Research
Epidemiology of Urban
Canine Rabies, Santa Cruz, Bolivia, 1972–1997
Marc-Alain Widdowson,* Gustavo J. Morales,† Sandra Chaves,‡
and James McGrane*
*Unidad Nacional de Epidemiología Veterinaria, Santa Cruz, Bolivia;
†Laboratorio de Investigación y Diagnóstico Veterinario, Santa Cruz,
Bolivia; and ‡Rijksinstituut voor Volksgezonheid en Mileu (RIVM),
Bilthoven, the Netherlands
We analyzed
laboratory data from 1972 to 1997 from Santa Cruz, Bolivia, to
determine risk factors for laboratory canine samples’ testing
positive for Rabies virus (RABV). Of 9,803 samples,
50.7% tested positive for RABV; the number of cases and the percentage
positive has dropped significantly since 1978. A 5- to 6-year
cycle in rabies incidence was clearly apparent, though no seasonality
was noted. Male dogs had significantly increased odds of testing
positive for RABV (odds ratio [OR]=1.14), as did 1- to 2-year-old
dogs (OR=1.73); younger and older dogs were at lower risk. Samples
submitted from the poorer suburbs of the city were more likely
to test positive for RABV (OR=1.71). Knowledge of the distribution
of endemic canine rabies in an urban area will help focus control
measures in a resource-poor environment.
Europe and North America have successfully controlled rabies in
domestic animals, leaving wildlife as the main reservoir of concern
(1,2). Nevertheless, rabies remains a serious public
health hazard in many developing countries, where dog bites continue
to be the main mode of transmission of the disease to humans. Throughout
the world, an estimated 35,000 to 100,000 people a year die of rabies
(1,3). The disease also elicits fear in communities,
and subsequent control measures are drains on public health budgets
(4,5). Rabies is a particular problem in the larger
cities of less-developed countries, with sprawling, impoverished
suburbs and high densities of dogs (3,6,7). Controlling
rabies in urban dog populations is seen as a more cost-effective,
long-term approach to prevent human rabies than reliance on postexposure
human treatment (8). To achieve control, knowledge
of the epidemiology of rabies in dog populations has long been recognized
as crucial (9).
In South America several larger urban areas have successfully eliminated
rabies through legislation, education, and mass vaccination of dogs
(10). Cities in poorer countries such as Bolivia,
however, lag behind in control efforts, in large part because resources
are scarce, and programs are poorly focused. In these situations,
control efforts and resources must be more directed. Knowledge of
risk factors for canine rabies in urban settings is needed to assess
the danger to public health.
We analyzed 26 years of laboratory data on rabies diagnosis in
dogs in the city of Santa Cruz, Bolivia, where rabies is endemic.
We interpreted the results in light of possible biases to determine
risk factors and temporal trends for rabies in the general dog population.
Materials
and Methods
Study Area
Santa Cruz is a city of 1 million inhabitants, located in the department
of Santa Cruz in the lowlands of eastern Bolivia. The city has been
rapidly expanding at an average rate of 6.7% per year since 1976
(11). The city center is circled by eight concentric
ring-roads; municipal services and general socioeconomic status
drop as distance increases from the city center. When we extrapolate
from a study of the dog population conducted in 1996 (Laboratorio
de Investigación y Diagnóstico Veterinario [LIDIVET], unpub. data),
the canine population in 1999 in Santa Cruz was an estimated 276,034
dogs (1 dog per 4 inhabitants). Dogs are routinely vaccinated by
private veterinarians and the municipality and Ministry of Health
staff during 1- to 2-day annual public vaccination campaigns. Nevertheless,
vaccination coverage data are unreliable. Additional municipal control
measures for rabies include a dog pound, which collects and euthanizes
up to 200 stray or aggressive dogs each month.
