Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 January 2021 | 13(1): 17521–17528
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.5907.13.1.17521-17528
#5907 | Received 25 March 2020 | Final
received 27 November 2020 | Finally accepted 18 January 2021
Histopathological findings of
infections caused by canine distemper virus, Trypanosoma cruzi,
and other parasites in two free-ranging White-nosed Coatis Nasua
narica (Carnivora: Procyonidae)
from Costa Rica
Jorge Rojas-Jiménez 1,
Juan A. Morales-Acuña 2, Milena Argüello-Sáenz 3, Silvia E. Acevedo-González
4, Michael J. Yabsley 5 & Andrea Urbina-Villalobos 6
1 Warnell
School of Forestry and Natural Resources, The University of Georgia, Athens,
Georgia 30602, USA / Costa Rica Wildlife Foundation, Barrio Escalante, 10101
San José, Costa Rica / Awá Science &
Conservation, 40101 San José, Costa Rica.
2 Departamento de Patología,
Escuela de Medicina Veterinaria,
Universidad Nacional de Costa Rica, Heredia, Costa Rica.
3 Laboratorio de Ecología
de Enfermedades y Una Salud,
Departamento de Etología,
Fauna Silvestre y Animales de Laboratorio,
Facultad de Medicina Veterinaria y Zootecnia,
Universidad Nacional Autónoma de México, Circuito Interior S/N, Ciudad Universitaria,
Coyoacán, 04520, Ciudad de México, Mexico / Awá Science & Conservation, 40101 San José, Costa Rica.
4 Laboratorio de Zoonosis, Escuela de Medicina Veterinaria, Universidad
Nacional de Costa Rica, Heredia, Costa Rica.
5 Warnell
School of Forestry and Natural Resources, The University of Georgia, Athens,
Georgia 30602, USA / Southeastern Cooperative
Wildlife Disease Study, Department of Population Health, College of Veterinary
Medicine, The University of Georgia, Athens, Georgia 30602, USA.
6 Laboratorio de Zoonosis, Escuela de Medicina Veterinaria, Universidad
Nacional de Costa Rica, Heredia, Costa Rica.
1 Jorge.Rojas@uga.edu
(corresponding author), 2 juan.alberto.morales.emv@gmail.com, 3
milenaarguellos@gmail.com,
4 silacegon@gmail.com, 5 myabsley@uga.edu,
6 andreaurbina3@gmail.com
Abstract: Canine distemper virus (CDV)
causes systemic infections and immunosuppression in carnivores, which
subsequently makes animals highly susceptible to opportunistic infections. Although Trypanosoma cruzi
infects procyonids, chagasic myocarditis in Coatis
has not been reported in Central America.
The aim of this study was to report the histopathological findings
caused by canine distemper virus, T. cruzi,
and other parasites in two free-ranging White-nosed Coatis Nasua
narica found dead in a national park on the
Pacific coast of Costa Rica. Heart,
lung, tongue, liver, brain and spleen samples were subjected to macroscopic and
microscopic examination. A mononuclear
meningoencephalitis associated with intra-nuclear eosinophilic inclusion bodies
consistent with canine distemper virus was observed in nervous tissue. Myocarditis and associated nests of
amastigotes of T. cruzi were observed
during microscopic examination in cardiac tissue, and in muscle from the tongue
of both animals. Molecular analysis confirmed T. cruzi
in formalin-fixed paraffin embedded cardiac tissues. The myocardial damage caused by the
opportunistic infection due to T. cruzi
in these individuals could be the result of a severe compromised immunological
status associated to the CDV infection, and subsequent opportunistic
polyparasitism described herein. To the
authors knowledge this is the first report of chagasic
myocarditis in free-ranging coatis from Central America.
Keywords: CDV, myocarditis, Nasua narica, PCR,
polyparasitism, Trypanosoma cruzi.
Editor: Carolyn L. Hodo, University of
Texas MD Anderson Cancer Center, Texas, USA. Date
of publication: 26 January 2021 (online & print)
Citation: Rojas-Jiménez, J., J.A. Morales-Acuña, M. Argüello-Sáenz, S.E.
Acevedo-González, M.J. Yabsley & A.
