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DOI: 10.7589/2017-01-017 Journal of Wildlife Diseases, 54(1), 2018, pp.

000–000
Ó Wildlife Disease Association 2018

TRYPANOSOMA CRUZI AND LEISHMANIA SP. INFECTION IN


WILDLIFE FROM URBAN RAINFOREST FRAGMENTS IN NORTHEAST
BRAZIL
Indira Trüeb,1 Ricardo D. Portela,2 Carlos R. Franke,1 Ianei O. Carneiro,1 Gilmar J. Ribeiro Jr.,3
Rodrigo P. Soares,4 and Stella Maria Barrouin-Melo1,5,6
1
Laboratório de Infectologia Veterinária, Hospital-Escola de Medicina Veterinária, Universidade Federal da Bahia,
Avenida Adhemar de Barros, 500, Salvador, Bahia, Brazil, 40170-110
2
Laboratório de Imunologia e Biologia Molecular, Instituto de Ciências da Saúde, Universidade Federal da Bahia,
Salvador, Bahia, Brazil, 40110-100
3
Laboratório de Patologia e Biologia Molecular, Centro de Pesquisas Gonçalo Moniz, Fundação Oswaldo Cruz,
Salvador, Bahia, Brazil, 40296-710
4
Centro de Pesquisas René Rachou, Fundação Oswaldo Cruz, Salvador, Avenida Augusto de Lima 1715, Belo
Horizonte, MG, Brazil, 30190-002
5
Departamento de Anatomia, Patologia e Clı́nicas, Escola de Medicina Veterinária e Zootecnia, Universidade Federal da
Bahia, Salvador, Bahia, Brazil, 40170-110
6
Corresponding author (email: barrouin@ufba.br)

ABSTRACT: Trypanosoma cruzi and Leishmania sp. are important protozoan parasites for humans and
animals in the Americas, causing Chagas disease and cutaneous or visceral leishmaniasis, respectively.
These vector-borne diseases affect permanent and transient populations in developing tropical
countries that exhibit favorable conditions for the perpetuation of the parasite cycle. Our objective was
to investigate the occurrence of infection with these parasites in wild animals from urban rainforest
fragments in the city of Salvador, the largest city in the northeast region of Brazil. Sixty-five wild animals
were captured, clinically examined, and sampled for parasite detection by PCR and culture. Ten
different mammalian genera were identified, being 58% (38/65) marsupials. The prevalence of T. cruzi
and Leishmania sp. infections was 13% and 43%, respectively. Both parasites were detected by PCR in
11% (7/65), three of which were also double infected as determined by culture. Among the 28 animals
found infected with at least one parasite (43%, 28/65), 68% (19/28) were marsupials, two specimens
were Callithrix sp. (7%), and one was Trinomys sp. (3%). Most infected animals (89%) had no clinical
signs of disease. We found that healthy free-living animals from urban rainforest fragments harbored
pathogenic trypanosomatids and should be included in epidemiology studies of diseases in big cities in
tropical countries, as these cities grow and engulf rainforest remnants.
Key words: Callithrix, Chagas disease, leishmaniasis, Trinomys, urban forests, wildlife infection.

INTRODUCTION reservoir adaptations to urban environments


(Souza et al. 2009). Enzootic infections in
With the expansion of urban centers and wildlife are a risk for public health, because
the use of natural areas for agriculture or after feeding in wild animals, vectors can
livestock breeding, native forest areas have easily reach urban humans (Dias-Lima and
been gradually fragmented, affecting ecosys- Sherlock 2000). Therefore, the monitoring of
tems (Grisotti 2010). Ecological disturbances infectious diseases in these animals, some of
create an imbalance in parasite-wildlife cycles, them endangered species, is important for
reaching humans in areas next to forest surveillance and control of emerging and
fragments (Epstein and Price 2009). In this reemerging diseases (McFarlane et al. 2012).
context, wild animals play an important role in Trypanosoma cruzi and Leishmania sp. are
the urban transmission of vector-borne zoo- parasites commonly found in developing
noses, maintaining parasite transmission cy- tropical countries, such as Brazil, in areas that
cles (de Almeida Curi et al. 2014). Life cycles nowadays include large cities as well as in
of Trypanosomatidae protozoa are examples areas favored by tourists. Invertebrate Triato-
of this process, because they share epidemi- minae and Phlebotominae vectors transmit T.
ological characteristics related to vector and cruzi and Leishmania sp., respectively, to
1
2 JOURNAL OF WILDLIFE DISEASES, VOL. 54, NO. 1, JANUARY 2018