Canine rabies is a major problem in Santa Cruz, accounting for
>90% of all animal rabies. In 1997, more than 2,178 people who
had been bitten by dogs attended the municipal clinic for rabies
prophylaxis; 1,464 required specific anti-rabies treatment. In 1997,
three persons died of rabies, for an incidence of 0.30/105
population, compared with the reported incidence of 0.025/105
for Latin America in the same year (3). (Derived
from 114 cases cited in that reference and using estimated Latin
American population of 500 million.)
Data Collection
LIDIVET receives samples of brain tissue for rabies diagnosis from
suspected cases in animals and humans. For animal samples, species,
age group, sex, and bite history have been noted since 1972. Since
1994, the location where the animal was found has also been recorded
by ring-road.
Canine samples come from three sources: 1) dogs that have bitten
people and have been killed or have died during the 10-day observation
period; 2) dogs brought in by the public or private veterinarians
because they showed suspicious symptoms; and 3) stray dogs routinely
collected and euthanized by the pound. Impression smears of brain
tissue from the cerebellum, Ammon's horn, and medulla are examined
after staining by fluorescein-labeled anti-rabies globulin (Centocor,
Malvern, PA).
Data Analysis
All the records of canine samples examined at LIDIVET for rabies
from within the municipal boundaries of Santa Cruz from 1972 through
1997 were analyzed. Secular trends were investigated with linear
regression with EXCEL (Microsoft, Redmond, WA), using time in months
as the independent variable (x) and number of cases per month as
the dependent variable (y). A t-test was used to test for the significance
of the slope (b). A centered moving average was applied to monthly
numbers of positive cases to assess cyclicity in the data. To assess
seasonality of rabies incidence, analysis of variance and the F-test
were used to test for significant differences in the mean number
of positives and mean percentage positive for each of the 12 calendar
months. Associations between numbers of positive samples and age
group, sex, and ring-road were examined by the chi-square test for
unequal odds and linear trend across groups (Epi-Info 6.04, Centers
for Disease Control and Prevention, Atlanta, GA).
Results
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Figure
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![Figure 1. Percentage of rabies-positive samples and total number of positive samples by direct fluorescent antibody test from dogs, Santa Cruz, Bolivia, 1972–1997.](images/01-0302-1t.gif) |
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Figure 1. Percentage of
rabies-positive samples and total number of positive samples
by direct fluorescent antibody test from dogs, Santa Cruz,
Bolivia, 1972–1997.
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Figure
2
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![Figure 2. Positive rabies samples by month with a moving 24-month centered mean, Santa Cruz, Bolivia, 1972–1997, and regression line, 1978–1997.](images/01-0302-2t.gif) |
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to view enlarged image
Figure 2. Positive
rabies samples by month with a moving 24-month centered mean,
Santa Cruz, Bolivia, 1972–1997, and regression line, 1978–1997. |
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From 1972 through 1997, 9,308 samples of canine brain tissue were
analyzed in Santa Cruz; the annual number of tests varied from 66
to 764. Of all samples, 4,694 (50.4%) were positive for Rabies
virus (RABV). The annual number of positive cases varied from
45 to 383, and the annual percentage of samples positive for RABV
ranged from 22.81% to 87.05%. The annual percentage of positive
samples dropped during the study period, as did the annual number
of cases confirmed as positive; this trend was especially apparent
in the last 5 years (Figure 1).
The equation of the regression line was fitted only from 1978 because
the low number of tests from 1972 through 1978 was uncharacteristic
of the rest of the data. The number of monthly cases dropped significantly
after 1978 (b = 0.04: t-test for slope= -4.53, 239 degrees of freedom
[df], p<0.001) (Figure 2).
The cyclicity of rabies incidence suggested by Figure
1 is clearly shown by the 24-month centered moving average on
cases per month in Figure 2. Since 1972,
the mean number positive and mean percentage positive by calendar
month (1972-1997) showed no significant variation (F-test= 0.47,
p=0.92).
