44
Review
TRENDS in Parasitology
Vol.19 No.1 January 2003
Chagas disease control in Venezuela:
lessons for the Andean region and
beyond
Maria Dora Feliciangeli1, Diarmid Campbell-Lendrum2, Cinda Martinez3,
Darı́o Gonzalez3, Paul Coleman2 and Clive Davies2
1
Facultad de Ciencias de la Salud, Universidad de Carabobo, Núcleo Aragua, and the Ministerio de Salud y Desarrollo Social,
Instituto de Altos Estudios de Salud, Dr Arnoldo Gabaldón, Maracay, Venezuela
2
Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street,
London WC1E 7HT, UK
3
Ministerio de Salud y Desarrollo Social, Dirección General de Salud Ambiental y Contralorı́a Sanitaria,
Dirección de Vigilancia Epidemiológica Sanitario Ambiental, Maracay, Venezuela
Following the success of the Southern Cone programme to control Chagas disease, Andean countries
are beginning to implement a similar international
initiative. Important lessons could be learnt from
Venezuela, which has one of the longest running
national control programmes in Latin America, but has
received little attention in the scientific literature. Retrospective analysis of age-specific Trypanosoma cruzi seroprevalence data and entomological sampling indicates
that while the programme successfully reduced the
annual incidence of infection from approximately ten
per 1000 people in the 1950s to one per 1000 in the
1980s, in the susceptible population of endemic areas,
transmission has not yet been interrupted and could
now be increasing. Andean governments can expect
control to be highly effective, but must maintain longterm vigilance and targeted control measures to consolidate these gains.
Within 10 years of Chagas disease being characterized in
Brazil, the first case was recorded in Venezuela [1].
National measurements of prevalence were first reported
in 1960 [2], when it was estimated that 500 000 of a total of
7 million Venezuelans were infected by Trypanosoma
cruzi, with prevalences as high as 45% in some rural
localities. The rate of chagasic myocardiopathy was estimated as 50% in infected people, and 20% in the rural
population as a whole. The overall burden of Chagas
disease was therefore comparable to the most highly endemic
regions of Latin America before large-scale control interventions (http://www.who.int/ctd/chagas/epidemio.htm).
At this time, the highly efficient vector Rhodnius
prolixus was widely distributed, found in 57% of municipalities in 22 of the 23 states, often at very high densities
inside houses. Other, apparently less-effective vectors
were less widely distributed, for example, Triatoma
maculata was found in 31% of municipalities throughout
the same states [3]. Since it was first reported that
Corresponding author: Maria Dora Feliciangeli ([email protected]).
R. prolixus was also found in high densities in palm trees
[4], controversy has remained over whether sylvatic
R. prolixus also colonizes houses (including recolonization
after control) [5– 7]. If re-invasion of houses by sylvatic
R. prolixus populations were common, the challenges to
sustained control in Venezuela would be even greater than
in the Southern Cone, where the main vector Triatoma
infestans is almost exclusively domestic, and post-control
re-infestation, where it occurs, appears to be mainly from
residual domestic populations [8– 10].
Control of Chagas disease in Venezuela
The earliest attempts to control Chagas disease in
Venezuela were made in 1945, when the Ministry of
Health concluded that the DDT sprayed inside houses as
part of the malaria control campaign should also be
effective against triatomine vectors. However, results were
surprising in that rural inhabitants reported increased
numbers of insects after DDT spraying [11]. Replacement
of DDT by hexachlorocyclohexane (HCH) in 1949 was
discontinued because it appeared to show low residual
activity in sprayed houses, despite encouraging results in
the laboratory. Dieldrin was then successfully substituted
for HCH in 1952 and, by 1955, was used in 17 states [11]. To
support the Chagas disease program, the Programa
Nacional de la Vivienda Rural (National Rural Housing
Program) was initiated in 1958, giving loans to householders to substitute their mud-walled palm-roofed huts
with cement block dwellings with zinc roofs, thus depriving domestic triatomines of resting and breeding sites [12].
By April 2000, 443 522 such rural houses had been built,
providing accommodation for . 2 400 000 inhabitants in
high-risk areas [13]. A later programme assisted rural
inhabitants to reduce the suitability of their houses for
triatomine colonization by replacing palm roofs with
metal, plastering adobe walls and cementing dirt floors.
