Trypanosoma cruzi infection diagnosed in dogs in nonendemic areas and results from a survey suggest a need for increased Chagas disease awareness in North America

Emily A. Gavic BluePearl Veterinary Partners, Southfield, MI

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Sarah E. Achen BluePearl Veterinary Partners, Southfield, MI

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Phillip R. Fox The Animal Medical Center, New York, NY

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Eduardo J. Benjamin Veterinary Teaching Hospital, College of Veterinary Medicine, Washington State University, Pullman, WA

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Jonathan Goodwin Garden State Veterinary Specialists, Tinton Falls, NJ

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Tamilselvam Gunasekaran BluePearl Veterinary Partners, Southfield, MI

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Karsten E. Schober Department of Clinical Sciences, College of Veterinary Medicine, The Ohio State University, Columbus, OH

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Sonja S. Tjostheim Department of Medical Sciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI

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John Vickers Castle Pines Veterinary Hospital, Castle Pines, CO

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Jessica L. Ward Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Iowa State University, Ames, IA

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Duncan S. Russell Department of Biomedical Sciences, Carlson College of Veterinary Medicine, Oregon State University, Corvallis, OR

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Mark Rishniw Veterinary Information Network, Davis, CA

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Sarah A. Hamer Department of Veterinary Integrative Biosciences, School of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, TX

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Ashley B. Saunders Department of Small Animal Clinical Sciences, School of Veterinary Medicine & Biomedical Sciences, Texas A&M University, College Station, TX

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Abstract

OBJECTIVE

To describe the clinical presentation and outcome in dogs diagnosed with Trypanosoma cruzi infection in nonendemic areas and to survey veterinary cardiologists in North America for Chagas disease awareness.

ANIMALS

12 client-owned dogs; 83 respondents from a veterinary cardiology listserv.

PROCEDURES

A retrospective, multicenter medical records review to identify dogs diagnosed with American trypanosomiasis between December 2010 and December 2020. An anonymous online survey was conducted August 9 to 22, 2022.

RESULTS

Diagnosis was made using indirect fluorescent antibody titer (n = 9), quantitative PCR assay (1), or postmortem histopathology (2). Time spent in Texas was < 1 year (n = 7) or 2 to 8 years (5). Time in nonendemic areas prior to diagnosis was < 1 year (n = 10) and > 3 years (2). Eleven had cardiac abnormalities. Of the 12 dogs, 5 had died unexpectedly (range, 1 to 108 days after diagnosis), 4 were still alive at last follow-up (range, 60 to 369 days after diagnosis), 2 were euthanized because of heart disease (1 and 98 days after diagnosis), and 1 was lost to follow-up. Survey results were obtained from 83 cardiologists in North America, of which the self-reported knowledge about Chagas disease was limited in 49% (41/83) and 69% (57/83) expressed interest in learning resources.

CLINICAL RELEVANCE

Results highlight the potential for encountering dogs with T cruzi infection in nonendemic areas and need for raising awareness about Chagas disease in North America.

Abstract

OBJECTIVE

To describe the clinical presentation and outcome in dogs diagnosed with Trypanosoma cruzi infection in nonendemic areas and to survey veterinary cardiologists in North America for Chagas disease awareness.

ANIMALS

12 client-owned dogs; 83 respondents from a veterinary cardiology listserv.

PROCEDURES

A retrospective, multicenter medical records review to identify dogs diagnosed with American trypanosomiasis between December 2010 and December 2020. An anonymous online survey was conducted August 9 to 22, 2022.

RESULTS

Diagnosis was made using indirect fluorescent antibody titer (n = 9), quantitative PCR assay (1), or postmortem histopathology (2). Time spent in Texas was < 1 year (n = 7) or 2 to 8 years (5). Time in nonendemic areas prior to diagnosis was < 1 year (n = 10) and > 3 years (2). Eleven had cardiac abnormalities. Of the 12 dogs, 5 had died unexpectedly (range, 1 to 108 days after diagnosis), 4 were still alive at last follow-up (range, 60 to 369 days after diagnosis), 2 were euthanized because of heart disease (1 and 98 days after diagnosis), and 1 was lost to follow-up. Survey results were obtained from 83 cardiologists in North America, of which the self-reported knowledge about Chagas disease was limited in 49% (41/83) and 69% (57/83) expressed interest in learning resources.

