Research paperPrevalence of Trypanosoma cruzi infection and associated histologic findings in domestic cats (Felis catus)
Introduction
Trypanosoma cruzi is a zoonotic protozoal parasite and etiologic agent of Chagas disease, a potentially debilitating and deadly cardiac disease of humans, dogs, and other mammals. The parasite infects approximately 8 million people in the Americas including an estimated 300,000 in the United States (Bern and Montgomery, 2009; Montgomery et al., 2014). Transmission occurs through contact with infectious feces of the bloodsucking triatomine insect or consumption of these insects, commonly known as kissing bugs. Other forms of transmission include vertical transmission in utero, blood transfusion, organ transplant, and through ingestion of contaminated foods (Montgomery et al., 2014). Trypanosoma cruzi is comprised of six lineages (Zingales et al., 2009) known as discrete typing units (DTU), T. cruzi I-VI (TcI-TcVI), and an additional bat-exclusive lineage known as T. cruzi bat (TcBat) (Pinto et al., 2012). Because the different DTUs may have different ecological, epidemiological, and clinical associations (Zingales et al., 2014), tracking their distribution in nature is important for a more complete understanding of disease ecology. In humans and dogs, initial infection may cause acute nonspecific disease that is typically followed by an asymptomatic indeterminate phase. Approximately 30% of infected people develop chronic Chagas disease, characterized by various cardiac or, less commonly, gastrointestinal or neurological complications (Montgomery et al., 2014). Identifying potential reservoir and sentinel species in peridomestic environments is important to fully understand the transmission dynamics of T. cruzi and protect human health.
The veterinary health burden of Chagas disease in the United States is largely unknown, but infected wild and domestic mammals have been described across the endemic range of triatomines. The wild hosts of T. cruzi in nature across the southern United States are diverse, with raccoons (Procyon lotor), opossums (Didelphis virginiana), and woodrats (Neotoma spp.) among the most commonly studied and infected wild species (Hodo and Hamer, 2017). Among domestic animals, canine Chagas disease has been described in experimental animal models (Andrade et al., 1997) and epidemiological studies (Meyers et al., 2019). In Texas, some shelter dogs show a seroprevalence of 8.8 %–18.1 % while some multi-dog kennels with vector infestations show a seroprevalence in excess of 55% of dogs (Curtis-Robles et al., 2017a; Hodo et al., 2019; Tenney et al., 2014). The prevalence of canine infection appears highly variable across populations and diagnostic methods used. While some infections may remain asymptomatic, acute and chronic heart disease has been attributed to T. cruzi infection (Vitt et al., 2016). Dogs of the southern United States may serve as sentinels of human Chagas disease risk in the same regions, yet far less is known about the involvement of other domestic animals like cats in Chagas disease ecology in the southern United States.
Even though cats were the first domestic animal host identified by Carlos Chagas in 1909 (Lewinsohn, 1981), they have been relatively neglected in the subsequent study of T. cruzi transmission and disease. Domesticated felids are described as potential household reservoirs of T. cruzi and key sources of infection for triatomines in peridomestic environments aiding in domestic transmission (Gürtler et al., 2007, 1993). In Latin America, T. cruzi has been documented in domestic cats in both rural (Gürtler et al., 2007; Mott et al., 1978) and urban (Eloy and Lucheis, 2012; Jiménez-Coello et al., 2012) environments. Natural infection with T. cruzi is reported in a small number of wild felids, including ocelot (Leopardus pardalis) in Brazil (Rocha et al., 2013) and bobcat (Lynx rufus) in the United States (Curtis-Robles et al., 2016). In the United States, feral and free roaming domestic cats pose threats to wildlife and human health through predation of animals (Loyd et al., 2013) and spreading zoootic pathogens to humans (Case et al., 2006), yet the epidemiology of T. cruzi in domestic cats and the degree to which they serve as sentinels of human disease risk is largely unknown. Further, the disease consequences of T. cruzi in cats have not been explored. The objectives of this study were to (i) quantify domestic cat infection with T. cruzi using serologic and molecular approaches in a Chagas-endemic region of the southern United States and (ii) evaluate cardiac pathology in naturally infected versus uninfected cats. Knowledge of the role that cats may play in the ecology and epidemiology of Chagas disease, and the extent to which they are clinically impacted by T. cruzi infections, could provide new information for veterinary and public health interventions.
