruvian town ulation earn less than 5% of national income.
of Chimbote to pick up a cargo of fishmeal. With Some of the root causes lie far beyond the country
several ill and infected crew members on board, the itself. Economic problems of the 1980s led to
ship released infected bilge water into the coastal the election of President Fujimori and the intro-
waters. Vibrio cholerae then infected the local shell- duction of economic stabilisation measures (known
fish that were eaten by people. The outbreak of as “Fujishock”) and the World Bank-backed struc-
El Tor cholera in the U.S. Gulf Coast is similarly tural adjustment programme in 1990. The social
thought to have arrived, in turn, by ships from consequences of such policies, and their dispropor-
Latin America.[17] tionately adverse impact on the poor, are widely
While this theory that transoceanic shipping was acknowledged today. Within 18 months poverty in
the initial cause of the outbreak is questioned by Peru increased by 11%.[19] Over the past twenty
some, it is widely recognised that ballast water from years, urban dwellers’ access to safe drinking water
shipping is a major culprit in the spread of aquatic declined from 72% to 24%. Government expend-
species. As French writes, some 3,000-10,000 spe- iture on the public health system also fell signifi-
cies are moving around the world on any given cantly during this period from 0.23% of GNP in
day in ship ballast. Wherever these waters are dis- 1982 to 0.04% in 1992, and decreased six-fold over
charged, so too are these organisms causing, in the previous year during the fi rst six months of the
some cases, serious threats to local environments. Fujimori government. Public expenditure on health
Examples of ship induced “bioinvasions” include care and disease prevention decreased from US$77
the Atlantic jellyfish in the Black Sea and zebra million in 1982 to U$2 million in 1990. As Panniset
mussel in the U.S. Great Lakes. The likelihood of concludes, “The Peruvian case demonstrates that
such occurrences has undoubtedly been increased the power of OECD countries (exerted, in this case,
by the intensification of trade links in the twentieth through the World Bank and the IMF) to interrupt
century, including the use of ever larger ships.[18] or promote Peru’s commercial and fi nancial rela-
As well as illustrating global interconnected- tions ultimately had an impact on the outcome of
ness through trade, the outbreak drew poignant the epidemic. The exercise of this power affected
attention to the susceptibility of the communities governmental policies to confront the epidemic and
affected. The coastal Peruvian towns of Chimbote, caused further deterioration of social conditions.”[16]
Piura and Chancay are located in a relatively eco- An alternative explanation for the Peruvian out-
nomically developed area of Peru with particularly break comes from research by Rita Colwell and
© Kluwer Academic Publishers
11 GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001)The global dimensions of cholera
others who believe that global climatic changes may Lima arrived in Los Angeles in March 1992 with
be responsible. She starts by challenging the rela- 65 people ill with cholera. The incident triggered a
tionship between V. cholerae and the natural envi- high-level diplomatic exchange between the presi-
ronment, arguing that “Cholera bacteria are part of dents of Argentina and Peru who argued over which
the natural ecology; they are in the environment, country was to blame, both seeking to avoid having
and this wasn’t accepted by the medical community their countries labeled as unable to control the dis-
for years. They thought it was person to person, ease.[23][24] Such unfortunate incidents did little to
but it is much more complicated than that”.[20] Of prevent major impact on the region’s economies. It
particular interest is the sea current, El Nino, that is estimated that in 1991, Peru’s tourist industry lost
comes from the north to the south along the South US$150 million, and tourist revenue to the region
American coast in the Pacific Ocean. This takes fell by US$750 million,[25] shrimp exports declined
place each year at the end of December and begin- by US$270 million, overall losses were estimated
ning of January. In 1991, this current produced a at US$770 million.[26] Within weeks of the out-
higher temperature than usual in that part of the break, the members of the European Community
Pacific Ocean. Warmer temperatures led to a higher and many other countries introduced restrictive
than average phytoplankton bloom upon which zoo- measures and even embargoes on many Peruvian
plankton feed. A proliferation of zooplankton, in imports. Some countries, such as the U.S., intro-
turn, can result in an increased number of vibrios duced measures beyond those recommended by
carried on zooplankton. The outcome is an infec- WHO to protect public health. For countries already
tious load of V. cholerae that can infect people who struggling fi nancially to provide basic public health
drink water inhabited with zooplankton, or eat fish services, the economic impact of the outbreak fur-
and shellfish that have eaten zooplankton. This ther undermined the capacity of governments to
may explain the simultaneous outbreak in different address the underlying socioeconomic causes of the
towns along the Peruvian coast and the time of year epidemic in the longer term.