FIGURE 1. Map of Salvador metropolitan region, Bahia State, Brazil (12858 0 13 0 0 S, 38830 0 45 0 0 W). Urban
rainforest fragments are shown in dark gray. Asterisks mark the four sites where wild animals were captured,
examined, and sampled for parasitological and molecular diagnosis of infection by Trypanosoma cruzi and
Leishmania sp. Clear areas represent the urbanized surface of the city, which has almost 3 million inhabitants.

humans and animals, causing Chagas disease population of 2,921,087 inhabitants, making it the
and cutaneous or visceral leishmaniasis, which third-largest Brazilian city (Instituto Brasileiro de
are among the greatest public health problems Geografia e Estatı́stica 2015). The studied areas
included Atlantic rainforest remnants that have
in the Americas (Thompson et al. 2010). undergone important anthropic influences, being
Because of the increasing anthropic action progressively reduced and isolated by the growth
on the environment, such vectors and wild of the city.
reservoirs are in close contact with perido- From January 2013 to December 2013, 20
mestic and urban regions, following the capture efforts were made in four urban rainforest
occupation of recently deforested areas by fragments, with five efforts in each of the studied
areas (in January, April, July, October, and
humans (de la Fuente et al. 2008). December), covering the rainy and the dry
There are no human vaccines for Chagas seasons. These collection sites in forest fragments
disease or cutaneous or visceral leishmaniasis, inside the city of Salvador were chosen consider-
diseases that have spread as fast as accelerated ing their neighboring areas, which are densely
urbanization and occupation of rain forest populated and had poor sanitary infrastructure,
areas have taken place in Brazil and other with no delimited borders between the rainforest
area and the neighboring houses (Fig. 1). For
tropical countries. We describe the detection free-living animal capture, 20 Sherman traps and
and prevalence of T. cruzi and Leishmania sp. 20 Tomahawk traps (Rosaminas, Piraúba, Brazil)
in wild mammals captured from urban rain- were strategically placed in the rainforest, with
forest fragments located in Salvador, Brazil. banana, pineapple, and smoked pig fat used as
bait. Traps were placed 20 m from each other in a
central area of each rainforest fragment; the
MATERIALS AND METHODS objective was to be as far as possible from the
borders to avoid human destruction of the traps
Animal capture and identification
and because the wild animals might be frightened
We worked in different rainforest fragments in by human presence. The taxonomic classification
the metropolitan region of Salvador, Bahia State, of animals captured was made as previously
Brazil (12858 0 13 0 0 S, 38830 0 45 0 0 W). Salvador has a described (Reis et al. 2011), and when it was not
TRÜEB ET AL.—TRYPANOSOMA CRUZI AND LEISHMANIA SP. INFECTION IN BRAZIL 3