This resulted in the improvement of a further 8776 houses
(with . 48 000 inhabitants) between January 1986 and
April 2000 [13].
Following the apparent success of these interventions,
http://trepar.trends.com 1471-4922/02/$ - see front matter q 2002 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(02)00013-2
Review
TRENDS in Parasitology
the Ministry of Health diverted part of the malaria control
budget and expertise to establish a national Chagas
disease control programme in 1966, with the aim of
interrupting intradomestic transmission by vector control.
Villages considered to be at high risk were selected on the
basis of accumulated experience, rather than strictly
defined criteria. Manual searches were then used to detect
intradomestic infestation and in any village where at least
one positive house was identified, all houses were sprayed
with dieldrin, and all outbuildings with HCH. In contrast
to control programmes elsewhere, sprayed villages were
not routinely revisited after six months to confirm that
control was effective, although the continuous nature of
the control programme means that the same villages
might be revisited after a variable number of months or
years. In addition, blood samples are taken, mainly from
children under ten years of age, if possible, at the same
time and in the same villages as the entomological surveys.
The blood is serologically tested following standard
protocols [14], and the results are used both to monitor
trends in infection and to allocate control resources
between states. The other main interventions have been
the introduction of routine screening of all public hospital
blood banks for T. cruzi using ELISA in 1988 [15], and
ongoing efforts to improve health education.
Although the control policy has remained relatively
constant since 1966, there have been some important
changes in practice. A limited focus of low-level resistance
of R. prolixus to dieldrin was detected in Venezuela
towards the end of the 1960s [16]. The organophosphate
fenitrothion replaced dieldrin and HCH in most states
during the 1980s. More importantly, the early success in
reducing infection and infestation rates to low levels
meant that Chagas disease was no longer considered a
high priority. Coupled with the re-emergence of malaria in
1982 and the dengue hemorrhagic fever emergency of
1989, this resulted in significant resources being diverted
from the Chagas disease control programme. Surveys and
spraying activities have consequently been reduced to
greater or lesser extents in the various states: the number
of municipalities entomologically surveyed declined from
around 110 – 150 per year during 1950s to the 1980s, to
15 – 18 per year in 1990– 1998, while annual insecticide
use for Chagas disease declined from ,44 tonnes to , 6
tonnes per year [17]. Decentralization of health services
throughout Latin America has also obliged the control
programme to devolve prioritization decisions and vector
control resources to the state and municipality level. The
programme still aims to eliminate transmission, but has
first set specific targets: (1) to decrease R. prolixus
infestation indices to below 20% of sampled localities
(and 2% of sampled houses); (2) to decrease T. cruzi
prevalence in R. prolixus to below 0.5%; and (3) to reduce
seroprevalence to less than 0.5% in children under 10
years of age.
In 1997, the Venezuelan Government joined Colombia,
Ecuador and Peru in signing the Andean Pact Initiative,
committing these countries to the elimination of vectorial
transmission of Chagas disease by 2010 [18]. Whereas the
other signatories are only just beginning large-scale
control activities, in Venezuela’s case, this is effectively a
http://trepar.trends.com
Vol.19 No.1 January 2003
45
re-affirmation of the objectives of the long-established
national control programme; hopefully, leading to renewed
political motivation and funding opportunities.
The control programme in Venezuela differs from the
well-known Southern Cone programme [19 –22] which restimulated Chagas disease control in Argentina, Chile,
Uruguay and southern Brazil in the 1990s. It has some
similarities with control programmes that existed in these
countries before the 1990s [23], emphasizing sustained
control over many years rather than a single campaign,
and annual spraying of selected villages with the aim of
reducing transmission below target levels, rather than
complete elimination of domestic bug populations. Several
important features, however, are unique to Venezuela,
such as: (1) an emphasis on house replacement and/or
improvement, as well as insecticide spraying; (2) use of
fenitrothion rather than pyrethroids; (3) no attempt to
introduce community monitoring for post-control reinfestation; and (4) a potential risk of post-control
recolonization from sylvatic populations that are at least
morphologically identical to the main vector species.