Section snippets
Study site
The Lower Rio Grande Valley (RGV) of Texas is an area of the United States-Mexico border with documented T. cruzi cases among humans and dogs, and is located within an endemic region of at least four triatomine species (Beard et al., 2003; Curtis-Robles et al., 2018b, 2017b). An animal shelter in the RGV intakes approximately 33,000 animals per year, including an annual average of 9,000 domestic cats. Cats are admitted to the shelter predominately by drop off by animal control agencies across
Demographic results
A total of 167 adult cats were sampled of which 87 were female (52.1%) and 80 were male (47.9%). The majority of the cats were classified as DSH (93.4%), while the remaining were classified as “other type” (6.6%) which included domestic medium hair (n = 6), domestic long hair (n = 4), and American Shorthair (n = 1). Most of the cats were sampled in the winter (71.9%), with the rest of the samples collected in the spring (18.6%) and the summer (9.6%). Cats sampled ranged in size: small (n = 6;
Discussion
In this work, for the first time Chagas-seropositive domestic cats (11.4%) were detected in the United States in a Chagas-endemic region along the Texas-Mexico border. Through detailed molecular investigations of various tissues, parasite DNA was documented in five tissue types (heart, esophagus, sciatic nerve, biceps femoris, mesentery) and four comprised of parasite DTU TcI. Through histopathologic examination, mild to moderate inflammation was seen in hearts of 42.1% (8/19) of the examined
Conclusion
We show that stray cats are infected with T. cruzi, possibly associated with mild to moderate pathology in multiple organs, in south Texas where ongoing autochthonous human and canine transmission occurs. Recent bloodmeal analysis studies of triatomines from Texas and other southern states show the presence of Felis catus bloodmeals (Gorchakov et al., 2016; Kjos et al., 2013; Waleckx et al., 2014), demonstrating vector-host contact in nature. Future research will determine the impact of T. cruzi
Declaration of Competing Interest
Postmortem blood and tissue samples were collected from animals euthanized by the shelter as part of the shelter’s own program. Animals were not euthanized specifically for the purpose of this research. A letter of exemption from ethical approval was issued by the Texas A&M University Institutional Animal Use and Care Committee on December 16, 2016.
Acknowledgement
We thank Bailee Ethridge and Dr. Erin Edwards for assistance in the field and with tissue prepartion. We thank Carlos Rodriguez for his help with serological testing. We thank shelter veterinary medical personnel and staff for assistance. The shelter staff and veterinary medical personnel gained no financial benefits for their participation. The Texas AgriLife/Texas Veterinary Medical Diagnostic Laboratory Seed Grant program and the AgriLife Insect Vector grant provided financial support. The
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2022, Veterinary Clinics of North America - Small Animal PracticeCitation Excerpt :In South Texas, 7.3% to 11.4% of shelter cats were seroreactive and 1.8% to 24.6% tested positive using PCR. Some infected cats had cardiac inflammation.59 Additionally, shelter cats in Louisiana were infected with diverse T. cruzi strains.60
Phylogenetic diversity of two common Trypanosoma cruzi lineages in the Southwestern United States
2022, Infection, Genetics and EvolutionCitation Excerpt :These numbers are significant and emphasize the need for recognition among physicians and public health officials, as the parasite can be transmitted through blood transfusion and congenitally (Manne-Goehler et al., 2015; Parise et al., 2014; Verani et al., 2010). In addition, both infected triatomines and mammalian reservoirs of the parasite such as packrats, armadillos, raccoons, skunks, foxes, mice, opossums, dogs and captive nonhuman primates are plentiful in the USA, particularly in southern states (Aleman et al., 2017; Barnabe et al., 2001; Beard et al., 2003; Bern et al., 2011; Bern et al., 2019; Bradley et al., 2000; Curtis-Robles et al., 2018; Elmayan et al., 2019; Ghersi et al., 2020; Herrera et al., 2019; Hodo et al., 2018; Kjos et al., 2008; Meurs et al., 1998; Padilla et al., 2021; Pung et al., 1995; Rodriguez et al., 2021; Roellig et al., 2008; Shender et al., 2016; Vandermark et al., 2018; Zecca et al., 2020). Despite this, only a small (〈100), but increasing number of autochthonous vector-borne cases of T. cruzi transmission have been reported to date, all in the southern part of the country (Reviewed in (Bern et al., 2019; Lynn et al., 2020).
Trypanosomiasis
2022, Greene's Infectious Diseases of the Dog and Cat, Fifth EditionThe tissue specific tropism in Trypanosoma cruzi. Is it true?
2021, Acta TropicaCitation Excerpt :These findings seem to cast doubts on the existence of a tissue-preference during T. cruzi-infection in the mammal host, considering, as demonstrated here, that almost all the tissues sampled during the study were invaded early, and totally colonized after the 7th day PI, reaching the highest intensity on day 12th of the acute infection. Our results strongly support previous findings from several researchers who pointed out that from 12 days onwards T. cruzi-tissue invasion may reach all organs in different species of mammals, including the CNS, the heart, the skeletal muscle, esophagus, mesentery, exocrine and endocrine glands, adipose tissues and also those less vascularized anatomical structures (Watkins, 1966, Hanson & Robertson, 1974, Melo & Brener, 1978, Barbosa & Andrade, 1984, Lenzi et al, 1996, Lages-Silva et al., 2001, Morocoima et al., 2006, Herrera et al, 2007, Villalba-Aleman et al, 2019, Zecca et al, 2020). In summary, the qualitative analysis of tissue invasion during the acute infection suggests that the T. cruzi-strategy appears to be simple, considering the enormous advantages gained throughout its adaptation and coevolution with many species of mammal hosts.