Urbina-Villalobos (2021). Histopathological findings of
infections caused by canine distemper virus, Trypanosoma cruzi,
and other parasites in two free-ranging White-nosed Coatis Nasua narica
(Carnivora: Procyonidae) from Costa Rica. Journal of Threatened Taxa 13(1): 17521–17528. https://doi.org/10.11609/jott.5907.13.1.17521-17528
Copyright: © Rojas-Jiménez et al. 2021. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: This
project was partially funded
by Project ID#0494-17 from the Diagnóstico de Micosis Veterinarias y de Enfermedades Zoonoóticas Parasitarias, Escuela de Medicina Veterinaria, Universidad Nacional de Costa
Rica, Heredia, Costa Rica.
Competing interests: The authors
declare no competing interests.
Ethical approval: The procedure was performed under
the approval of the National Environment Ministry (MINAE), and the National
System of Conservation Areas (SINAC), Área de Conservación Pacífico Central
(ACOPAC) (No permits found due to poor records). No animals were specifically harmed for the
purpose of this study but were part of a mortality investigation; in addition,
the necropsy protocols were performed at the Pathology Service of the School of
Veterinary Medicine of the National University of Heredia, Costa Rica,
(EMV-UNA), within the cases identification ND 107-2010 (female) and ND 112-2010
(male), respectively.
Acknowledgements: We thank Dr.
Fernando Riera, (DVM, Costa Ballena
Veterinary, Uvita, Puntarenas) for submitting the
individuals to the Pathology Service of the School of Veterinary Medicine of
the National University of Heredia, Costa Rica, (EMV-UNA) for evaluation.
In Latin America, Nasua spp. host for several zoonotic
parasites including Trypanosoma cruzi, and
viruses such as canine distemper virus (Chinchilla 1966; Herrera 2010; Santoro
et al. 2016; Duarte Moraes et al. 2017; Michelazzo et al. 2020).
In Costa Rica, the White-nosed Coati Nasua
narica is a procyonid that is widely distributed
in protected areas and is a frequent inhabitant of semi-urban or peridomiciliary zones (Wainwright 2007; Cuarón
et al. 2016). An epidemic of sudden
death in coatis with previous neurological signs occurred in a conservation
area in the southern Pacific coast of Costa Rica in 2010. This report provides details on the
diagnostic investigation of two individuals.
In 2010, a troop of 15–20
White-nosed Coatis from the Bahia Ballena Marine
National Park (BBMNP) in Uvita, Dominical, Puntarenas
(9.157N, -83.746W) presented with neurological signs and incoordination
followed by sudden death. Due to
decomposition and limited logistics, only two adult coatis (one male and one
female) were collected and transported to a local small animal veterinary
clinic by local authorities from the National System of Conservation Areas,
Costa Rica (SINAC). In addition, the
outbreak occurred only once and no more events of this type have been reported
subsequently in the region (Dr. Fernando Riera pers. comm. January 2020). The veterinarian in charge submitted the carcasses
to the Pathology Service of the School of Veterinary Medicine of the National
University of Heredia, Costa Rica, (EMV-UNA) for necropsy and diagnostic
evaluation. Selected tissues from heart,
lung, tongue, liver, brain, and spleen were routinely processed, embedded in
paraffin, and 4–5 mm thick sections were stained with hematoxylin
and eosin (H & E), toluidine blue or Giemsa for light microscopy.
For detection of T. cruzi DNA, a conventional PCR using
formalin-fixed paraffin-embedded (FFPE) tissues was performed on selected
tissues from heart, lung, tongue, liver, brain and spleen. About 25mg sections were cut from each block
and placed in a 1.5ml sterile microcentrifuge tube. The microtome and blade were cleaned with
xylene between each block. The sections
were de-waxed by cutting off paraffin edges and then mixed with 500μl xylene
for eight minutes followed by washing with 95% ethanol and with 70% ethanol for
five minutes each. Pellets were dried at
80°C for eight minutes on a heat block.
As positive controls, FFPE cardiac tissue sections of mice
experimentally infected with T. cruzi
were used. The T. cruzi strain used in the mice experimentally
infected corresponded to T. cruzi I (TcI) and was isolated from a naturally infected dog from
Costa Rica (Mena-Marín et al. 2012).