TABLE 1. Number, by genus and species, of free- medium containing 1.5 mL of blood-agar solid
living wild mammals captured and examined for medium and 2 mL of Schneider’s medium
trypanosomatid (Trypanosoma cruzi and Leishmania (Sigma-Aldrich, St. Louis, Missouri, USA) sup-
sp.) infection, in rainforest urban fragments from plemented with 20% of fetal bovine serum (Life
Salvador City, Brazil, during 2012 and 2013. Technologies, Grand Island, New York, USA) and
antibiotics. The cultures were incubated for 6 wk
Mammal n (% total animals) at 25 C and observed by optical microscopy once
per week. Positive cultures were subjected to
Didelphis sp. (opossum) 22 (33.8) DNA extraction for PCR evaluation and parasite
Micoureus sp. (opossum) 16 (24.6)
identification. Thirteen animal samples—five
splenic samples, five liver samples, and eight
Cerdocyon thous (crab-eating fox) 5 (7.7)
blood samples—were analyzed by culture. These
Nasua nasua (coati) 1 (1.5) samples were taken when it was possible to 1)
Dasypus sp. (armadillo) 5 (7.7) collect a sufficient amount of blood for the
Callithrix sp. (marmoset) 5 (7.7) procedures and/or 2) perform liver or spleen
Mus musculus (mouse) 2 (3.1) puncture.
Rattus rattus (rat) 4 (6.2)
Trinomys sp. (rodent) 3 (4.6) PCR for T. cruzi and Leishmania sp. detection
Oecomys sp. (rat) 2 (3.1)
Total 65 (100)
A PCR for Leishmania sp. detection was
performed on genomic DNA extracted from
blood samples from all 65 animals, as previously
described (Rocha et al. 2010), using primers D1
possible to perform complete species identifica- (5 0 -GGGGAGGGGCGTTCTGCGAA-3 0 ), D2 (5 0 -
tion, genus classification was assumed. CCGCCCCTA TTTTACACCAACCCC-3 0 ), and
D3 (5 0 -GGCCCACTATATTA CACCAACCCC-
Samples collection and clinical evaluation 3 0 ). This PCR reaction amplifies the Leishmania
Captured animals were anesthetized (Santiago braziliensis, Leishmania infantum, and Leishman-
et al. 2007) to undergo clinical examination by ia amazonensis kDNA minicircle (120 bp) geno-
veterinarians with the objective to search for signs mic region, with high specificity and sensitivity.
of disease such as mucosal paleness, congestion or A PCR for T. cruzi molecular detection was
jaundice, emaciation, lymph node enlargement, carried out as described (Leça-Junior et al. 2013)
skin lesions, discharges from natural orifices, in blood samples from all 65 studied animals using
presence of ectoparasites, and sampling. Blood the primers S35 (5 0 -AAATAATGTACGGGGGA-
was collected from the tail vein, jugular vein, or GATGCATGA-3 0 ) and S36 (5 0 -GGGTTCGATTG
femoral artery using vacuum tubes containing GGGTTGGTGT-3 0 ). These primers are specific
EDTA as an anticoagulant. Fine needle aspira- to T. cruzi kDNA conserved regions and were
tions of spleen and liver were performed using previously described as sensitive and specific tools
sterile materials, adapting the method described for the parasite detection and classification (Avila
for canids (Barrouin-Melo et al. 2006). All animals et al. 1990).
had their left ear marked through the excision of a
1–2 mm ‘‘V’’-shaped fragment of the ear tip with RESULTS
the objective of avoiding data duplication and
were returned to their habitat. Samples were
A total of 65 free living mammals were
refrigerated until laboratory processing.
All procedures were performed under the captured (Table 1). The specimens belonged
license of the Brazilian Institute of Environment to 10 different genera, being mostly marsupi-
and Renewable Resources–Sistema de Autoriza- als (58%, 38/65), which were 34% (22/65)
ção e Informação em Biodiversidade (IBAMA– from Didelphis and 25% (16/65) from Mi-
SISBIO no. 32058) and were approved by the coureus. There was a more intense trapping of
Ethics Committee on Animal Use from the
Federal University of Bahia (license no. 19/2011). wild animals during the rainy season (from
May to August), and a similar number of
Parasite isolation and culture animals were trapped in each of the studied
areas.
Culture for parasite isolation was performed
using 18 samples taken from the captured Among the 65 animals tested by PCR, 28
animals. Briefly, samples of whole blood, spleen, were positive for at least one of the parasites:
or hepatic puncture were cultivated in a biphasic 41% (27/65) were positive for Leishmania sp.
4 JOURNAL OF WILDLIFE DISEASES, VOL. 54, NO. 1, JANUARY 2018

