O International Epldemiological Association 1998
International Journal of Epidemiology 1998:27:330-334
Printed in Great Britain
Are there national risk factors for epidemic
cholera? The correlation between
socioeconomic and demographic indices and
cholera incidence in Latin America
Marta-Louise Ackers,a Robert E Quick,a Christopher J Drasbek,b Lori Hutwagner c and Robert V Tauxea
Background From 1991 through 1995, all Latin American countries maintained cholera surveillance systems to track the epidemic that entered the region through Peru in
January 1991. These data were used to assess correlations between socioeconomic and demographic indices that might serve as national risk predictors
for epidemic cholera in Latin America.
Methods
Correlations between country-specific cumulative cholera incidence rates from
1991 through 1995 and infant mortality, the Human Development Index ([HDI]
a numerical value based on life expectancy, education, and income), gross national
product (GNP) per capita, and female literacy were tested using the Pearson
correlation coefficient.
Results
A total of 1 339 834 cholera cases with a cumulative incidence rate of 183 per
100 000 population were reported from affected Western Hemisphere countries
from 1991 through 1995. Infant mortality rates were the most strongly correlated
with cumulative cholera incidence based on the Pearson correlation coefficient.
The HDI had a less strong negative correlation with cumulative cholera incidence.
The GNP per capita and female literacy rates were weakly and negatively correlated
with cholera cumulative incidence rates.
Conclusions Infant mortality and possibly the HDI may be useful indirect indices of the risk of
sustained transmission of cholera within a Latin American country. Cumulative
cholera incidence is decreased particularly in countries with infant mortality
below 40 per 1000 live births. The lack of reported cholera cases in Uruguay and
the Caribbean may reflect a low risk for ongoing transmission, consistent with
socioeconomic and demographic indices. Cholera surveillance remains an important instrument for determining cholera trends within individual countries and
regions.
Keywords Cholera, infant mortality, Latin America, surveillance
Accepted
4 August 1997
The detection of Vibrio cholerae Ol in patients from a Peruvian Central, and North America, with indigenous or imported cases
coastal village in January 1991 signalled the arrival of the sev- reported from all countries by 1995 except Uruguay and the
enth pandemic of cholera to the Western Hemisphere. From its Caribbean. Now, after the first five epidemic years, cholera has
explosive onset in Peru, the epidemic spread to affect South, become established in a number of countries in the hemisphere,
a
b
c
Foodborne and Diarrheal Diseases Branch and
Biostatistlcs and
Information Branch, Division of Bacterial and Mycotic Diseases, National
Center for Infectious Diseases, Centers for Disease Control and Prevention.
Atlanta, GA, USA
Integrated Management of Prevalent Childhood Illness. Communicable
Diseases Program. Division of Disease Prevenuon and Control. Pan
American Health Organization, Washington, DC, USA
330
serving as a stark reminder of the deficiencies in water quality,
sanitation, and hygiene that will continue to challenge governments and health agencies into the next century. All countries
in Latin America have maintained cholera surveillance systems
since the beginning of the epidemic and these provide an opportunity to compare national risk factors for epidemic cholera.
We used country-specific cholera surveillance data from
NATIONAL RISK FACTORS FOR EPIDEMIC CHOLERA
331
Table 1 Total reported cholera cases, deaths, cumulative incidence rates, infani mortality rates, and human development index (HDI),
by country. Western Hemisphere, 1991-1995 3
Country
South America
Argentina
Bolivia
Brazil
Chile
Colombia
Ecuador
French Guiana
Guyana
Paraguay
Peru
Suriname
Venezuela
North/Central America
Belize
Canada
Costa Rica
El Salvador
Guatemala
Honduras
Mexico
Nicaragua
Panama
a
b
Cumulative
Incidence
(per 100 000
population)
Infant
mortality
(per 1000
live births)
Cumulative cases
Deaths
3710
37 603
328 421
55
11
26
749
507
74
1792
203
57
147
3
1
14
33 614
88 982
521
96
32
1016
776
44
19
0
13
20
b
622
10
74
46
3
0
42
651 130
4581
0.06
2738
12
1
3
31
3264
80
15
26
0.622
0.723
0.709
0.762
0.859
59
319
8
148
36
22
0
0.07
7
87
0
3
12
30 288
75 095
14 203
42 053
26 405
3636
138
525
43
834
707
51
384
251
44
519
46
30
564
596
53
82
138
21
8
USA
199
1
0.07
Total
1 339 834
11 338
183
HDI
0.882
0.588
0.804
0.880
0.836
0.784
0.883
0.950
0.883
0.579
0.591
0.578
0.842
0.611
0.856
0.937
Countries (Uruguay and all Canbbean countries) with no reported cholera cases are excluded
Not calculated.
Western Hemisphere countries to investigate possible correlations between national cumulative cholera incidence rates and
a variety of demographic and socioeconomic indices that might
be useful as predictors of the behaviour of epidemic cholera at
the national level.