CLINICAL RELEVANCE

Results highlight the potential for encountering dogs with T cruzi infection in nonendemic areas and need for raising awareness about Chagas disease in North America.

Introduction

Chagas disease (American trypanosomiasis) results from infection by the protozoal organism Trypanosoma cruzi. Transmission occurs via a triatomine insect vector (family Reduviidae, known as the “kissing bug”), which is endemic to Latin America and certain regions of the US.13 Triatomines feed upon blood from a number of hosts including humans and wild and domestic mammals.1 Primary transmission occurs through the vector-fecal route, in which the vector, while feeding, excretes T cruzi trypomastigotes contained in its feces onto the host that enter through mucous membranes or open skin.1 Oral transmission via ingestion of an infected vector is also a potential source of infection.4 In acute infections, trypomastigotes invade cells near the site of inoculation, where they differentiate into intracellular amastigotes within host tissues including the heart, forming pseudocysts. The amastigotes multiply by binary fission and differentiate into trypomastigotes and then are released into the circulation as bloodstream.2 The development of myocardial fibrosis occurs in the chronic stage at least 8 months following infection, based on experimentally infected dogs, and at this point, amastigotes are rarely identified.5,6 Thus, cardiac injury and related clinical signs can manifest in both acute and chronic disease stages.2,57 Dogs with positive serology tests can develop Chagas cardiomyopathy, and some remain subclinical.5 Of the estimated 8 million infected people, approximately 20% to 30% develop Chagas cardiomyopathy.8 The number of infected dogs that develop Chagas cardiomyopathy remains unknown but could be similar.1,9 No effective vaccine or antiparasitic prophylaxis exists to prevent infection. Therefore, efforts to prevent Chagas disease rely on raising awareness of exposure and insect vector control.1,10

As travel and interstate companion animal transport programs have grown over the past decade, these changes could increase certain animal infectious diseases in nonendemic areas, particularly where veterinarians might be unaware of potential exposure.11 Additionally, insect vectors of disease have increased in nonendemic areas of the US.1,12 While insect vectors have been reported in northern states, for the purpose of this study endemic areas were defined as those with high triatomine insect density and established infected vector populations, in which a robust enzootic cycle of local transmission occurs among dogs.13

The objectives of this study were to describe the travel history, clinical presentation, and outcome in dogs translocated from Texas and diagnosed with T cruzi infection in nonendemic areas and to survey veterinary cardiologists in North America for Chagas disease awareness.

Materials and Methods

Case selection

We reviewed medical records for client-owned dogs diagnosed with T cruzi infection at 9 veterinary hospitals located in nonendemic areas in the US between December 1, 2010, and December 1, 2020. The inclusion criteria for identified cases included location in a nonendemic area of the US at the time of T cruzi diagnosis and previous time spent in an endemic area in Texas, available medical records to review, and evidence of T cruzi infection based on indirect fluorescent antibody (IFA) immunoglobulin G antibody titer for T cruzi > 1:20 performed at the Texas A&M Veterinary Medical Diagnostic Laboratory, real-time quantitative PCR assay using the 122/123 primers for Tc kinetoplast DNA,14 or histopathology postmortem findings.

Medical records review

Baseline data included breed, age, date of birth, sex, neuter status, body weight, location and meteorologic season at the time of diagnosis, method of T cruzi infection diagnosis from those listed in the inclusion criteria, travel history, history of previous congenital or acquired heart disease, presenting complaint, murmur characteristics, and the presence and type of arrhythmia from the date of the visit T cruzi diagnosis was confirmed. Season was defined as winter for December, January, and February; spring for March, April, and May; summer for June, July, and August; and fall for September, October, and November.