of the outbreak.[21] While the link between the El
Nino and the 1991 outbreak is debatable, the cli- Cholera in Africa: the South African epidemic (2000-present)
mate-induced disasters that befell Central America A time bomb ticking away….[27]
in the late 1990s, notably Hurricane Mitch, had The El Tor cholera pandemic reached Africa in
a clear impact on number of cholera cases. The August, 1970, with the identification of the fi rst
number of cases were declining again up to 1997, case in Guinea. The disease was most likely intro-
but there was a resurgence in 1998 with over 300% duced by a symptom-free infected traveler return-
more cases than in the previous year. Peru, again, ing from a cholera-endemic area in Asia, possibly as
led the way with a major outbreak in the fi rst three part of the massive population movement resulting
months of 1998. By 1999 there was a decline of 86% from the war between Pakistan and India. The dis-
in the number of cases reported.[22] ease spread quickly to 30 of the 46 countries in the
The consequences of the cholera epidemic have region, resulting in more than 150,000 cases and
global dimensions. A transborder public health 20,000 deaths. By 1990, Africa accounted for 90%
threat such as infectious disease has potentially of cases reported to WHO.[28] Particularly vulner-
widespread knock on effects. Government officials able has been the Horn of Africa, where almost all
in Peru and then other affected countries moved countries host refugees or have internally displaced
quickly to downplay any public health risk from populations. There is a high risk of cholera among
fish exports (the fishing industry is one of Peru’s these vulnerable populations because of poor san-
primary industries employing around 56,000 Peru- itary conditions and overcrowding in temporary
vians) and to tourists. Perhaps, most memorable settlements. The worst outbreak was among Rwan-
is the now infamous gesture in 1991 by the then dan refugees in relief camps in Goma, Zaire, and
Peruvian minister of health to calm public alarm resulted in 70,000 cases and 12,000 deaths.[29] In
by eating a local raw fish delicacy (ceviche) on the late 1990s, the heavy rains and flooding, due to
television. The broadcast had the opposite effect, El Nino, affected cholera in the region, particularly
however, when the minister subsequently developed in Kenya, Uganda, Somalia, Zanzibar and Mozam-
cholera. Similarly, a fl ight from Buenos Aires and bique. Poor hygiene and unsanitary conditions in
GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001) 12 © Kluwer Academic PublishersThe global dimensions of cholera
Figure 3 Panoramic view from the city of Huancavelica in Peru (Source: M/MC Photoshare, www.jhuccp.org/mmc).
poor communities contributed to cholera’s becom- The root cause of this outbreak the local gov-
ing endemic. ernment authority’s ceasing to provide free water to
In South Africa, cholera has a seasonal pattern local residents. The new policy is a result of ongo-
that appears to follow the ambient local patterns ing pressures on the government to reduce public
of rainfall and temperature. El Tor cholera was spending as part of wider macroeconomic reforms.
fi rst detected in South Africa in 1974, when it was The policy included introducing a charge to very
brought to the country by migrant mine workers. poor people living in a squatter settlement near the
The outbreak remained confi ned to a small number town of Empangeni. The settlement is not unlike
of mines, but subsequent outbreaks have been more many others in South Africa and other African
serious. In October 1980, the fi rst case was detected countries that form from migrating populations
in the KaNgwane area of the Eastern Transvaal, seeking employment. Oftentimes these informal set-
possibly from the same cause, and the ensuing epi- tlements are located near local rivers used for both
demic continued until 1987. How the disease sur- drinking water and sanitation. In South Africa,
vives during inter-epidemic periods remains a point about 80% of poor (largely black) people have no
of speculation. Recently, South Africa experienced running water and a higher proportion have no toi-
its worst cholera outbreak in twenty years, with lets.[30] With reduced access to clean water, and
the fi rst cases of the current epidemic appearing increased use of open river water, the cholera epi-
in August 2000. As of March 2001, almost 46,000 demic has spread rapidly.
people had been infected, with more than 100
deaths. The disease has spread to all but one of
South Africa’s nine provinces.