Methods
Reported cholera cases and deaths for Latin America were
summarized from information submitted to the Pan American
Health Organization (PAHO) by the Ministry of Health of each
country. Cholera data for the US and Canada were obtained
from the Centers for Disease Control and Prevention (CDC) and
the Laboratory Centre for Disease Control (LCDC), respectively.
Country-specific cumulative incidence rates were calculated
by dividing the sum of reported cholera cases for each country
during 1991-1995 by its estimated 1995 population. Total 1995
population, 1994 infant mortality rates, female literacy rates,
and 1993 gross national product (GNP) per capita estimates for
each country were obtained from PAHO.1 The Human Development Index (HDI), constructed by the United Nations, ranks
countries by their relative progress toward development goals
from three variables: life expectancy at birth, educational
attainment (weighted between adult literacy [2/3] and primary,
secondary, and tertiary educational enrolment [1/3]), and standard of living (real gross domestic product [GDP] per capita). 2 A
numerical value is calculated for individual countries as a function of the three variables. Values range from a high of 0.950
(Canada) to a low of 0.207 (Niger); a lower value signifies a
lower level of development. The Pearson correlation coefficient
was used to determine the correlation between cholera cumulative incidence rates from 1991 through 1995 and infant mortality and female literacy rates, GNP per capita, and the HDI of
Western Hemisphere countries affected by this decade's epidemic.
P-values were calculated to serve as a general guide to differentiate among the correlations between cholera incidence rates
and the socioeconomic and demographic indices.
Results
From 1991 through 1995, over one million cases and 11 000
deaths due to cholera were reported from a total of 22 countries
in the Western Hemisphere (Table 1). Based on the number of
reported cases during 1991-1995, the cumulative cholera incidence for these 22 countries was 183 cases per 100 000 population. Country-specific cumulative cholera incidence for the
332
INTERNATIONAL JOURNAL OF EPIDEMIOLOGY
Figure 1 Cumulative cholera lnddence rates (per 100 000
population), 1991-1995, the Western Hemisphere
Cholera inddence per 100,000 people
|21-300
•
1-20
I <300
affected countries of the Western Hemisphere reporting any
cholera ranged from a low of 0.06 per 100 000 in Paraguay to a
high of 2738 per 100 000 in Peru (Table 1). The countries with
a cumulative cholera incidence of >20 per 100 000 were concentrated in a band extending south from Mexico to the northern border of the Southern Cone countries (Figure 1). The
Andean countries in South America, and Guatemala and Nicaragua in Central America had the highest cumulative incidence.
Cumulative incidence rates were lowest in Chile, Paraguay,
Canada, and the US. No cases were reported from any Caribbean
countries nor from Uruguay.
By simple linear comparison, infant mortality rates were
strongly and positively correlated with cumulative cholera incidence in Western Hemisphere countries (Table 2). The HDI values,
which tend to increase with increasing levels of development,
had a negative correlation with cumulative cholera incidence
with a smaller absolute coefficient than infant mortality. Female
literacy rates and GNP per capita were also negatively correlated
with cholera cumulative Incidence with smaller coefficients and
P-values > 0.1.
Countries with higher infant mortality rates tended to
have markedly higher cumulative incidence rates of cholera
(Figure 2a). Cholera incidence was much lower (0.7-3 per
100 000 population) in countries with infant mortality rates
<20 per 1000 live births (Canada, the US, Chile, and Costa Rica).
With the exception of Paraguay (infant mortality rate of 42 per
1000 live births), countries with infant mortality rates >40 per
1000 live births had higher cumulative cholera inddence rates,
ranging from 203 per 100 000 (Brazil) to 2738 per 100 000 population (Peru) (Figure 2a). The relationship between cumulative
cholera incidence and infant mortality does not appear to be a
simple linear one; when infant mortality rates increased above
40 deaths per 1000 live births the cumulative cholera incidence
rose less steeply, suggesting that a threshold effect exists. Other
relationships between cumulative cholera incidence and socioeconomic indices exhibited thresholds as well. Countries with
an HDI <0.720 had higher cumulative cholera incidence rates,
ranging from 74 (Guyana) to 2738 (Peru) (Figure 2b). Countries
with a GNP per capita >US$ 2000 (Canada, Chile, Costa Rica,
Argentina, Brazil, Belize, Panama, Mexico, and the US), had
lower cholera cumulative incidences, as did nations with female
literacy rates >90%, (Canada, Chile, Costa Rica, Argentina,
Guyana, Suriname, and the US) (Data not shown).
Caribbean countries and Uruguay were not included in the
above analysis because of their lack of reported cholera cases.
Uruguay, with an infant mortality rate of 19, GNP per capita of
US$ 3830, and HDI of 0.881 falls in the low risk group. Of
the 22 Caribbean countries, all but three (Haiti, the Dominican
Republic, and Anguilla) had infant mortality rates <20. Only
Haiti and the Dominican Republic had an HDI <0.720, all but
three countries (Haiti, the Dominican Republic, and Jamaica)
were above the GNP per capita of US$ 2000, and all but five
countries (Haiti, the Dominican Republic, Bahamas, Saint Lucia,
and Antigua and Barbuda) had female literacy rates >90%. These
general measures of development suggest that among countries
not yet affected in this hemisphere, Haiti and the Dominican
Republic are at highest risk for sustained cholera transmission
should the epidemic be introduced there, and that much of the
Caribbean may be at low risk for sustained transmission.