Assessing the effectiveness of the control programme
Because the clinical consequences of T. cruzi infection are
delayed, chronic and difficult to diagnose, progress made in
the interruption of Chagas disease transmission is best
shown by the results of successive seroprevalence surveys
[24 –27]. In Venezuela, such seroprevalence data are available from the combined entomology and serology surveys
described above, recorded in the scattered reports of the
Dirección de Endemias Rurales (Office of Rural Endemic
Diseases). Summaries of these data [17,28] show that the
proportion of samples taken across the country that were
seropositive (the national seroprevalence) was 44.5% in
1958– 1968, 15.6% in 1969– 1979, 13.7% in 1980– 1989 and
8.1% in 1990– 1999. In children under 10 years of age, the
figures were 20.5%, 3.9%, 1.1% and 0.8%, respectively.
Although large and unequivocal reductions are shown,
the precise values shown here might be somewhat
imprecise and difficult to interpret because they depend
on the relative amounts of sampling in more or less
endemic areas, and the diagnostic methods used at
different times. Because infection confers lifelong seropositivity, the observed prevalences reflect the cumulative
infection rate throughout the lifetime of the population,
rather than just the sample period. They also depend
crucially on the age distribution of the sampled population,
and are affected not only by the infection rate, but also by
the death rate [29]. A potentially less biased and more
intuitive measure of the change in transmission was
derived using only the most recent age-stratified seroprevalence data (1992 – 1999) to calculate retrospectively
the average force of infection (FOI) [30] (the per capita rate
at which susceptibles acquire infection) for each year from
1945 to 1999. The results of this analysis (Box 1; Fig. 1)
confirm that the force of T. cruzi infection showed little
tendency to decrease before the implementation of
control activities. Transmission dropped dramatically
after the implementation of the national control programme in 1966, although part of this drop could be a
result of the cumulative effect of the earlier interventions.
Review
46
TRENDS in Parasitology
Vol.19 No.1 January 2003
Box 1. Cross-sectional Trypanosoma cruzi age-seroprevalence data and the force of infection
0
Average age
0.3
0.2
0.1
0
Average age
ðEqnIIÞ
Where P is the age –specific seroprevalence and l is the annual FOI for
each year over the time period [y 2 (a 2 2.5)] to [y 2 (a þ 1.5)].
The FOI in each period was allowed to vary independently, until the
maximum-likelihood fit between the modelled and observed age –
prevalence curves was optimized. This procedure was applied sequentially to the results of each year’s survey.
The resulting estimates represent average annual FOI over five-year
periods. In addition, surveys in different years can give information
about the same time point: For example, the FOI in 1945–1950 can also
be measured by comparing 45-year-olds with 50-year-olds, surveyed in
1995. Our best estimate of FOI in any year is given by averaging across
all independent measurements (i.e. those from each survey year). To
assess the fit of this model, we applied our estimates of FOI over time to
Eqns I and II, to generate predicted age – prevalencecurves. These
showed good agreement with the observed data from the various
annual surveys, as shown in Fig. Ia–d. Ageseroprevalence curves
showed a similar pattern in 1992, 1994, 1996 and 1998 (data not shown).
References
a Grenfell, B.T. and Anderson, R.M. (1985) The estimation of agerelated rates of infection from case notifications and serological data.
J. Hyg. (Lond.) 95, 419 – 436
b Williams, B.G. and Dye, C. (1994) Maximum-likelihood for parasitologists. Parasitol. Today 10, 489 – 493
c Mota, E.A. et al. (1990) A nine year prospective study of Chagas’
disease in a defined rural population in northeast Brazil. Am. J. Trop.