Gender
Twice as many samples and reported rabies cases were associated
with male dogs (Table). The association between
male dogs and sample positivity was significant, with an odds ratio
[OR] of 1.14 (chi square=8.27, p=0.004).
Age
Of the 8,352 samples for which age was recorded, dogs <1 year
old accounted for 4,893 (58.6%) samples and for 2,475 (60.3%) of
4,104 positive samples (Table). The odds for
positive samples varied significantly between age groups (chi-square
unequal odds = 189, p<0.001). Dogs 1 to 2 years of age were significantly
more likely to test positive than dogs <3 months old (OR=1.73,
chi square = 43, p<0.001). Testing positive for RABV was less
likely in dogs >2 years of age, with dogs >3 years old at
lower risk than those <3 months old (OR=0.69, chi square
= 23, p<0.001).
Location
The percentage of positive samples increased significantly as distance
increased from the town center (chi-square trend = 25, 1 df p<0.001).
This trend was especially evident after the sixth ring.
Despite similar estimated owned dog populations, fewer samples
were received from outside the fourth ring than within. Samples
from dogs outside the fourth ring were significantly more likely
to test positive (Table; chi square = 14.67.
1 df, p<0.001).
Discussion
The overall percentage of confirmed rabies in dogs submitted for
diagnosis in Santa Cruz (50.4%) was similar to the 44% found in
another urban study in Ghana (12). Other studies,
not specifically urban, have shown percentages of samples positive
varying from 54% to 67% (13-15). Canine rabies
incidence appeared to decrease during the study period, especially
since 1992. The significant drop in both number and percentage of
positive samples suggested that this was not a reporting artifact.
This decrease in incidence may be a result of vaccination, although
vaccine coverage data are unreliable, and public sector vaccination
has not been focused in recent years.
The data strongly suggested a 5- to 6-year cyclicity of rabies
incidence; this cycle was most clearly apparent with a centered
moving average of number of cases diagnosed per month. The cyclicity
was independent of any changes in control measures and might explain
the recent downturn in rabies cases. Some previous studies have
reported a cyclical nature of rabies incidence (14,16),
but this feature was not noted in an urban study in Delhi (17).
Cyclicity is usually explained by increasing numbers of young, susceptible,
unrestrained dogs in a population with low vaccine coverage. These
factors lead to a drop in herd immunity, allowing rapid spread of
the disease (6,16). However,
even if underreporting is taken into account, the canine deaths
from rabies in an epidemic year are unlikely to have substantially
affected the number of susceptibles. A reduction in susceptibles
may also be due to dogs’ becoming immune after recovering from clinical
or inapparent infections. Recovery of dogs from rabies is well documented
(18-20); one study showed 20% of experimentally
infected dogs recovered (21). Also, serologic
evidence shows that almost 20% of unvaccinated dogs in Thailand
have been exposed to rabies (22).
Gender does seem to be a risk factor for sample positivity: male
dogs had a significantly higher percentage of samples diagnosed
positive (OR 1.14). This increased risk may be explained by males’
fighting over females. Studies in Mexico and India (6,17)
show higher numbers of male dogs being affected, though the authors
concluded that gender was not a risk factor, perhaps because of
low numbers studied.
Rabies was not evenly distributed in Santa Cruz. The percentage
of positive samples increased significantly with distance from the
city center and as socioeconomic status dropped. In addition, a
higher number of positives were reported from beyond the fourth
ring-road, despite a similar-sized dog population. Some of the increase
in percentage positive (but not in number positive) as distance
increased from the center may be due to reporting bias. Fewer samples
were submitted from outside the fourth ring, and these samples probably
included a higher proportion of dogs that showed specific signs
of rabies. An association of increased risk for canine rabies and
areas of low socioeconomic status has also been shown in Mexico
(6). Lower vaccination coverage and increased densities
of unrestrained dogs have previously been reported to be associated
with poorer urban areas (23), a characteristic
also shown in a recent survey of the canine population in Santa
Cruz (LIDIVET, unpub. data).