Table 2 Correlation of cumulative cholera Inddence rates, 1991-1995, with infant mortality and female literacy rates, the Human Development
Index (HDI),' and 1993 gross national product (GNP) per capita. Western Hemisphere
Method
Pearson correlation coefDdent
P-value
Infant mortality
(per 1000 live births)
0.55
0.006
HDI
-0.38
0.08
Female literacy
(%)
-0.31
0.15
1993 GNP per capita
(US$)
-0.23
0.303
' A numerical indicator of development calculated by the United Nauons based on three variables: life expectancy at birth, educational attainment, and
income.2
NATIONAL RISK FACTORS FOR EPIDEMIC CHOLERA
Cumulative Incidence (per 100,000 person*)
10,000
1,000
100
10
1
0.1
0.01
20
40
60
Intuit mortaffly (per 1,000 Uvs bkDu)
80
Figure 2a Cumulative cholera incidence rates, 1991-1995, by infant
mortality rates 3 and country. North, Central, and South America
* Health Situation in the Americas. Basic Indicators 1995. Washington, DC:
PAHO; 1995.
Cumulative Incidence (per 100,000 person*)
10.000
1,000
100
10
1
0.1
0.6
0.7
0.6
0.9
HDI
Figure 2b Cumulative cholera incidence rates, 1991-1995, by human
development index* and country, North, Central, and South America
* Human Development Report 1995. New York: Oxford University Press;
1995.
Discussion
333
through contaminated food and water, and high infant mortality rates are in part a reflection of poor sanitation and poverty.4
Vibrio cholerae is also usually transmitted through contaminated
food and water.5 A high cumulative incidence means that transmission has been sustained through many cycles of infection.
Efforts to prevent cholera through education and improved
sanitation would be expected to have an effect on infant
mortality.
These general indices may be applicable outside Latin
America. The continued lack of cholera cases in Caribbean
countries during the recent Latin American epidemic is noteworthy. Most of these countries have socioeconomic and demographic indices that resemble the group of Latin American
countries at lower risk for cholera. The indices for Haiti and the
Dominican Republic fit the profile of countries at higher risk for
sustained cholera transmission. It may be reasonable for those
countries to prepare for the possibility of sustained transmission
should the infection be introduced.
This analysis has several limitations. First, the quality of the
data is variable because of varying resources and cholera reporting policies among countries. Case definitions differed between
countries, introducing uncertainty into inter-country comparisons. 6 In several countries, cholera case definitions or reporting
policies changed during the epidemic, which may have distorted
the year-to-year trends in reported cases of cholera. Second, the
number of cases reported to the surveillance systems represents
only a small fraction of the cases that actually occurred. For
example, a seroprevalence study conducted in Peru in 1991
revealed that only 47% of people with serological evidence of
recent infection with V. cholerae Ol reported gastrointestinal
symptoms, and only 26% had visited a medical facility where
they could be registered as a possible cholera case. 7 Finally, the
utility of general health and development indices as correlates
and predictors of risk in other regions of the world remains to
be shown. This may be difficult in the absence of reliable surveillance data. The degree to which different demographic and
socioeconomic characteristics reflect the local risk factors for
cholera transmission merits further investigation.
Surveillance data reported in this hemisphere provide a useful estimate of the magnitude and time trends of the cholera
epidemic. Cholera surveillance remains an important instrument for determining cholera trends in regions as well as within individual countries. The continued expansion of seventh
pandemic strains of V. cholerae Ol and the threat of an eighth
pandemic posed by the emergence of V. cholerae 0139 in Asia
provide ample motivation for continued vigilance throughout
the world. 8
In the Western Hemisphere, there has been substantial
variation in cumulative reported cholera incidence since the
beginning of the epidemic. Infant mortality rates were strongly
correlated with a high incidence of cholera within a country.
The HDI was less strongly correlated, but may provide an
additional estimator of risk. Although female literacy and GNP
per capita had small correlation coefficients with cumulative
incidence by themselves, they may also be useful variables to
examine when analysing cholera risk and are, in fact, incorporated indirectly into the HDI. We observed that in Latin
Acknowledgements
America, infant mortality rates <40 per 1000 live births and
HDI values >0.720 are thresholds at which cholera risk deMr Michael Roessler's 7th grade geography class, Portland Middle
creases. Countries above these thresholds may be at higher risk
School, Portland, Michigan, who in 1993 performed the first
for sustained epidemic transmission in the future.
linear analysis of epidemic cholera in the Western Hemisphere.
The correlation of infant mortality with cumulative cholera
incidence suggests they may be linked to the same root causes.
Diarrhoeal diseases are a leading cause of death in children
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