Med. Hyg. 42, 429– 440
d Contreras, F.T. et al. (2000) Serological follow-up of Trypanosoma
cruzi infection from 1987 to 1994 in 50 countries of the State of
Jalisco. Mexico. Rev. Soc. Bras. Med. Trop. 33, 591 – 596
e Aché, A. and Matos, A.J. (2001) Interrupting Chagas disease
transmission in Venezuela. Rev. Inst. Med. Trop. São Paulo 43,
37 – 43
(d)
0.4
0.3
0.2
0.1
0
Average age
0.4
0.3
0.2
0.1
0
2.5
7.5
12.5
17.5
22.5
27.5
32.5
37.5
42.5
47.5
0.1
Pðy;aÞ ¼ Pðy;a25Þ þ ½1 2 Pðy; a 2 5Þ½1 2 e 25l 2.5
7.5
12.5
17.5
22.5
27.5
32.5
37.5
42.5
47.5
0.2
0.4
ðEqnIÞ
For a . 2.5 years (all other age groups)
Infection prevalence
0.3
Pðy;aÞ ¼ 1 2 e 22:5l
(c)
2.5
7.5
12.5
17.5
22.5
27.5
32.5
37.5
42.5
47.5
0.4
Infection prevalence
(b)
2.5
7.5
12.5
17.5
22.5
27.5
32.5
37.5
42.5
47.5
Infection prevalence
(a)
set to zero, and the FOI in each five-year period determined the
difference in seroprevalence between age groups.
More formally, if y is the year of the cross-sectional survey, and a is the
mid-point age of the five-year age group, then for a ¼ 2.5 years (i.e. the
youngest age group, 0 –5 years old):
Infection prevalence
The age-seroprevalence patterns observed in cross-sectional surveys
reflect previous rates of infection and serorecovery, and any difference
between seropositive and seronegative individuals in rates of emigration, immigration and death. Most previous studies assume that
population movements are independent of infection status, and attempt
to measure variation in infection rates with age (making the additional
assumption that infection rates are constant over time) [a], or to estimate both infection and serorecovery rates (assuming that these do not
vary either with age or time) [b].
Age-seroprevalence patterns for Trypanosoma cruzi infection are
easier to interpret than for many infections. Because the overwhelming
majority of triatomine bites on humans occur inside houses, infections
are broadly independent of age [c]. Serorecovery is either very rare or
non-existent [c,d]. There is no evidence that infected and noninfected
people differ in their tendency to enter or leave the survey area, which in
the Venezuelan situation covers the rural population of all endemic
states. Although infected individuals could suffer higher mortality
(leading to an underestimate of risk in the earlier years), this effect
should be relatively small. Thus, the observed differences in prevalence
between age groups can be attributed to infections acquired in the
specific additional years lived by the older subjects. For example, for a
survey conducted in 1990, the difference in prevalence between subjects
who are an average of 45 years old (i.e. born in 1945), and those who are
40 (i.e. born in 1950), is a measure of the overall risk of infection during
1945 –1950.
Our calculations are based on age seroprevalence rates derived from
over 110 000 samples taken in field surveys by the Venezuelan National
Control Programme between 1992 and 1999 (previously published in
summarized form in Ref. [e]). Data were supplied by the control
programme as numbers of positive and negative samples, divided into
five-year age classes, and by state. Surveys are concentrated in regions
considered highly endemic (. 85% of the samples are from rural areas in
only six out of the 23 states), and the measurements therefore do not
represent the overall national seroprevalence. However, because the
calculations for force of infection (FOI) depend on comparisons between
age groups within the same survey, they should not be affected by yearto-year sampling variations, and should therefore allow unbiased
estimation of trends within these regions over time. The surveys are
also independent because they are taken in a different sample of villages
in each year.
The maximum likelihood method described by Williams and Dye [b]
was used to estimate FOI. The method was adapted to reflect the
characteristics of T. cruzi infection outlined above: the recovery rate was
Average age
TRENDS in Parasitology
Fig. I. Fit of age –prevalence curves predicted from estimates of force of infection over time (lines) to observed data (bars) from independent surveys carried out in: (a)
1993; (b) 1995; (c) 1997; and (d) 1999.
The past 20 years, however, have seen no further decrease
and there is a suggestion of a slight increase towards the
end of the 1990s (although this is based on a smaller
number of surveys than earlier periods). This is supported
http://trepar.trends.com
by surveys of seroprevalence in blood donors, which oscillated between 0.77% and 1.32% from 1992 to 1997 [31].