FIGURE 2. Molecular detection of Trypanosoma cruzi (A) and Leishmania sp. (B) in blood cells from wildlife
mammals captured in Salvador metropolitan region during 2013. Numbers inside/above the columns represent
the number of positive or negative animals for each assay.

and 12% (8/65) for T. cruzi. Seven animals one positive isolation was obtained from a
(11%, 7/65) were positive for both parasites. blood sample. All samples that were positive
All animals whose samples were positive for T. by culture were positive for both Leishmania
cruzi by PCR belonged to the genus Didelphis sp. and T. cruzi–specific DNA amplification,
sp. (Fig. 2A). Marsupials also showed positive demonstrating concomitant infection of the
results by PCR for Leishmania sp.: 36% (10/ two parasites in the same host.
28) were Didelphis and 32% (9/28) were Clinical evaluation showed that 88% (57/65)
Micoureus (Fig. 2B). Infections by both of the animals were clinically healthy, having
parasites could be detected in trapped animals no apparent signs of disease. Skin alterations
throughout the whole experiment period. found in 18% (12/65) of the animals were
Among the 13 animals whose samples were characterized as small fresh abrasions in the
tested by culture for parasite isolation, three snout or tail, apparently caused by attempts to
(all Didelphis sp. marsupials) had positive escape from the trap. Other skin changes
flagellated forms as observed by microscopy, suggested clashes caused by territorialism
including one from spleen, one from liver, and fights or reactions to ectoparasite bites.
TRÜEB ET AL.—TRYPANOSOMA CRUZI AND LEISHMANIA SP. INFECTION IN BRAZIL 5

TABLE 2. Clinical signs and parasitological diagnosis of Trypanosoma cruzi and/or Leishmania sp. in wild
mammals from rainforest urban fragments in Salvador City, Brazil, during 2013.

PCR PCR Isolation


Animal Genus/species T. cruzi Leishmania sp. T. cruzi and Leishmania sp. Clinical signs

AV001 Didelphis sp. Positive Positive Positive (HP)a None


AV002 Didelphis sp. Positive Positive NCb None
AV003 Didelphis sp. Positive Positive Positive (SP)c None
Negative (HP)
AV004 Didelphis sp. Positive Negative Negative (SP) Exfoliative dermatitis
Negative (HP)
AV005 Didelphis sp. Positive Positive Negative (SP) Exfoliative dermatitis
Negative (HP)
AV006 Didelphis sp. Positive Positive Negative (SP) None
Negative (HP)
AV007 Didelphis sp. Positive Positive NC None
AV008 Didelphis sp. Negative Positive NC None
AV009 Didelphis sp. Positive Positive NC None
AV013 Dasypus sp. Negative Positive NC None
AV020 Micoureus sp. Negative Positive NC None
AV021 Micoureus sp. Negative Positive NC None
AV022 Mus musculus Negative Positive NC None
AV023 Micoureus sp. Negative Positive NC Cyanosis, diarrhea, hypothermia
AV026 Didelphis sp. Positive Positive Positive (BC)d None
AV033 Callithrix sp. Negative Positive NC None
AV035 Micoureus sp. Negative Positive NC Focal alopecia
AV039 Rattus rattus Negative Positive NC None
AV045 Micoureus sp. Negative Positive NC Focal alopecia
AV050 Micoureus sp. Negative Positive NC None
AV051 Didelphis sp. Negative Positive NC None
AV057 Trynomis sp. Negative Positive NC None
AV059 Callithrix sp. Negative Positive NC None
AV063 Dasypus sp. Negative Positive NC None
AV067 Cerdocyon thous Negative Positive NC None
AV067 Micoureus sp. Negative Positive NC None
AV069 Micoureus sp. Negative Positive NC None
AV072 Micoureus sp. Negative Positive NC None
a
HP ¼ hepatic puncture.
b
NC ¼ not collected.
c
SP ¼ splenic puncture.
d
BC ¼ blood culture.