FFPE cardiac tissue sections of healthy mice were used as negative
controls. Total DNA extraction from the
paraffin material was performed using a commercial kit (QIAmp
DNA Mini Kit ® QIAGEN). The primers used
for PCR were S35 (5’AAATAATGTACGGGTGGAGATGCATGA-3’) and S36
(5’-GGGTTCGATTGGGGTTGGTGT-3’) (Ferrer 2015).
This set of primers amplifies a 330bp fragment derived from the variable
region of T. cruzi minicircles (Ferrer
2015). Although this set of primers
amplifies the majority of strains of T. cruzi,
and it is considered specific to T. cruzi,
two fragments of Trypanosoma rangeli (300bp
and 450bp) can be also amplified with this set (Vallejo et al. 1999). This is, however, a non-pathogenic parasite
and it is not observed in mammalian tissue (Vallejo et al. 2015). PCR reaction conditions were carried out as
previously described with the S35–S36 set with some modifications (Barrera et
al. 2008). Briefly, PCR was carried out
using a DNA thermal cycler (Gene Amp PCR System. Perkin Elmer), the amplification
reaction was performed in a final volume of 20μl with 10μl of 2X Dream TaqTM PCR Master Mix (Thermo
Fisher ScientificTM, Whatman, MA), 4μl of
nuclease free water (Thermo Fisher ScientificTM Whatman, MA), 1.5μl of 99.99% DMSO,
2μl of sample DNA, 1μl of each of the primers at 10μM and 0.5μl of bovine serum
albumin (BSA) at a concentration of 20mg/ml, one cycle of initial denaturation
for 5min at 95oC followed by 35 cycles of denaturation for 20sec at
95oC, alignment for 30sec at 63oC, elongation for 30sec
at 72oC, and a final cycle of elongation for 10min at 72oC. The amplified DNA was visualized with 2%
agarose gel using a UV transilluminator.
At gross examination, both coatis
were in poor body condition, with dermatological lesions including alopecia,
exudative dermatitis, abscesses, scabs, and pustules. Other significant findings were
conjunctivitis and mass muscle atrophy of limbs. Both individuals had enlarged spleens. The female coati had several nematodes
compatible with Dirofilaria sp. in
the right ventricle and pulmonary artery (Image 1a). The lungs were congested, edematous,
had multifocal hemorrhages, and a 0.5cm hemorrhagic nodule with eosinophilic infiltrate associated
with the migration of immature trematodes compatible with Paragonimus
spp. and microfilariae were in the right diaphragmatic lobule. Small numbers of cestodes, acanthocephalans
and nematodes were found in the small intestine. In the male coati, the lungs were congested
and edematous.
Additionally, the male coati had a dilated esophagus
and small numbers of acanthocephalans and nematodes were present.
Histologic evaluation revealed a
mixed exudative dermatitis consistent with Dermatophilus
congolensis and unidentified mites in both
animals. In cardiac tissue of both
coatis, a mild mononuclear infiltrate with lymphocytes, plasma cells,
histiocytes, and few eosinophils were observed in both the myocardium and
pericardium, from mainly the left ventricle and the atria. In addition, myocardial muscle fibers were edematous and
exhibiting degeneration and necrosis.
The inflammation was associated with multifocal amastigote nests in
myocardial muscle fibers, and nematode larvae
morphologically similar to Dirofilaria spp.
(Images 1b, 1c, 1d). Moreover, cardiac
tissue from both animals was positive for the expected 330bp amplicon product
for Trypanosoma cruzi.
Both individuals had eosinophilic
infiltrates in the lungs associated with the migration of immature trematodes
compatible with Paragonimus sp. and
microfilariae compatible with Dirofilaria sp.
(Images 2a, 2b). In muscle tissue from
the tongue of both coatis, an infiltrate with lymphocytic cells, macrophages
and giant cells were observed in the muscle fibers. This inflammation was associated with
protozoal cysts consistent with Sarcocystis
sp. and with amastigote nests of T. cruzi
(Image 2c). A multifocal mild infiltrate
of neutrophils, eosinophils and macrophages was observed in the mucosa and
submucosa of the ileum and colon. This
inflammation was associated with acanthocephalans. In addition, unidentified adult nematodes
consistent with spirurids were detected in the
pancreatic ducts from both animals (Image 2d).
In nervous tissue of both animals, the medulla oblongata and pons were edematous and congested, with gliosis, satellite glial
cells, demyelination, and multifocal areas of encephalomalacia. Moreover, the meninges were edematous and congested, and a mild perivascular
mononuclear infiltrate with neuronal necrosis, and syncytial cells containing
intranuclear eosinophilic inclusions consistent with canine distemper virus
(CDV) were observed in the hippocampus (Images 3a, 3b). Also, unidentified microfilaria were found in
blood vessels of the cerebral cortex and nervous tissue.
White-nosed Coatis are widespread
in Central America and Mexico and occur in parts of the southwestern United
States. Their conservation status is
Least Concern (Cuarón et al. 2016) and they do not
have any protection in Costa Rica. They
are distributed throughout the country including the mangrove and the beach of
the BBMNP where this mortality event occurred (Wainwright 2007). This species is exposed to a great diversity
of pathogens due to its diverse diet, long life expectancy, ability to disperse
over long distances, and the use of both arboreal and terrestrial habits (de
Lima et al. 2015; Alves et al. 2016).
Moreover, living in social groups may increase the probability of
transmission of parasites and other pathogens (Hass & Valenzuela 2002).
The interaction between several
parasites and other infectious agents should be further investigated in order
to explain the immune response in coatis.
For example, the finding of mononuclear meningoencephalitis and
intranuclear eosinophilic inclusions as seen in CDV deserves more study. CDV is one of the most important infectious
agents of carnivores worldwide including procyonids (Deem et al. 2000). To date, the only published study on CDV in
Costa Rican wildlife was on wild cats in the Osa
Peninsula region which is located ~145km from the BBMNP (Avendaño
et al. 2016). There are only a few
previous published reports of CDV in coatis (Martinez-Gutierrez &
Ruiz-Saenz 2016), and some studies have failed to detect CDV antibodies in wild
or captive coatis (Furtado et al. 2016; Taques et al.
2018). The social nature of coatis
likely makes them particularly at risk as this virus can quickly spread among
different individuals belonging to the same troop, as has been reported in
raccoons (Hass & Valenzuela 2002; Kapil & Yeary
2011; Rentería-Solís et al. 2014; Dr.
Catao-Dias pers. comm. July 2019). In addition, due to the mass mortality event
we suggest that CDV was the primary cause of death, with polyparasitism likely
contributing to an impaired immune status (Origgi et
al. 2012; Kubiski et al. 2016). An initial differential diagnosis for CDV
considered by local authorities was rabies, which is present in the region (Hutter et al. 2016).
Compatible clinical signs, however, were not observed in the animals and
Negri bodies were not detected in nervous tissue. Other differential diagnoses such as feline
panleukopenia, toxoplasmosis and canine parvovirus were considered (Deem et al.
2000). Due to diagnostic limitations it
was not possible to definitively rule these out, but the inclusion bodies
observed were supportive of our diagnosis of CDV.
There have been numerous reports
of T. cruzi infecting several
species of coatis, including White-nosed Coatis in Costa Rica (Mehrkens et al. 2013), Mexico (Martínez-Hernández et al.
2016), and Honduras (Lainson 1965), and Ring-tailed Coati or Southern Coati N.
nasua in Brazil and Peru (e.g., Alves et al.
2016; Morales et al. 2017). Coatis use
of arboreal nests increases the risk of exposure to triatomine vectors, and
these nests may be shared among multiple members of the social group (de Lima
et al. 2015; Alves et al. 2016).
Generally, the prevalence of T. cruzi
can be high in coatis and they appear to have long-lasting parasitemias
(Alves et al. 2011). Also, the
attenuated pathogenicity of T. cruzi in
neotropical mammals could be explained by its long co-evolution with this
parasite (Schofield 2000). Moreover,
experimental infection of another procyonid (i.e., Procyon lotor) with a strain of T. cruzi
that normally does not infect that host led to severe clinical disease (hind
limb paralysis and labored breathing) and severe
myocarditis, suggesting that this corresponded to an acute phase of infection
in these raccoons (Roellig et al. 2009). Alternatively, as reported in dogs by Barr et
al. (1991) and also in raccoons by Curtis-Robles et al. (2016), the animals did
not present cardiac lesions. In the
latter, the authors mentioned that the high infection prevalence of T. cruzi detected in raccoons, could be explained since
these animals were able to host infections without serious chronic pathological
implications (i.e., no cardiac lesions observed) (Curtis-Robles et al.