The method described in Box 1 was also applied
separately to the results of surveys in the 11 states with
Review
TRENDS in Parasitology
0.020
FOI per year
0.016
0.012
0.008
0.004
0
1940
1950
1960
1970
1980
1990
47
Vol.19 No.1 January 2003
2000
Year
TRENDS in Parasitology
Fig. 1. Trends in estimated annual force of Trypanosoma cruzi infection (FOI) in
endemic areas of Venezuela. Note that all estimates from 1950 to 1992 are the average of eight independent survey years. Estimates either side of this period are
based on decreasing numbers of surveys, and are therefore less reliable. Different
time events are indicated as follows: insecticide spraying at the state level (green);
housing programme initiated (blue); and national control programme initiated
(red).
. 1000 samples over the period from 1992 to 1999. The
resulting estimates of annual FOI were then averaged for
the decade before the implementation of the national
control programme (1956 – 1965), and for subsequent
decades to 1995 (Fig. 2). This confirms that transmission
has been drastically cut throughout the endemic area, but
not yet eliminated in the most severely affected states.
At present, Chagas disease in Venezuela appears to be
restricted principally to the foothills of the Andean and
coastal mountain range. Age– prevalence data from 1996
to 1999 demonstrate that infection levels in children under
10 years of age remain above the 0.5% target levels in
Portuguesa (1.3%), Barinas (0.9%) and Yaracuy (0.8%).
The effectiveness of the control programme can also be
measured from entomological surveys. These are a more
sensitive measure of current transmission risk and therefore future infection rates. Although the precise values
again depend on where sampling took place, comparison of
summarized infestation prevalences in different decades
demonstrates that the vector control activities had a very
large impact in the early years, reducing the estimated
house infestation rates from 60 – 80% in 1958 – 1968 to
1.6 – 4.0% in 1990– 1998 [17]. However, the overall geographic distribution of triatomines has not decreased: 20
triatomine species have now been reported throughout the
country [32], with R. prolixus in 79.1% of municipalities
[28]. Results from the past ten years are tested for temporal trends in Box 2. The sampled infestation prevalence
is relatively low, but is no longer decreasing. Infestation is
also recorded in a significant proportion of previously
sprayed villages.
In summary, it is clear that the Venezuelan control
Box 2. Investigating recent risk trends using entomological data
Although the lifelong positivity of Trypanosoma cruzi-infected patients
allows the estimation of historical infection rates (Box 1), it obscures
more recent trends because only infections in the youngest age groups
can be safely attributed to transmission in recent years. Because
infection rates are low, a large sampling effort is required to make
accurate measurements.
The Venezuelan National Control Programme also actively searches
rural houses in the 14 states (out of 23) that are considered at highest
risk, recording house and locality level measurements of the prevalence
of infestation with: (1) triatomines; and (2) infected triatomines.
Comparison of these measures taken in different years should provide
a more sensitive measurement of recent trends in risk. However,
sampling effort varies markedly over time, depending on the availability
of resources. In years when the operational budget is small, surveillance
teams tend to visit those areas that they consider to be at highest risk.
Year-to-year variation in the amount of sampling effort might therefore
affect the prevalence measures and obscure real trends.
We tested for temporal trends in infestation rates in . 250 000 houses
surveyed between 1990 and 1999. Data were supplied by the National
Control Programme, and describe: (1) numbers of houses and localities
searched; (2) numbers found infested with triatomines; and (3) numbers
found infested with triatomines positive for T. cruzi, divided by state and
by year. Binomial regression models with logistic errors were used to
test for a linear time trend in each variable (i.e. testing whether the odds
of houses or localities being found positive in each state changes over
time) [a]. To control for variation in sampling effort in space and time, we
included a categorical variable representing the state from which
samples were taken, and a continuous variable representing the
number of localities or houses sampled, as a proportion of the total
number recorded in the 1990 census [b]. The results of this analysis
(Table I) indicate that there has been no progress in reducing infestation
rates over the past ten years. If anything, the measures have increased,
emphasizing the need for continued control. Prevalence measures vary
between states and, for most indicators, also vary inversely with
amount of sampling effort (confirming that when resources are limited,
more endemic areas are indeed sampled first). Standardized stratified
surveys will therefore be necessary to accurately measure progress
towards the official targets.