Nineteen animals (29%19/65) had ectopara- tive clinical signs. The Micoureus sp. that
sites, such as fleas, ticks, or insect larvae and presented diarrhea, hypothermia, and cyano-
eggs, and most of these animals (13/19) were sis also tested positive for Leishmania sp.
Didelphis. An opossum (Micoureus sp.) had infection by PCR. Two other Micoureus that
severe diarrhea at the time of capture, as well presented multifocal alopecia, a common
as bradycardia and pale mucous tissues, the clinical sign of leishmaniasis as described in
last being an indicator of anemia. dogs and humans, were also positive for
None of the animals with negative PCR Leishmania sp. by PCR. Two of the positive
results showed clinical abnormalities. Table 2 Didelphis for Leishmania sp. infection by
shows PCR-positive animals and their respec- PCR also exhibited exfoliative dermatitis.
6 JOURNAL OF WILDLIFE DISEASES, VOL. 54, NO. 1, JANUARY 2018

Most PCR-positive animals (82%, 23/28) (Santiago et al. 2007). Other species of
showed no clinical signs that could be related marsupials, such as Micoureus, have not been
to trypanosomatid infections. well described as parasite reservoirs. Never-
theless, other authors have reported a Leish-
mania sp. infection prevalence of 7.5% of in
DISCUSSION
Micoureus paraguayanus from an isolated
Among the wild animals identified as forest reserve in São Paulo, Brazil (Quintal
Leishmania sp. reservoirs in Brazil, the most et al. 2011). In our study, 56% of captured
thoroughly studied have been wild canids and Micoureus were positive for Leishmania sp.
marsupials of the genus Didelphis. However, The methodological approach may represent a
only one out of the five canids analyzed in the reason for such different frequencies, since
present study was positive for Leishmania sp. we performed diagnostic tests on blood,
Other authors also observed low frequencies spleen, and liver, while the former authors
of positivity in wild canids from endemic areas used only skin samples. Perhaps even more
for Leishmania infection (Courtenay et al. critically, the environmental characteristics of
2002; Ferreira et al. 2013). These findings the studied areas differed between the
studies, suggesting that wild animals living in
endorse the idea that the role of canids in the
rainforest fragments engulfed by the city
epidemiological cycle of this parasite may not
could be more susceptible to, or at least more
be more important than that of other wild
exposed to, infections than animals from a
mammals, even though they indicate that
forest reserve. In fact, according to previous
canids are at least potential reservoirs. In fact,
studies (Santiago et al. 2007), animals inhab-
the concept of potential reservoirs has been
iting periurban areas may present a higher
redescribed as those that are able to maintain
prevalence when compared to those captured
and act as a source of the parasite in nature
in conserved forest areas. Other authors have
(Roque et al. 2014). Nevertheless, this aspect
described findings of infection under similar
was beyond the scope of this study and would conditions in some countries from Africa
require some studies with larger numbers of (Bousslimi et al. 2012) and in other areas
canids to answer the question. The character- within Brazil (Leça-Junior et al. 2013). These
ization of the Leishmania spp. encountered in reports indicate the need for better planning
wild mammals would be relevant, but the of public health and environmental policies.
assay to distinguish Leishmania species re- A Rattus rattus, a Mus musculus, and a
quires a large sample (de Andrade et al. 2006), Trinomys sp. were found positive for Leish-
and for ethical and methodological reasons it mania sp. and represented 11% of Leishmania
was impossible to retrieve such samples from sp.–positive animals in the present study.
the wild animals we tested. Since the PCR There are few studies describing rodents as
used in our study is specific for L. braziliensis, natural hosts of Leishmania, but recently a
L. infantum, and L. amazonensis kDNA report described natural infection of wild M.
minicircle (120 bp) genomic region (Rocha musculus and R. rattus in an endemic area for
et al. 2010), it is worth saying that the L. infantum in Europe (Navea-Pérez et al.
Leishmania isolates from these animals are 2015). Some other species have been cited as
pathogenic and involved in public health reservoirs of Leishmania and T. cruzi (Mar-
problems. celino et al. 2011; Botto-Mahan et al. 2012).
Didelphis sp. marsupials presented the Rattus norvegicus have been found positive
highest percentage of positivity for Leishman- for Leishmania sp. at the frequency of 36.3%
ia sp. (37%) in the present study. Our data in Minas Gerais, another leishmaniasis-en-
may corroborate the results of previous demic state in Brazil (Marcelino et al. 2011).
studies that demonstrate evidences that these However, no R. norvegicus was captured in
marsupials could be important wild reservoirs our study sites. There are no reports of
of the parasite in urban fragments of forests infection by trypanosomatids in the rodent
TRÜEB ET AL.—TRYPANOSOMA CRUZI AND LEISHMANIA SP. INFECTION IN BRAZIL 7