Recorded ECG data included date the ECG was performed, average heart rate, and rhythm diagnosis. Supraventricular arrhythmias were further categorized as supraventricular premature complexes, supraventricular tachycardia, or atrial fibrillation. Atrioventricular block (AVB) was classified as first-, second-, or third-degree AVB. Ventricular arrhythmias were assigned a modified Lown score as follows: 1 = single ventricular premature complexes, 2 = ventricular bigeminy or trigeminy, 3 = accelerated idioventricular rhythm, 4 = ventricular couplets or triplets, and 5 = ventricular tachycardia, R-on-T phenomenon, or both.1517 When available, 24-hour Holter monitor data were recorded and graded similarly to the ECG. Echocardiographic data obtained by board-certified cardiologists or supervised cardiology residents included left ventricular internal dimensions at end-diastole (LVIDd) and end-systole (LVIDs) from M-mode measurements normalized to body weight (LVIDdN and LVIDsN). Left ventricular enlargement was diagnosed when LV dimensions were outside of the 95% CI using the exponents LVIDdN cm/kg0.294 and LVIDsN cm/kg0.315 (LVIDdN > 1.85 or LVIDsN > 1.26).18 Left ventricular fractional shortening was calculated from M-mode measurements, and values < 20% were considered to represent reduced systolic function for the purposes of this study.19 The left atrium-to-aorta dimension ratio was calculated from 2-D measurements of the left atrium and aorta obtained in right parasternal short axis view, and a left atrium-to-aorta dimension ratio > 1.57 defined left atrial enlargement.20 Assessment of right ventricular chamber size was made by subjective comparison with left ventricular dimensions from the right parasternal, long-axis, 4-chamber view and graded as normal (≤ 35% of left ventricular size), mildly dilated (35% to 50%), moderately dilated (50% to 100%), or severely dilated (> 100%).21 Subjective assessment of right atrial size was made using the same echocardiographic view comparing the left and right atrium and graded as normal (< 110% of left atrial size), mildly dilated (110% to 150%), moderately dilated (150% to 200%), and severely dilated (> 200%).22 Additional data collected from medical records when available were test results for other potential indicators of cardiac damage or causes for cardiomyopathy including cardiac troponin I concentration, taurine concentration, and results of any other infectious disease tests. Treatment at the time of diagnosis was recorded.

Outcome was categorized as alive, deceased, or euthanized. For deceased animals, medical records were reviewed and, when possible, owners were contacted to determine cause of death or reason for euthanasia and date euthanized. Survival time from diagnosis to death or last follow-up was recorded.

Survey to assess awareness and knowledge of Chagas disease

We created an online survey (Supplementary Appendix S1) using a commercial survey software platform (Alchemer version 2022.11.16.00; Alchemer LLC), that was distributed to members of a global veterinary cardiology listserv, via an email invitation containing a link to the survey. Participation in the survey was voluntary and anonymous. An initial email with the survey link was sent via the listserv on August 9, 2022, a reminder was sent 1 week later, and the survey was closed on August 22, 2022. The survey consisted of 28 possible questions. Respondents were not required to answer all of the questions. Questions identified respondents’ demographics including area of practice (obtained via zip code) and their history of testing for or diagnosing cases of Chagas disease. Respondents then answered a set of 10 questions examining general knowledge of Chagas disease and grading the relative frequency that respondents considered Chagas disease as a differential diagnosis in dogs presenting with specific clinical abnormalities. A final question asked whether respondents were interested in more resources about Chagas disease. The survey was submitted to the Texas A&M University Institutional Review Board and was classified as exempt.

Statistical analysis

Descriptive statistics were calculated and reported as mean ± SD or median and IQR. Frequency distributions were reported as numbers and percentages. All analyses were performed with standard software (Excel version 16.67; Microsoft Corp).

Results

Patient population

During the time period, these veterinary hospitals had examined and treated an infected dog, had a dog or dogs suspected of Chagas disease and sought information from one of the study investigators (ABS or SAH), or had reported cases with T cruzi infection at an educational forum. One of these dogs was summarized in a group of 64 dogs with myocarditis,23 but because specific details for this dog including clinical presentation, outcome, and recent relocation from Texas to a nonendemic area were not described, the dog was included in the present study.