Age was a clear risk factor for sample positivity in our study.
The median age of a dog that tested positive for rabies was up to
1 year, as found in Mexico (6). The age group most
at risk of testing positive for rabies, however, was 1- to 2-year-old
dogs (OR=1.73). Dogs 3 months to 1 year of age were at intermediate
risk (OR=1.49); however, this risk for rabies in dogs up to 1 year
old may be underestimated. Perhaps because of the die-off of dogs
of that age from all causes and the relative ease of carrying a
puppy to the laboratory, the proportion of submissions (68% of all
samples) from dogs <1 year was high, even relative to the population
(37% of all dogs). This disproportion led to the finding of more
positive samples but also to less specific reporting, with proportionally
more nonrabid dogs with vague symptoms; such dogs would not have
been submitted had they been older. This discrepancy may have decreased
the percentage positive and thus underestimated the comparative
risk for rabies in dogs <1 year old. It is nonetheless plausible
that the risk for contracting rabies in dogs <1 year is lower
than for 1- to 2-year-old dogs. Although dogs <1 year are less
likely to have been vaccinated, sexually immature dogs are also
less likely to roam, interact, and fight with other dogs. Puppies
<3 months old may also benefit from passive immunity from their
mothers. The large population of puppies, however, and their increased
contact with children and adults make them a particular public health
risk. The decreasing odds of sample positivity after 2 years of
age may be due to increased likelihood of vaccination and less fighting
among older dogs. Older dogs are also more likely to be owned.
We have shown that laboratory data can provide important information
on risk groups and temporal trends for rabies in an urban environment.
Especially if combined with additional work on the epidemiology
of dog bites and seroepidemiologic studies, such data can help to
effectively focus rabies-control efforts.
Acknowledgments
The authors thank Nico Nagelkerke, Thomas Grein, Alain Moren, and
Udo Buchholz for comments on the manuscript.
Drs. Widdowson and McGrane were employed by the U.K. Department
for International Development, which also supported the Unidad Nacional
de Epidemiología Veterinaria project.
Dr. Widdowson is a veterinary public health epidemiologist now
based at the Centers for Disease Control and Prevention. He is responsible
for the foodborne virus epidemiology program, with a particular
focus on Norwalk-like viruses. His other research interests include
all aspects of zoonotic infections.
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Table.
Canine laboratory samples examined for rabies and odds ratios
for positive result, Santa Cruz, Bolivia, 1972–1997 |
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Clinical and demographic characteristics
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% of canine populationa
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No. of samples
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No. (%) positive
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OR (95%
CIb)
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Gender |
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Female
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50
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2,969
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1,419 (47.9)
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1
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Male
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50
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5,655
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2,887 (51.1)
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1.14 (1.04 to 1.25)
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Unknown
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684
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368 (56.7)
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Age group
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<3 mo
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20.6
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1,624
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713 (43.9)
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1
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3 mo to l yr
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16.7
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3,273
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1,762 (53.8)
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1.49 (1.32 to 1.68)
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<l yr to 2 yrs
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18.8
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743
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802 (57.5)
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1.73 (1.49 to 2.00)
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>2 yrs to 3 yrs
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13.2
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1,395
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364 (49.0)
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1.23 (1.03 to 1.47)
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>3 yrs
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30.7
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1,317
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463 (35.5)
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0.69 (0.59 to 0.81)
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Unknown
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956
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590 (61.7)
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Ring roadc
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Within 4th
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50.4
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132 (20.9)
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1
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4th and beyond
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49.6
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488
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152 (31.4)
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1.71(1.29 to 2.26)
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Unknown
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8,189
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4,410 (53.9)
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Total |
100
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9,308
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4,694 (50.4)
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aPercentages of total population
of owned dogs (228,170) as estimated in 1996 (LIDIVET, unpub.
data).
bConfidence interval.
cData only available since 1994.
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