References
a Crawley, M.J. (1993) GLIM for Ecologists, Blackwell
b Oficina Central de Estadistica e Informàtica (2000) Nomenclador de
Centros Poblados, CD-ROM
Table I. Factors affecting prevalence of entomological indicators during 1990 –1999
Year since 1990a
Percentage sampleda
Stated
a
Localities with
triatomines
Houses with
triatomines
Localities with
infected triatomines
Houses with
infected triatomines
1.049 (0.986, 1.116)b
0.994 (0.985, 1.003)b
F13,97 ¼ 13.7c
1.026 (0.961, 1.095)b
0.983 (0.974, 0.993)c
F13,97 ¼ 14.3c
1.010 (0.930, 1.097)b
0.956 (0.940, 0.973)c
F13,97 ¼ 56.4c
1.056 (0.996, 1.123)b
0.976 (0.969, 0.984)c
F13,97 ¼ 74.5c
The statistical significance of the trend in probability of being positive, for each additional year since 1990, and each percentage increase in sampling
coverage is indicated. The 95% confidence intervals for the odds ratios are given in parentheses.
b
These values were non-significant (P . 0.05).
c
P , 0.001.
d
F-value and associated statistical significance of the variation between states.
http://trepar.trends.com
48
Review
TRENDS in Parasitology
(a)
Falcon Lara
Yaracuy
Carabobo
Aragua
Guarico
Vol.19 No.1 January 2003
(b)
Anzoategui
Merida
Barinas
Portuguesa
Cojedas
(c)
(d)
<1000 samples
0.001 – 0.005
0.01 – 0.015
0 – 0.001
0.005 – 0.01
0.015 – 0.019
TRENDS in Parasitology
Fig. 2. Average annual force of infection (FOI) in the states of Venezuela in: (a) 1956– 1965; (b) 1966–1975; (c) 1976–1985; (d) 1986–1995. States for which the total number
of serological samples collected is judged insufficient to reliably estimate FOI (, 1000) are shown in white.
programme has greatly reduced the prevalence of triatomine infestation in rural houses. This has led to a dramatic
drop in the incidence of T. cruzi infection in humans,
presumably both by reducing vectorial transmission and
(as secondary, long-term mechanisms) reducing the
frequency with which infections are transmitted either
through blood banks, or congenitally. However, the goal
of interrupting transmission has not been achieved and
there has been no real progress in further reducing risk in
recent years. It is not clear whether this is due to problems
with the efficacy of insecticide spraying, incomplete and
recently reduced coverage (allowing re-invasion from
unsprayed areas), or continuous re-invasion of sylvatic bugs.
Prospects for the future
Accumulated experience in Venezuela suggests that the
aim of the control programme to eliminate vectorial transmission is highly desirable, but unlikely to be achieved in
the short term. At worst, it might be impossible (due to
possible re-invasion from sylvatic vectors), or at best
require large increases in control resources and/or major
improvements in the quality of rural housing. In the
absence of these conditions, the new management policy of
the Chagas disease control program in Venezuela is
focusing on two major areas: (1) the integral medical
attention of chagasic patients; and (2) vector control and
monitoring, targeted as accurately as possible towards
those locations with the highest transmission rates and
the greatest risk of re-infestation following control.
The first aim is to be met by the organization of
nationwide workshops, training programmes and manuals to standardize practices for clinical, epidemiological
and laboratory diagnosis, and symptomatic medical treatment. Increased awareness at the primary health care
http://trepar.trends.com
level would permit early detection of acute cases (particularly pregnant chagasic women and their newborn infants),
and treatment to prevent progression to chronic status
[33]. The safety of blood transfusions will continue to be
guaranteed through the quality control of blood screened
for T. cruzi in all blood banks. To achieve the second aim,
vector control will continue to be carried out at state level
by the Rural Endemic Diseases Services, in response both
to the results of entomological and serological surveys, and
notification of acute cases by the Services of Epidemiology.
However, given the decreased resources now available
for Chagas control, further monitoring and research will
be needed to ensure that control effort is directed as
effectively as possible. Most sampling is currently carried
out in localities that have been shown to be at high risk in
the past, and many potentially infested sites still have not
been surveyed. This is now being addressed by stratified,
random surveys across a range of ecotypes. Because the
measurements of infestation prevalence depend on the
amount and distribution of sampling effort (Box 2),
standardized repeated surveys are also necessary to
measure progress towards the national targets.