Twelve dogs met the inclusion criteria, and 10 seropositive dogs were excluded because case records were not available for review (1 dog in the Northeast and 9 dogs at a kennel in the Midwest). The 12 included dogs were reported as mixed breed (n = 5) and 1 each of Shetland Sheepdog, Labrador Retriever, Golden Retriever, Belgian Malinois, Chihuahua, Border Collie, and Australian Shepherd. Body weight ranged from 4.5 to 44 kg (mean ± SD, 18.5 ± 12.9 kg). Median age was 1.8 years (IQR, 0.4 to 3.8 years). Seven dogs were male (6 neutered) and 5 were female (2 spayed).

At the time of T cruzi infection, dogs were diagnosed in Southfield, Michigan (n = 3); New York City, New York (2); and 1 each in Castle Pines, Colorado; East Lansing, Michigan; Tinton Falls, New Jersey; Raleigh, North Carolina; Columbus, Ohio; Pullman, Washington; and Madison, Wisconsin. All dogs had lived in Texas prior to transport. Time spent in Texas was < 1 year (n = 7) or 2 to 8 years (5). Time in nonendemic areas prior to diagnosis was < 1 year (n = 10) and > 3 years (2). Seven dogs were transported from Texas to an animal rescue organization as part of a shelter rescue exchange program. One dog was adopted from a Texas-based animal rescue and subsequently transported after adoption. One dog was adopted from a breeder in Texas and transported to a nonendemic area after purchase. Two dogs were acquired by their current owners in Texas, who later relocated to the northeastern US. Meteorologic season at the time of diagnosis was winter (n = 4), spring (2), summer (2), and fall (4). None had previous history of congenital or acquired heart disease.

Clinical presentation

Clinical signs reported at presentation included respiratory abnormalities (ie, cough, tachypnea, dyspnea; n = 4), collapse (3), abdominal distension (3), exercise intolerance (1), and lethargy (1). One dog was presented for evaluation because a littermate had recently tested positive for T cruzi. On hospital admission, arrhythmias were detected in 8 dogs, a soft left apical systolic heart murmur in 1 dog, and muffled heart sounds attributed to pleural effusion in 1 dog. Six dogs were diagnosed with effusion (peritoneal only, n = 1; pleural only, 1; or both, 4).

Cardiac diagnostics

Electrocardiography was obtained with a standard 6-lead ECG recording in 9 of 11 dogs, simultaneous ECG during echocardiographic examination (n = 1), or continuous telemetry (1). Recorded arrhythmias included ventricular tachycardia in 7 of 11 dogs, single ventricular premature complexes (2), ventricular couplets (1), and accelerated idioventricular rhythm (1). The modified Lown score ranged from 0 to 5 (median, 5; IQR, 1 to 5). Three dogs also had supraventricular arrhythmias (supraventricular premature complexes and paroxysmal supraventricular tachycardia). Two dogs had third-degree atrioventricular block requiring emergency pacemaker placement, as well as ventricular ectopy (modified Lown scores 4 and 5). All 3 dogs with a 24-hour Holter monitor recording had ventricular arrhythmias (modified Lown scores 3, 4, and 5); 1 dog also had 901 sinus pauses, with the longest R-R interval lasting 6.9 seconds.

Ten dogs had an echocardiographic examination, and pertinent variables are summarized (Table 1). Ventricular enlargement was documented in the left ventricle (n = 5), right ventricle (5), or both (3). Atrial enlargement was documented in the left atrium (n = 3), right atrium (5), or both (3).

Table 1

Select echocardiographic variables and serum cardiac troponin I concentration for dogs with Trypanosoma cruzi infection diagnosed in nonendemic areas of North America.