© Kluwer Academic Publishers
13 GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001)The global dimensions of cholera
A reversal of fortunes: cholera outbreaks in the former Soviet Union in 1817, it is from this region that the most recent
The spread of cholera and other infectious diseases is the changes to the organism have emerged to challenge
calling card of an economy in trouble.[31] the public health community. As described above,
El Tor cholera reached the then Soviet region of from the mid 1960s, V. cholerae O1 classical bio-
Uzbekistan in 1965 through the importation of type was steadily displaced in the region by V.
the disease from Afghanistan. Local outbreaks and cholerae O1 El Tor which, subsequently became
sporadic cases continued to occur in Uzbekistan, endemic. In 1982, a new variant of classical chol-
Turkmenistan and regions of Russia until the late era emerged in Bangladesh, initially displacing, but
1960s. Coinciding with the peaking of the global eventually coexisting with El Tor cholera for almost
pandemic, between 1970 and 1977, cholera spread a decade.[36] However, of even greater concern has
more extensively, with outbreaks in more than 80 been the emergence of V. cholerae O139 Bengal, the
regions of the country. Since 1977, the number fi rst non-O1 strain of cholera that causes an epi-
of cases has declined, although outbreaks have demic form of the disease. V. cholerae O139 was fi rst
occurred periodically in different regions.[35] In the detected in Bangladesh in January 1993 at a gath-
1990s, cholera continued to occur in the region ering of Muslim pilgrims near Dhaka. During the
amidst growing political and economic instability. spring and summer of 1993, the number of V. chol-
During 1994, cholera returned to ten cities in south- erae O139 cases outnumbered those of the O1 sero-
ern and western Ukraine resulting in approximately type, but were on the wane by the autumn. By
20 deaths, and putting about fi fty million people at the end of 1993, 170,000 cases, resulting in 2000
risk. The number of cases has since decline again. deaths. Heavy rainfalls were documented. as con-
In 1998, Russia reported 10 local cases; in 1999, tributing to the high toll. Using a diagnostic serum
Russia reported 3 local and 5 imported cases, while developed in Japan, cases were detected in Thai-
the Ukraine reported 2 local cases. land, Malaysia, Nepal, Pakistan, Burma (Myan-
While the number of cholera cases in the former mar) and China. Imported cases were reported in
Soviet Union remains relatively low compared to the US, UK, Japan, Korea, Hong Kong and Singa-
Africa, Asia and Latin America, the disease can be pore. By 1994, fewer cases of V. cholerae O139 were
seen as an early warning sign of the declining state reported, and the epidemic was essentially over by
of the public health system. Their nineteenth cen- the end of the year. A single case was reported in
tury experience with cholera led the countries of Denmark in 1995. Then, in August, 1996, V. chol-
the former Soviet Union to improve water and sani- erae O139 reemerged in Southern India (Calcutta,
tation infrastructure. By the 1980s, however, this Vellore, Madras), causing severe cases. In 1998,
infrastructure was deteriorating. As Narkevich et the disease was again detected in India, Bangla-
al. observe, water supply and sewage facilities in desh, Thailand, Pakistan and possibly Afghani-
most towns and villages are unsatisfactory. Envi- stan. Overall, the specific number of cases remains
ronmental pollution has also been a major problem unknown because current reporting systems do not
in the region. In some regions, cholera cases occur report V. cholerae O139 and O1 separately. None-
every year and virulent toxigenic cholera vibrios theless, it is known that the disease has affected at
are recovered from surface waters.[32-35] Regions least 11 countries in south and southeast Asia.
with particular climatic, geographical, sanitary and There are ongoing debates about the origins of
social conditions, as well as transient populations this new cholera strain, but most attribute at least
and territories bordering cholera endemic coun- some causation to global changes impacting on the
tries are especially at risk. It is perhaps not surpris- social and natural environments. There is specula-
ing, therefore, that in 1997, the Russian ministry of tion that O139, for example, evolved from El Tor
health reported that it isolated V. cholerae O139 bio- in the highly polluted waters of the Bay of Bengal.