There has been little emphasis on research for several
decades because Chagas disease control in Venezuela has
previously been well funded and successful. This is now
changing and it is becoming appreciated that applied
research could help optimize the cost-effectiveness of
control. The Venezuelan Control Programme is collaborating in new research projects in several important areas.
These include measurements of susceptibility and resistance to a variety of insecticides, and comparisons of entomological monitoring methods. Other studies will combine
analyses of the environmental and social influences on
post-control re-infestation of houses (testing whether
Review
TRENDS in Parasitology
specific housing characteristics and the proximity of palms
harboring sylvatic bugs are significant risk factors), with
population genetic studies (measuring the similarity
between pre- and post-control domestic populations, and
nearby sylvatic populations). This should be a major contribution to the currently inconclusive debate over the
frequency with which sylvatic Triatominae might colonize
houses. Taken together, these projects should help to
identify the most appropriate monitoring and control tools,
and target them to where they will have most effect.
Conclusions
Vector control was implemented at an early stage in
Venezuela relative to most other Latin American countries,
and has dramatically reduced transmission. Most unusually
for a vector-borne disease control programme in a developing
country, the FOI has been effectively kept at a low level for
several decades. It has therefore averted a huge burden of
disease among the rural poor.
Despite early successes, the programme has yet to
achieve the goal of eradicating transmission and currently
faces the challenge of maintaining effective control with
fewer resources and less central management. Infestation
and infection rates are no longer dropping, and the
analyses presented in this article suggest that they
might be increasing. Control personnel are therefore reexamining how best to target treatment, monitoring and
control effort.
There are clear lessons from the Venezuelan experience,
not only for the other participants in the Andean Pact
Initiative, but also for similar regional programmes elsewhere (e.g. the Central American Initiative, also signed in
1997 [34,35]). First, it reinforces the message from the
Southern Cone: vector control can be highly effective in
cutting transmission rates and should be implemented as
widely as soon as possible. Second, the unique long-term
experience of the control programme demonstrates that
eradication might be difficult to achieve and that either
localized control failure or re-infestation can occur, at least
under the ecological, social and control conditions in
Venezuela. Governments should appreciate the value of
continuing to invest in programmes that consistently
deliver large net health gains, but which might not be as
visible as interventions in other diseases. Control programmes, for their part, should develop long-term strategies to target their monitoring and control so as to make
the best possible use of limited resources.
Acknowledgements
Thanks to Alı́ Matos for provision of surveillance data, and Katrin Kuhn,
Ricardo Gurtler and three anonymous reviewers for constructive
comments on the manuscript. This work was supported by a Wellcome
Trust project grant. Paul Coleman is funded by the UK Department for
International Development.
References
1 Tejera, E. (1919) La Trypanosome Americaine ou maladie de Chagas au
Venezuela. Bull. Soc. Pathol. Exot. (Paris) 12, 509– 513
2 Pifano, F. (1960) Algunos aspectos de la Enfermedad de Chagas en
Venezuela. Arch.Venez. Med. Trop. Parasit. Méd. 3, 73 – 99
3 Cova Garcı́a, P. and Suarez, M., Estudio de los triatominos de
Venezuela. (Publ. No. 11.) Ministerio de Sanidad y Asistencia Social
http://trepar.trends.com
Vol.19 No.1 January 2003
49
4 Gamboa, C.I. (1963) Comprobación de Rhodnius prolixus extradomiciliarios en Venezuela. Bol. San. Panam. 54, 18 – 25
5 Dujardin, J.P. et al. (1998) The origin of Rhodnius prolixus in Central
America. Med. Vet. Entomol. 12, 113 – 115
6 Schofield, C.J. and Dujardin, J.P. (1999) Theories on the evolution of
Rhodnius. Actualidades Biologicas 70, 183– 197
7 Monteiro, F.A. et al. (2001) Molecular tools and triatomine systematics:
a public health perspective. Trends Parasitol. 17, 344 – 347
8 Gurtler, R.E. et al. (1994) Chagas disease in north-west Argentina: risk
of domestic reinfestation by Triatoma infestans after a single
community-wide application of deltamethrin. Trans. R. Soc. Trop.
Med. Hyg. 88, 27 – 30
9 Dujardin, J.P. et al. (1998) Population structure of Andean Triatoma
infestans: allozyme frequencies and their epidemiological relevance.