Trinomys sp.; ours may be the first report of humans infected by Leishmania in Camaçari,
natural infection with Leishmania sp. in this a town very close to Salvador (Cunha et al.
species. 1995). Recently the same area was again
We observed concomitant infections with studied 20 years later, and a 46% prevalence
Leishmania sp. and T. cruzi in 17% 6/35(6/35) was found. In addition, individuals residing in
positive samples from 28 animals. Coinfection houses with a sand backyard had significantly
with trypanosomatids has been reported lower rates of Leishmania infection, when
previously in wild animals (Ramirez et al. compared to those with a different type or no
2002). De Araújo and collaborators (2013) backyard (Maia et al. 2016). Despite being
found mixed infections with T. cruzi, Try- surrounded by areas with a high incidence of
panosoma rangeli, and Leishmania sp. in the disease, Salvador is not considered an
whole blood and bone marrow of an anteater endemic area, because no proved autochtho-
(Tamandua tetradactyla). Didelphis was the nous cases have been described so far. For
only genus diagnosed positive for both para- Chagas disease, some cities close to Salvador
sites, Leishmania sp. and T. cruzi, in our are considered endemic areas (Mota et al.
study, indicating the possible importance of 1990).
this marsupial in the transmission of both A missing step in the epidemiology of the
parasites. Yet two out of the five armadillos forest remnants in Salvador yet to be deter-
(Dasypus sp., family Xenarthra) we captured mined is to ascertain the vectors species
and examined were positive only for Leish- involved. Lutzomyia longipalpis, a species
mania sp. complex, is a very urbanized and anthropo-
Among the wild animals described in our philic species rarely found in forest remnants
study, two out of five (40%) free-living (Soares and Turco 2003; Salomón et al. 2015).
Callithrix sp. were positive for Leishmania This is in accordance with other vector studies
sp. There have been no previous reports of in Gafanhoto Park, Minas Gerais, Brazil,
free-living Callithrix infected with Leishmania which did not find L. longipalpis in periur-
sp. in Brazil. The susceptibility of Callithrix ban-forested areas (Margonari et al. 2010).
sp. to infection by Leishmania sp. has been Also, no study has reported the finding of L.
investigated by experimental infection (Car- longipalpis in Salvador (Magalhães-Junior et
neiro et al. 2012). However, in contrast to the al. 2012). However, the scenario for the
results of those authors, the naturally infected vectors of cutaneous leishmaniasis is com-
primates we examined showed no clinical pletely different, as they are often associated
signs of leishmaniasis. Together with the with forests and peridomestic areas. Such
finding of Leishmania infection in Trinomys vectors may include Lutzomyia whitmani and
sp., our finding of Leishmania in Callithrix sp. Lutzomyia intermedia, very anthropophilic
may indicate the possibility that wild animals species commonly found in the neighboring
may become hosts for such an important region of Corte de Pedra in Bahia State, Brazil
parasite, as environmental changes affect their (Soares et al. 2010). Vector surveys in our
habitats. The subject of newly infected species study sites are still needed to determine the
in areas that have been modified by human species, frequency, fluctuation, and percent-
action should be investigated more thorough- age of infected insects. Considering that some
ly. We hypothesize that rainforest remnants of the reservoirs observed in the present study
located inside urban regions with poor sani- could act as potential reservoirs for sandflies,
tary infrastructure may become focuses of Salvador must be at risk at least for cutaneous
infection and represent risks for the human leishmaniasis.
population as well as for endangered animal In the present study, T. cruzi infection was
species. detected only in Didelphis sp. marsupials. A
Bahia State is endemic for canine and recent study described the infection by T.
human leishmaniasis and Chagas disease. A cruzi in marsupials and chiroptera from
previous study found a 30% seroprevalence of Maranhão State, Brazil, but these animals
8 JOURNAL OF WILDLIFE DISEASES, VOL. 54, NO. 1, JANUARY 2018

were captured in deep forest areas (da Costa Botto-Mahan C, Bacigalupo A, Correa JP, Oda E, Solari
et al. 2015). Also, Rosypal et al. (2014) A. 2012. Field assessment of Trypanosoma cruzi
infection and host survival in the native rodent
reported that wild canids from Tennessee, Octodon degus. Acta Trop 122:164–167.
US, present T. cruzi specific antibodies, but Bousslimi N, Ben-Ayed S, Ben-Abda I, Aoun K,
again these animals did not belong to Bouratbine A. 2012. Natural infection of North
periurban forest areas. The overlap between African gundi (Ctenodactylus gundi) by Leishmania
wild and domestic environments where T. tropica in the focus of cutaneous leishmaniasis,
Southeast Tunisia. Am J Trop Med Hyg 86:962–965.
cruzi circulates is increasing and the risk Carneiro LA, Laurenti MD, Campos MD, Gomes CM,
factors for Chagas disease and the boundaries Corbett CE, Silveira FT. 2012. Susceptibility of
between wild and domestic transmission peritoneal macrophage from different species of
cycles have been redefined in tropical coun- neotropical primates to ex vivo Leishmania (L.)
tries (Herrera 2014). Our study reinforces this infantum chagasi-infection. Rev Inst Med Trop São
Paulo 54:95–102.
situation, because it showed that Didelphis sp. Courtenay O, Quinnell RJ, Garcez LM, Dye C. 2002. Low
marsupials, living in forest fragments inside infectiousness of a wildlife host of Leishmania
the third largest Brazilian city, were infected infantum: The crab-eating fox is not important for
with T. cruzi. These marsupials are very transmission. Parasitology 125:407–414.
common in those wild environments, have a Cunha S, Freire M, Eulalio C, Critosvao J, Netto E,
Johnson WD Jr, Reed SG, Badaro R. 1995. Visceral
large contact with the population living close leishmaniasis in a new ecological niche near a major
to those areas, and are commonly captured in metropolitan area of Brazil. Trans R Soc Trop Med
suburban streets and backyards. Not surpris- Hyg 89:155–158.
ingly, Ribeiro et al. (2015) found T. cruzi– da Costa AP, Costa FB, Soares HS, Ramirez DG, de
Carvalho Mesquita ETK, Gennari SM, Marcili A.
infected triatomines in suburban areas of
2015. Trypanosoma cruzi and Leishmania infantum
Salvador city. The present study, which chagasi infection in wild mammals from Maranhão
reports data on natural infection by T. cruzi State, Brazil. Vector-Borne Zoonot Dis 15:656–666.
in wild mammals in related areas, reinforces de Almeida Curi NH, de Oliveira Paschoal AM, Massara
that the parasite is circulating between the RL, Marcelino AP, