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Dispatch
Chagas Disease in a Domestic
Transmission Cycle, Southern Texas, USA
Charles B. Beard,* Greg Pye,† Frank J. Steurer,* Ray Rodriguez,‡ Richard
Campman,† A. Townsend Peterson,§ Janine Ramsey,¶ Robert A. Wirtz,* and
Laura E. Robinson†
*Centers for Disease Control and Prevention, Atlanta, Georgia, USA; †Texas
Department of Health, Harlingen, Texas, USA; ‡Cameron County Health Department,
San Benito, Texas, USA; §Natural History Museum, University of Kansas,
Lawrence, Kansas, USA; ¶Centro de Investigaciones sobre Enfermedades Infecciosas,
Instituto Nacional de Salud Pública Cuernavaca, Morelos, México
Suggested citation for this article: Beard CB,
Pye G, Steurer FJ, Rodriguez R, Campman R, Peterson AT, et al. Chagas
disease in a domestic transmission cycle in southern Texas, USA. Emerg
Infect Dis [serial online] 2003 Jan [date cited]. Available from:
URL: http://www.cdc.gov/ncidod/EID/vol9no1/02-0217.htm
After three dogs
died from acute Chagas cardiomyopathy at one location, an investigation
was conducted of the home, garage, and grounds of the owner. A serologic
study was conducted on stray dogs, and an ecologic niche model was developed
to predict areas where the vector Triatoma gerstaeckeri might
be expected.
The Study
Chagas disease is caused by the parasitic protozoan Trypanosoma cruzi
and affects an estimated 12 million persons throughout South and Central
America and Mexico (1,2). In the United States, the disease
exists almost exclusively as a zoonosis; only five autochthonous insect-borne
cases have been reported in humans (3). The distribution
of Chagas disease in the United States includes approximately the southern
half of the country. Twelve species of triatomines are known to occur
in the United States, the most important being Triatoma sanguisuga
in the eastern United States, Triatoma gerstaeckeri in the region
of Texas and New Mexico, and Triatoma rubida and Triatoma protracta
in Arizona and California (4,5).
In the small community of San Benito, Texas (Figure
1), after three pet dogs died from Chagas cardiomyopathy, personnel
from the Texas Department of Health, the Cameron County Health Department,
Environmental Health Division, and the Centers for Disease Control and
Prevention (CDC) inspected the owner’s home, garage, and grounds for potential
triatomine insect vectors (Figure 2). Blood was
drawn from four dogs and two persons residing on the property and tested
for antibodies to T. cruzi. A second site approximately 2 miles
away was also inspected and blood drawn from three dogs, one of which
had been diagnosed as positive for T. cruzi by the original veterinarian.
A follow-up serologic survey was conducted to determine the percentage
of the stray dogs in Cameron County that would test positive for Chagas
disease antibodies. Once a week, samples from stray dogs were shipped
to CDC for testing. Each sample was issued an identification number; and
information on the animal’s location, sex, age, health condition, and
size was recorded. Serum specimens were tested for anti-T. cruzi
antibodies by indirect immunofluorescence (IIF) (6,7).
Ecologic niches and potential geographic distributions were modeled by
using the Genetic Algorithm for Rule-set Prediction (GARP) (8-10).
In general, the procedure focuses on modeling ecologic niches, the conjunction
of ecologic conditions within which a species is able to maintain populations
without immigration. Specifically, GARP relates ecologic characteristics
of known occurrence points to those of points randomly sampled from the
rest of the study region, seeking to develop a series of decision rules
that best summarizes those factors associated with the species’ presence.
Recently, this method has been used to study the distribution of species
complex members and vector-reservoir relationships with respect to Chagas
disease (11,12).
Inspection of the residence where the three dogs lived indicated a substantial
infestation with the triatomine species T. gerstaeckeri (Figure
3). Triatomines were collected under cement slabs of a backyard patio
adjacent to the house and from a garage located approximately 75 feet
from the home (Figure 2). Of 31 live triatomines
collected, including adults of both sexes and immature stages (i.e., two
fifth-instar nymphs), 24 contained T. cruzi-like parasites in their
hindgut (Figure 4). Cultures were established from
triatomine urine collected from insects that were fed in the laboratory
and placed in 1.5-mL microcentrifuge tubes. Approximately 50 µL of clear
urine was injected into Novy, Nicolle, & MacNeal culture medium (13).
The cultures were positive for parasites confirmed to be T. cruzi,
on the basis of morphologic criteria. Inspection of the second residence
failed to indicate a bug infestation; however, the pet owner recalled
frequently observing both rats (Rattus spp.) and opossums (Didelphis
virginiana) on the premises. At the first site, three of the four
dogs tested positive for T. cruzi, with titers ranging from 1:128
to 1:256. Neither of the two persons had positive antibody titers against
T. cruzi. At the second site, only the previously diagnosed dog
tested positive, with a titer of 1:256. The other two dogs tested negative,
as did the pet owner. Serum samples from stray dogs from Cameron County,
Texas, were tested for anti–T. cruzi antibodies. Of 375 dogs tested,
28 (7.5%) were positive by IIF, with titers ranging from 1:32 to 1:512.
The sensitivity of this test in humans is 98.8% (pers. comm., Patricia
P. Wilkins, Division of Parasitic Diseases, CDC). Because of the low specificity
of serologic tests for distinguishing T. cruzi from Leishmania
spp., all positive samples were tested for antibodies to L. donovani.
A low level of cross-reactivity was observed in 17 of the 28 samples.
In each case, however, the titer was 1–2 dilutions less than the titer
to T. cruzi, indicating a primary response to T. cruzi rather
than to Leishmania spp. Ecologic niche models for T. gerstaeckeri
were developed by using GARP, based on published and unpublished collection
records from Mexico and the southwestern United States. The model predicted
a distribution for this species that extends from central Mexico, through
central Texas, the Texas panhandle, into northern Texas and southeastern
New Mexico (Figure 5).
Conclusions
Triatoma gerstaeckeri is considered a sylvatic species, most frequently
associated with pack rat (Neotoma spp.) burrows (4).
Although individual triatomine insects occasionally invade domestic dwellings
throughout the southwestern United States and Mexico (4,5,14),
this species has not been reported to colonize these habitats. In this
investigation, colonization appears to have occurred, based on the observation
of large numbers of bugs, including ones in immature stages. In the Chagas
disease–endemic regions of South and Central America, the primary risk
for insect transmission to humans is related to the efficiency with which
local vector species can invade and colonize homes, resulting in a domestic
transmission cycle for what is otherwise exclusively a zoonotic disease
in the southern United States. In disease-endemic countries, higher house
infestation rates generally result in a higher risk of transmission. At
the first site in south Texas, six dogs either died or tested positive
for T. cruzi, and 24 of 31 bugs contained hindgut trypanosomes.
These observations demonstrate the existence of a domestic transmission
cycle for an insect species that is typically considered a zoonotic vector.
Whether this observation represents an isolated case or actually occurs
more frequently but remains unrecognized, indicating an emerging public
health problem, remains to be determined. The serologic results in stray
dogs are very similar to those reported in previous studies from the region,
suggesting that the disease is stably maintained in this reservoir host
(15,16). The distributional predictions based on GARP
models indicate a potentially broad distribution for this species and
suggest additional areas of risk beyond those previously reported (14),
should this problem become of greater public health concern.
Dr. Beard is chief
of the Vector Genetics Section in the Division of Parasitic Diseases,
Centers for Disease Control and Prevention. His research focuses on
the molecular biology of insect disease vectors and the molecular epidemiology
of Pneumocystis pneumonia in HIV-infected persons.
References
- Schmunis GA. Iniciativa del Cono Sur. In: Schofield
CJ, Ponce C, editors. Proceedings of the second international workshop
on population biology and control of Triatominae, Col. Santo Tomás,
México: Instituto Nacional de Diagnostico y Referencia Epidemiológicos;
1999. p. 26–31.
- Monteiro FA, Escalante AA, Beard CB. Molecular
tools and triatomine systematics: a public health perspective. Trends
Parasitol 2001;17:344–7.
- Herwaldt BL, Grijalva MJ, Newsome AL, McGhee CR, Powell MR, Nemec
DG, et al. Use
of polymerase chain reaction to diagnose the fifth reported US case
of autochthonous transmission of Trypansoma cruzi, in Tennessee,
1998. J Infect Dis 2000;181:395–9.
- Lent H, Wygodzinski P. Revision of the Triatominae (Hemiptera: Reduviidae)
and their significance as vectors of Chagas disease. Bull Am Mus Nat
Hist 1979;163(Pt. 3):123–520.
- Ryckman RE. The Triatominae of North and Central America and the West
Indies: a checklist with synonymy (Hemiptera: Reduviidae: Triatominae).
Bulletin of the Society of Vector Ecologists 1984;9:71–8.
- Camargo M. 1969. Cross-reactivity
in fluorescence tests for Trypanosoma and Leishmania antibodies.
Am J Trop Med Hyg 1969;18:500–5.
- Kagan IG. Serodiagnosis of parasitic diseases. In: Lennet EH, Balows
A, Hausler WJ, Truant JP, editors. Manual of clinical microbiology.
3rd ed. Washington: American Society for Microbiology; 1980. p. 724–50.
- Stockwell DRB, Noble IR. Induction of sets of rules from animal distribution
data: a robust and informative method of analysis. Mathematics and Computers
in Simulation 1992;33:385–90.
- Stockwell DRB. Genetic algorithms II. In: Fielding AH, editor. Machine
learning methods for ecological applications. Boston: Kluwer Academic
Publishers; 1999. p. 123–44.
- Stockwell DRB, Peters DP. The GARP modeling system: problems and solutions
to automated spatial prediction. International Journal of Geographic
Information Systems 1999;13:143–58.
- Costa J, Peterson AT, Beard CB. Ecological niche
modeling and differentiation of populations of Triatoma brasiliensis
Neiva, 1911, the most important Chagas disease vector in northeastern
Brazil (Hemiptera, Reduviidae, Triatominae). Am J Trop Med Hyg 2002;67:516-20.
- Peterson AT, Sanchez-Cordero V, Beard CB, Ramsey JM. Identifying
mammal reservoirs for Chagas disease in Mexico via ecological niche
modeling of occurrences of ectoparasites and hosts. Emerg Infect
Dis 2002;8:662–7.
- American Society for Microbiology. Clinical microbiology procedures
handbook. Section 7. Parasitology. Washington: American Society for
Microbiology; 1992.
- Sullivan TD, McGregor T, Eads RB, Davis J. Incidence of Trypanosoma
cruzi, Chagas, in Triatoma (Hemiptera, Reduviidae) in Texas.
Am J Trop Med Hyg 1949;29:453–8.
- Burkholder JE, Allison TC, Kelly VP. Trypanosoma cruzi (Chagas)
(Protozoa: Kinetoplastida) in invertebrate, reservoir, and human hosts
of the lower Rio Grande Valley of Texas. J Protozol 1980;66:305–11.
- Bradley KK, Bergman DK, Woods, JP, Crutcher JM, Kirchoff
LV. Prevalence of American trypanosomiasis (Chagas disease) among dogs
in Oklahoma. J Am Vet Med Assoc 2000;217;1853–7.
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