Med. Vet. Entomol. 12, 20 – 29
10 Dujardin, J.P. et al. (1997) The use of morphometrics in entomological
surveillance of sylvatic foci of Triatoma infestans in Bolivia. Acta Trop.
66, 145 – 153
11 Berti, A.L. et al. (1960) Ensayos profilácticos de la Enfermedad de Chagas
en Venezuela. Arch. Venez. Med. Trop. Parasit. Méd. 3, 203–238
12 Briceno-Leon, R. (1987) Rural housing for control of Chagas disease in
Venezuela. Parasitol. Today 3, 384 – 387
13 Anon. (2000) Records of the ‘Servicio Autónomo de la Vivienda Rural’
14 WHO (1991) Control of Chagas Disease (Report of a WHO Expert
Committee). WHO Tech. Rep. Ser. 811
15 Ache, A. (1993) Prevalence of human infections by Trypanosoma cruzi in
blood banks in Venezuela. Rev. Inst. Med. Trop. São Paulo 35, 443–448
16 Nocerino, F. (1972) Resistance of Rhodnius prolixus Stal to Dieldrin in
Venezuela (WHO/VBC/IRG/72-21)
17 Aché, A. and Matos, A.J. (2001) Interrupting Chagas disease
transmission in Venezuela. Rev. Inst. Med. Trop. São Paulo 43, 37 – 43
18 WHO (1997) Andean countries initiative launched in Colombia, TDR
News 53
19 Schmunis, G.A. et al. (1996) Interruption of Chagas’ disease
transmission through vector elimination. Lancet 348, 1171
20 Schofield, C.J. and Dias, J.C. (1999) The Southern Cone Initiative
against Chagas disease. Adv. Parasitol. 42, 1 – 27
21 WHO, (1998) Chagas disease – interruption of transmission, Uruguay.
Weekly Epidemiol. Rec. 1, 4
22 WHO, (2000) Chagas disease, Chile. certification of interruption of
transmission. Weekly Epidemiol. Rec. 2, 1 – 12
23 Dias, J.C.P. (1987) Control of Chagas disease in Brazil. Parasitol.
Today 3, 336 – 341
24 Camargo, M.E. et al. (1984) [Serological survey of the prevalence of
Chagas’ infection in Brazil, 1975/1980]. Rev. Inst. Med. Trop. São
Paulo 26, 192 – 204
25 Hoff, R. et al. (1985) Serologic surveillance of Chagas’ disease. Ann.
Soc. Belg. Med. Trop. 65 (Suppl. 1), 187 – 196
26 de Andrade, A.L. et al. (1992) Surveillance of Trypanosoma cruzi
transmission by serological screening of schoolchildren. Bull. WHO 70,
625– 629
27 Costa, F.C. et al. (1998) Chagas disease control programme in Brazil: a
study of the effectiveness of 13 years of intervention. Bull. WHO 76,
385– 391
28 Aché, A. (1993) Programa de control de la Enfermedad de Chagas en
Venezuela. Bol. Dir. Malar. San. Amb. 33, 11 – 22
29 Carrasco, R.L. et al. (1985) Chagas serology and its problems. Ann. Soc.
Belg. Med. Trop. 65 (Suppl 1), 79 – 84
30 Anderson, R.M. and May, R.M. (1991) Infectious Diseases of Humans:
Dynamics and Control, Oxford University Press
31 Anon. (2000) Records of the Department of Transfusions and Blood
Banks of the Ministry of Health and Social Development: Ministry of
Health and Social Development
32 Ramirez Perez, J. (1987) Revisión de los triatominos (Hemiptera:
Reduviidae) en Venezuela. Bol. Dir. Malar. San. Amb. 27, 118 – 146
33 Rodriques Coura, J. and de Castro, S.L. (2002) A critical review on
Chagas disease chemotherapy. Mem. Inst. Oswaldo Cruz 97, 3 – 24
34 Schofield, C.J. and Dujardin, J.P. (1997) Chagas disease vector control
in Central America. Parasitol. Today 13, 141 – 144
35 Moncayo, A. (1999) Progress towards the interruption of transmission
of Chagas disease in Latin America. Medicina-Buenos Aires 59,
120– 124