Variable No. of dogs Mean ± SD or median (IQR)
LVIDd (cm) 10 4.43 (3.33–5.96)
LVIDdN 10 1.68 ± 0.40
LVIDdN > 1.85 3 NA
LVIDs (cm) 10 3.26 (2.36–5.29)
LVIDsN 10 1.26 ± 0.36
LVIDsN > 1.26 5 NA
FS (%) 10 22 (1–33)
FS < 20% 4 NA
LA:Ao 8 1.47 ± 0.39
LA:Ao > 1.57 3 NA
RV enlargement 5 NA
 Mild, moderate, severe 2, 2, 1
RA enlargement 5 NA
 Mild, moderate, severe 2, 2, 1
Troponin I (ng/mL) 5 0.84 (0.6–6.1)

FS = Fractional shortening. LA:Ao = Left atrium-to-aorta ratio. LVIDd = Left ventricular internal dimension at end-diastole. LVIDdN = Left ventricular internal dimension at end-diastole normalized to body weight. LVIDs = Left ventricular internal dimension at end-systole. LVIDsN = Left ventricular internal dimension at end-systole normalized to body weight. NA = Not applicable. RA = Right atrium. RV = Right ventricle.

T cruzi diagnosis

Nine dogs were tested for Chagas disease in response to travel history, observation of cardiac arrhythmias, or a dilated cardiomyopathy phenotype. One was screened because a littermate that had recently died was positive for T cruzi. Nine were diagnosed with T cruzi infection using IFA with titers ranging from 1:80 to 1:1,280 (median, 1:640; IQR, 1:160 to 1:1,280). One was diagnosed with T cruzi infection by real-time quantitative PCR assay performed on a peripheral blood sample. Two were diagnosed postmortem based on histopathologic identification of T cruzi amastigotes in the myocardium. One dog that was diagnosed using IFA died, and postmortem evaluation identified pseudocysts of amastigotes within the cardiac muscle tissue.

Additional testing

Serum cardiac troponin I concentration was evaluated in 5 dogs using either ultrasensitive (n = 3) or standard (2) assays. All 5 dogs had elevated concentrations (high-sensitivity assay > 0.128 ng/mL; standard assay > 0.5 ng/mL; Table 1). Ancillary tests to investigate for potential underlying causes for myocardial dysfunction and evaluate for infectious disease were performed in 6 dogs. Whole blood taurine concentration evaluated in 2 dogs was 79 and 396 nmol/mL (normal > 200 nmol/mL); 1 dog subsequently received taurine supplementation. One of 4 dogs undergoing heartworm antigen testing was positive. Tick-borne disease testing was negative for 3 dogs in which it was performed. One dog was negative when tested for parvovirus.

Treatment

Treatments included pacemaker placement for 2 dogs with third-degree AVB and antiarrhythmic medications in 11 dogs (sotalol, n = 5; mexiletine, 2; lidocaine, 2; and amiodarone, 2). Six dogs received pimobendan, and 4 dogs with congestive heart failure also received furosemide.

Outcome

At the time of data collection (February 2021), 5 dogs had died unexpectedly (range, 1 to 108 days after initial diagnosis), 4 were still alive at last follow-up (range, 60 to 369 days after diagnosis), 2 were euthanized because of heart disease (1 and 98 days after diagnosis), and 1 was lost to follow-up. All 5 dogs that died unexpectedly had complex arrhythmias that included ventricular arrhythmias and also either supraventricular arrhythmias (n = 3) or third-degree AVB (2). Four of the 5 dogs that died unexpectedly had echocardiography performed that showed dilated cardiomyopathy phenotype, and 3 of the 5 dogs had congestive heart failure.

Survey results

Of the 784 listserv participants, 110 responded to the survey and 83 of 110 (75%) were board-certified cardiologists living or working in North America (77 US, and 6 Canada). Of the 83 cardiologists, 74 (89%) were working in nonendemic areas and 9 (11%) were working in endemic areas (Texas and Louisiana; Table 2). The self-described recorded level of knowledge about Chagas disease was considered limited for 41 of 83 (49%) respondents, all of whom were working in nonendemic areas. The respondents indicated that Chagas disease was taught in their veterinary school curriculum (57/83), was not taught (12/83), or they did not remember (14/83). Most respondents displayed knowledge about transmission of Chagas disease. Fifty-seven of 83 (69%) indicated interest in learning more about Chagas disease in dogs including 53 of the 74 (72%) working in nonendemic areas.

Table 2

Results for key variables reported between August 9 and August 22, 2022, by 83 board-certified veterinary cardiologists from North America in a voluntary and anonymous online survey designed to gather information about respondents’ general knowledge of T cruzi and Chagas disease.

Variable All participants Nonendemic Endemic
Practice type (N) 83 74 9
 Private practice 60 (72%) 54 (73%) 6 (67%)
 Academia 24 (29%) 20 (27%) 4 (44%)
 Consultant, including telemedicine 8 (10%) 7 (9%) 1 (11%)
 Retired 1 (1%) 0 (0%) 1 (1%)
Duration of cardiology practice (N) 71 63 8
 < 5 y 13 (18%) 11 (17%) 2 (25%)
 5–10 y 25 (35%) 23 (36%) 2 (25%)
 11–20 y 26 (37%) 23 (36%) 3 (38%)
 > 20 y 7 (10%) 6 (11%) 1 (13%)
How would you describe your level of knowledge about Chagas disease (T cruzi infection)? (N) 83 74 9
 Excellent 7 (8%) 2 (3%) 5 (56%)
 Good 35 (42%) 31 (42%) 4 (44%)
 Limited 41 (49%) 41 (55%) 0 (0%)
T cruzi is spread by which of the following? (N) 82 73 9
 Reduviid bug 71 (87%) 63 (86%) 8 (89%)
 Tsetse fly 8 (10%) 8 (11%) 0 (0%)
 Sand fly 6 (7%) 6 (8%) 0 (0%)
 Biting fly 3 (4%) 2 (3%) 1 (11%)
 Mosquito 1 (1%) 1 (1%) 0 (0%)
 Person-to-person contact 1 (1%) 1 (1%) 0 (0%)
 I don’t know 1 (1%) 1 (1%) 0 (0%)
Which do you consider to be the correct statement regarding T cruzi and Chagas disease? (N) 82 73 9
 T cruzi is present across the southern US and Central and South America. 73 (89%) 64 (88%) 9 (100%)
 T cruzi is only present in isolated endemic regions of southern Texas and Louisiana. 9 (11%) 9 (12%) 0 (0%)
What is the most common form of transmission of T cruzi in dogs? (N) 82 73 9
 Contact with vector fecal material or ingestion of vector 44 (54%) 37 (51%) 7 (78%)
 Bite from vector 38 (46%) 36 (50%) 2 (22%)
Which of the following ECG findings is most common in chronic Chagas disease in dogs? (N) 82 72 9
 Ventricular arrhythmias 58 (71%) 49 (68%) 9 (100%)
 Second- or third-degree AV block 19 (23%) 19 (26%) 0 (0%)
 Bundle branch block 1 (1%) 1 (1%) 0 (0%)
 Sinus node dysfunction 1 (1%) 1 (1%) 0 (0%)
 I don’t know 3 (4%) 3 (4%) 0 (0%)

AV = Atrioventricular. N = Number of respondents for each question.

Fifty-six of 74 (76%) cardiologists working in nonendemic areas indicated the vector for T cruzi is not found in the region where they work or worked if retired or where their clients reside if working as a telemedicine consultant, 16 of 74 (22%) indicated the vector is found in the region they work or their clients reside, and 2 of 74 (3%) did not know. Also for those working in nonendemic areas, 35 of the 60 (58%) that responded indicated they occasionally interpret diagnostic tests for dogs that live in an area outside of where they practice, 14 (23%) were likely to interpret tests for dogs that live in an area outside of where they practice, and 11 (18%) never do. Forty-three of 65 (66%) respondents indicated they had tested dogs for T cruzi and 4 (6%) had tested cats, while 17 (26%) had never tested an animal and 1 (2%) did not remember. Thirty-four of 58 (59%) respondents indicated that they had tested < 10 dogs for T cruzi in the last 10 years, 3 (5%) had tested 11 to 20 dogs, 5 (9%) had tested > 30 dogs, and 16 (28%) had never tested a dog. Thirty-three of 72 (46%) that responded felt comfortable recognizing cardiac clinical signs of Chagas disease in dogs, and 65 of 72 (90%) were more likely to include it as a differential diagnosis in a dog that traveled to an endemic area or was transported to their area from an endemic area and was found to have ventricular arrhythmias, AV block, or dilated cardiomyopathy (Supplementary Table S1).

Discussion

Results of the present study illustrated the value of a comprehensive medical and travel history, including questions related to pet origin and travel, and consideration of Chagas disease in a list of differential diagnoses. In this study, T cruzi infection was diagnosed in dogs transported from endemic to nonendemic areas and antemortem T cruzi testing was performed due to the presence of cardiac abnormalities and a travel history involving Texas.

Most dogs in this study were diagnosed on the basis of a positive serologic test, which indicates previous T cruzi infection but does not necessarily confirm T cruzi is the source of the clinical abnormalities. Elevated troponin concentration supported the presence of myocardial damage, and additional diagnostic tests could help identify other potential causes of myocardial damage or dysfunction including taurine deficiency or myocarditis from other infectious diseases. The IFA for T cruzi is the most readily available test and is an indicator of exposure to what is often thought to be a lifelong disease. It can be negative in acute infection, and titer values have not been correlated to severity of disease. Acute infections occur approximately 21 days postinfection in experimentally infected dogs.5,6 The PCR test, predominately available in research laboratories, can detect parasite in blood or tissue and is more likely to be positive when there are circulating parasites in the acute stage of the disease or for direct testing of infected tissues.24 Four dogs were presented within 3 weeks of moving to a nonendemic area during the months of August and September, a time frame consistent with the active period of the insect vectors.25 Although stage of infection can be difficult to determine in naturally infected dogs, more recent infection was considered possible in 1 dog that had a positive blood PCR test and was euthanized for refractory ventricular arrhythmias and 2 dogs that died unexpectedly at 8 weeks old and were diagnosed with T cruzi on the basis of presence of amastigotes on histopathology.

For dogs in this study, arrhythmias and cardiac remodeling were consistent with those reported with Chagas cardiomyopathy including the predominate finding of ventricular arrhythmias and combinations of arrhythmias.2628,30 In humans with Chagas cardiomyopathy, arrhythmias correlated to disease severity and outcome including risk of sudden death.2 While cardiac arrhythmias can be the primary manifestation of Chagas disease in humans and dogs, Chagas cardiomyopathy is also characterized by myocardial dysfunction and congestive heart failure in the acute stage of the disease, in young dogs < 1 year of age, and in end-stage chronic infections.5,6,29 In humans and dogs, remodeling of the right ventricle serves as a marker of overall severity of cardiac disease and has been associated with a worse prognosis.26,30 While research efforts continue to work to identify effective prophylaxis and antiparasitic treatment for T cruzi infection in dogs, management is predominately symptomatic for cardiac disease.

Most dogs in this study were translocated from Texas as part of animal rescue or shelter transport programs, highlighting the potential impact of interstate companion animal transport on the increased identification of infectious disease in atypical areas. Over the past decade, interest in companion animal transport programs has grown considerably in North America in an effort to improve outcomes for dogs in shelters.11 A Colorado news report published in 2018 suggested that nearly 30,000 dogs were imported into the state in a single year, primarily from the southern US.31 Rescue organizations transported dogs interstate from overcrowded areas containing high numbers of stray animals into areas where groups believe dogs have a better chance of being adopted.11 These organizations also provided important rescue and relocation services during severe weather emergencies like hurricanes and floods, such as what was seen with Hurricane Katrina in 2005.31 The potential risk of transmitting infectious disease posed by transported dogs is one of increasing attention. For example, the prevalence of canine heartworm disease cases in Colorado increased between 2013 and 2017, correlating with the import of over 114,000 dogs into the state by animal shelters and rescue organizations during the same years.31 Without the knowledge that a dog originated from, traveled to, or lived in an endemic area, infectious diseases including T cruzi could be easily overlooked. Thus, it is possible that T cruzi infection in dogs is under-reported in nonendemic areas of the US. Collaboration between transport programs and destination organizations could facilitate effective partnership through information sharing, record keeping, regulatory guidelines, and transport methods.32 To raise awareness, exporting organizations could disclose disease risks particular to each geographic region and any activities that might enhance the animal’s risk of exposure.32

Dogs in this study were translocated from areas of Texas with high prevalence of triatomine insect vectors.3 Kissing bugs infected with T cruzi are found in increasingly more states in the US.33,34 While infected triatomine vectors have been well-documented in Texas and Louisiana,3,35 they have also been identified in the states of Arizona, California, Nevada, Utah, Colorado, New Mexico, Kansas, Oklahoma, Arkansas, Missouri, Tennessee, Illinois, Indiana, Ohio, Kentucky, Georgia, Alabama, Florida, North and South Carolina, Virginia, Maryland, Pennsylvania, and New Jersey, with variable incidence of infection when reported.12,3639 Importantly, insect distribution can change with time, and when studied in humans, insect bites have not always been associated with transmission of disease.10,12 Nationwide exposure has been documented in government working dogs, including dogs in northern states and nonendemic areas where triatomine insects are not found, with infections speculated to have occurred when dogs were training before deployment in Texas and other areas of the south where vectors are found.40

A limited knowledge and awareness of T cruzi infection in human medicine has been a key challenge in diagnosing Chagas disease, and there is increasing interest to improve education and awareness in the medical community.4143 Our findings suggest that history of transport from an endemic area in a dog with cardiac abnormalities increased the likelihood that a veterinary cardiologist would consider testing for T cruzi; however self-reported overall knowledge of the topic was limited for those working in nonendemic areas. Approximately 30% of veterinary cardiologists either did not remember being taught or reported that they were not taught about Chagas disease in school, and while most did not think the vector occurred in their area and only rarely tested dogs for Chagas disease, many do interpret diagnostic tests from dogs in other areas. This is an important point as dogs are increasingly transported across state lines and insect vector distribution can change. Given these factors and the survey results, the authors believe there is a need for improved awareness and resources for Chagas disease in the veterinary community.

This study was retrospective, and therefore the accuracy and completeness of the case data collected is dependent upon the information available in the medical record. The retrospective design also led to inconsistencies in echocardiographic measurements, diagnostic approaches for infectious disease testing including T cruzi, and the type of cardiac troponin I assay used. This study was limited by a small sample size restricting our ability to perform statistical analysis to evaluate patient variables and association with outcome. The cases presented here are known infected dogs with clinical disease that presented primarily to cardiologists and thus do not necessarily reflect the larger population of untested, apparently healthy dogs. Triatomine insect vectors have been reported in some of the states in our study, namely Colorado, New Jersey, North Carolina, and Ohio; therefore, it is possible that infection was acquired locally. With the history of living in an endemic area within weeks of diagnosis in some cases, local infection was considered less likely but remains possible. The survey results represent a focused sample from a specialty group listserv and do not necessarily represent the greater population of veterinarians. Nevertheless, findings suggest that development of Chagas-related educational resources could improve awareness and recognition of Chagas disease in dogs, particularly in nonendemic areas.

In summary, considering the growing impact of interstate transport programs, results of this study reinforce the value of a comprehensive medical and travel history. Identification of infectious diseases such as Chagas disease in atypical areas should be more routinely considered, especially when travel history is combined with arrhythmias and other cardiac abnormalities. Further, the need for increased improved awareness and more resources for Chagas disease in the veterinary community may merit these considerations in academic curricula.

Supplementary Materials

Supplementary materials are posted online at the journal website: avmajournals.avma.org

Acknowledgments

No external funding was used in this study. The authors declare that there were no conflicts of interest.

Presented as a research abstract at the 2021 American College of Veterinary Internal Medicine Virtual Forum.

The authors thank the Veterinary Information Network for facilitating survey distribution.

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