type (see below) in Moscow sewage. With intense population pressures in large urban
concentrations (e.g. Calcutta, Dhaka), intensifica-
Home again, home again jiggidy jig: tion of farming to feed growing populations, and
V. cholerae O139 Bengal as the eighth pandemic? widespread poverty and inequalities in the region,
Just as disruption of the social and natural environ- tons of pesticides, millions of gallons of industrial
ment in South Asia led to the fi rst cholera pandemic waste and raw sewage, and millions of tons of chem-
GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001) 14 © Kluwer Academic PublishersThe global dimensions of cholera
ical fertilizers are dumped daily into local rivers demic) argues that patterns of cholera epidemics
flowing into the bay. It was previously thought that in South Asia can be linked to patterns of global
pollution dumped at sea would quickly degrade as climatic change. Human-induced climate change
it sunk downwards, but there is growing evidence may be creating favourable conditions such as water
that microbes and other biological material can sur- temperature, nutrient concentration and plankton
vive “in suspended animation” in the ocean depths, production, for the growth and reproduction of
capable of resurfacing via the food chain (plants the bacterium. The El Nino-Southern Oscillation
and plankton to fish and shellfish to humans) or (ENSO) influence on climate is also considered an
ocean currents.[37] This human-induced degrada- important factor.[39] Like the O1 serogroup, O139
tion of the local environment is also leading, it is is found in association with plankton in pond sur-
believed, to widespread changes in the coastal ecol- face waters that serve as a reservoir for V. cholerae
ogy. The creation of “hot systems”, in which muta- in the aquatic environment. Research on the coinci-
tions of V. cholerae are selected and amplified under dence of zooplankton blooms and cholera outbreaks
new environmental pressures may explain changes in September and October support this hypothesis.
in classical and El Tor cholera and the emergence of Blooms in early summer are also associated with
V. cholerae 0139.[38] lesser outbreaks.[40] Similarly, using remote sensing,
An alternative environmentally-focused theory Lobitz et al. (2000) found that sea surface tempera-
(described above in relation to the Peruvian epi- ture shows an annual cycle similar to the cholera
Box 1 Classification of types of Vibrio cholerae strains
Vibrios are one of the most common organisms in sur- strain that is virilent. V. cholerae O1, in turn, is divided
face waters of the world, occurring in marine and fresh- into three biotypes: Ogawa, Inaba and Hikojima. Each
water habitats, and in associations with aquatic ani- biotype may display the “classical” or El Tor phenotype.
mals. Cholera is caused by certain strains of the bacte- V. cholerae O139 Bengal is the first non O1 strain
rium Vibrio cholerae, distinguished by antigenic variation that is known to cause epidemic cholera. Indeed, with
among the different strains. O antigens divide strains of a unique O-antigen existing populations have a lack of
V. cholerae into 139 different serotypes. Until recently, residual immunity and are thus more vulnerable to the
strains classified as O1 antigen were the only known bacterium.
Serogroup 139 serotypes of Vibrio cholerae
O1 O139 (Bengal) others
Biotype Classical El Tor
Serotype Ogawa Inaba Hikojima Ogawa Inaba Hikojima
Antigens A, B A, C A, B, C A, B A, C A, B, C
© Kluwer Academic Publishers
15 GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001)The global dimensions of cholera
case data.[41] Furthermore, sea surface height may ices. The lessons learned in industrialised countries
be an indicator of incursion of plankton-laden water from the great pandemics of the nineteenth century
inland (e.g. tidal rivers) and correlates with cholera have not yet been applied to the world as a whole.
outbreaks. While the biology of cholera is among the best
One of the main concerns with V. cholerae 0139 understood of that of infectious diseases, there is
is that it will spread beyond Asia to become the much that we still don’t know. Cholera is recog-
eighth cholera pandemic. Significantly, most of nised as more complicated and durable than previ-
the cases so far have been adults, indicating that ous thought, possibly existing permanently within
human populations in areas where V. cholerae O1 the environment rather than only living a few days
is endemic has no previous exposure to the strain. outside of the human intestine. The relationship
Recurrent infections of cholera are rare because of between the organism and environmental condi-
local immune defenses. In heavily endemic regions tions continues to be a subject of keen debate.
such as South Asia, the number of El Tor cases is An effective vaccine for the variety of strains now
low among adults in comparison with that in chil- known, especially for V. cholerae O139, requires fur-
dren. It appears that V. cholerae O139 is genetically ther development. Current disease reporting sys-
derived from El Tor because it produces indis- tems do not distinguish between the O1 and O139
tinguishable symptoms. However, one of the key serotypes, thus making impossible precise epidemi-
differences between the two strains is that O139 ological analysis of the different cholera strains.
has new adaptive mechanisms, such as a thin cap- The poor quality of data also arises from the
sular layer which increases its virulence and inva- close link between the global economy and cholera.
sive properties. This change in antigenic structure Despite being one of three mandatory notifiable
means that there is no existing immunity and diseases under the International Health Regula-
all ages are susceptible and, equally significant, tions of WHO, it is widely accepted that there
it allows the bacteria to survive and multiply for is substantial underreporting of cases. The main
extended periods in surface water. Finally, V. chol- reason for this is the lack of desire by national gov-
erae O139 strains display different patterns of anti- ernments to attract adverse publicity that would
biotic susceptibilities from O1 isolates. Research have negative political and economic consequences.
suggests that antimicrobial resistance is progressing The outbreak in East Africa in 1997-98, for exam-
in both serotypes but in different patterns. ple, led the European Union to ban fresh imports
from Kenya, Uganda, Tanzania and Mozambique.
Conclusions Fish exports are the fourth largest foreign-exchange
Cholera remains among those infectious diseases earner (US$34-52 million) for Uganda.[42] These
posing a potentially serious threat to public health are valid concerns and are not yet effectively
systems around the world in the twenty-fi rst cen- addressed under current international law. The
tury. Since 1991 around 120 countries have reported links between global economic change and cholera
indigenous cases of cholera, nearly half of those may also be usefully explored in relation to chang-
countries during at least five of the last eight years. ing patterns of agriculture, food production and
It is a recurring problem in many areas and has other human activity. For example, Agarwal sug-
become endemic in others. Cholera illustrates many gests that the distribution of cholera matches the
of the increased health risks associated with the geographical distribution of sugar cane, and sugar-
global changes taking place around us - large scale cane harvesting synchronises with interepidemic
movement of people, changes to ecosystems from periods of cholera epidemiology[43]. Does this sug-
heavy pollution, human-induced climate change, gest something about modern agricultural practices
rapid technological change, and economic and polit- and disease epidemiology?
ical instability. Widening socioeconomic inequali- The epidemiology of cholera in the four regions
ties within and between countries leaves over one described in this paper suggests that cholera is very
billion people without access to clean water and much a global story, one that requires going far
1.7 billion people with no access to sanitation serv- beyond traditional approaches to public health.
GLOBAL CHANGE & HUMAN HEALTH,VOLUME 2, NO. 1 (2001) 16 © Kluwer Academic PublishersThe global dimensions of cholera
The author [13] World Health Organization. Cholera. In: WHO Report on Global Surveillance
of Epidemic-prone Infectious Diseases. Communicable Disease Surveillance
Kelley Lee is is Senior Lecturer and Response, Geneva, 2000.
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March 2000.
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[16] Panisset U. International Health Statecraft, Foreign Policy and Public
and Health at the London School Health in Peru’s Cholera Epidemic. University Press of America, New York,
of Hygiene & Tropical Medicine. 2000.
[17] Harvard Working Group on New and Resurgent Diseases. New and Resur-
After several years analysing the gent Diseases, The Failure of Attempted Eradication. The Ecologist. 1995;
World Health Organisation and United Nations reform, 25: 21-24.
[18] French H. Vanishing Borders, Protecting the Planet in the Age of Globaliza-
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cholera, tuberculosis, HIV/AIDS, influenza and tobacco- Comes by the Bucket. New York Times. 2000; 8 December.
[21] Speelmon E, Checkley W, Gilman R, Patz J, Calderon M, Manga S. Cholera
related disease. She is chair of the WHO Scientific incidence and El Nino-related higher ambient temperature. JAMA. 2000;
283: 3072-3074.
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[22] World Health Organization. Cholera, 1999. Weekly Epidemiological Record.
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[26] Cash RA and Narasimhan V. Impediments to global surveillance of infec-
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[27] Schalk van Schalkwyk, South Africa Democratic Alliance Chief Provincial
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[31] Alexander Moroz, Head of the Ukrainian Parliament, 1994 as quoted in
Ryan F. Virus X: Understanding the Real Threat of the New Pandemic
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[32] Walberg P, McKee M, Shkolnikov V, Chenet L, Leon DA. Economic
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