2016). Nonetheless, more research is
needed to better understand the role of T. cruzi
in co-infections with other agents in wild hosts, both experimentally and in
wild conditions (Roellig et al. 2009; Curtis-Robles
et al. 2016). In our case study, the myocardial
damage caused by the opportunistic infection due to T. cruzi could be the result of a severe compromised
immunological status associated to the CDV infection, and subsequent
opportunistic polyparasitism described herein (Araujo Carreira
et al. 1996; Herrera 2010; Origgi et al. 2012; Kubiski et al. 2016).
The exact mechanisms underlying CDV infections and circulation of the virus
among susceptible wild mesocarnivores, however, are
relatively unknown, that is, several authors suggested that this could be
related to CDV genotypes with different virulence and cell tropism (Origgi et
al. 2012; Rentería-Solís et al. 2014; Kubiski et al. 2016).
As for the
discrete typing unit (DTU), TcI is the most common in Central America, and has been
reported in coatis in Mexico, but unfortunately the DTU in these animals was
not determined (Herrera 2010; Rocha et al. 2013; Martínez-Hernández et al.
2016; Dorn et al. 2017). More studies
are necessary to elucidate if coatis may be competent reservoirs of T. cruzi and a source of infection for the triatomine
bugs in the region (Roellig et al. 2009; Curtis-Robles
et al. 2016).
Several other parasites were
detected in these two individuals and though the worms found in the heart of
the coatis were not saved so could not be identified, they were morphologically
similar to Dirofilaria sp. These parasites are likely Dirofilaria immitis
(i.e., canine heartworm), a parasite which is common in domestic dogs from
coastal areas in Costa Rica (Montenegro et al. 2017). Additionally, D. immitis
has been reported in Ring-tailed Coatis from Argentina and Brazil; however,
infections in Brazil were based on morphology of microfilaria alone, and the
parasites from Argentina were originally described as D. nasuae (now considered a synonym of D. immitis) (Vezzani et al. 2006; Duarte Moraes
et al. 2017). Thus, given the extreme rarity of
confirmed D. immitis infections in
procyonids, careful morphologic and molecular characterization of
heart-dwelling Dirofilaria species in coatis
is warranted. Also, human and animal
health authorities should draw attention to this parasite due to its potential
for zoonotic transmission.
Paragonimus spp. have been reported in
coatis previously (Calvopiña et al. 2014) and the
parasites we detected could be P. mexicanus
or P. caliensis, both of which have
been reported in freshwater crabs in the same province (Hernández-Chea et al. 2017).
Molecular and/or careful morphologic characterization are needed to
determine the species. Similarly, the Sarcosystis sp. in these coatis is unknown but could
be acquired from numerous carnivores or didelphid
species in the region, the latter of which have a wide distribution in Costa
Rica, including the Pacific coast (Wainwright 2007), and are known definitive
hosts of several Sarcocystis spp. (Dubey et
al. 2008). The unidentified spirurid nematodes in the pancreatic ducts may be related
to the Thelazioidea which contains several
interesting genera that inhabit the pancreatic ducts of non-human primates and
rodents (Trichospirura), skates and sharks (Pancreatonema), marine teleosts
(Johnstonmawsonia) and freshwater teleosts (Prosungulonema)
(Anderson et al. 2009). Finally, the
similarities in the histopathological findings in the two individuals included
in this study may reflect life histories that lead to similar contact rates
with vectors and parasites, since the animals apparently belonged to the same
troop (Curtis-Robles et al. 2016).
To our knowledge this is the
first report of chagasic myocarditis in free-ranging
coatis from Central America. In
addition, we recognize the diagnostic and logistic limitations of this report;
however, we strongly consider the histopathological findings relevant because
of the limited information on zoonotic infectious diseases that currently
exists in wildlife populations such as coatis, in Costa Rica. Therefore, these findings may help local
authorities to improve surveillance and conservation management strategies in
protected areas such as keeping a safe distance from wild animals and
discouraging supplemental feeding.
Furthermore, we encourage local researchers and local authorities to
carry out epidemiological surveys to assess the ecology of infectious diseases
on coatis, and to better understand the current health status of N. narica populations that frequent protected
areas and other regions of the country.
A multidisciplinary approach, including education of local residents,
park visitors and park rangers, is necessary to minimize cross-infections
between wildlife, domestic animals and humans.
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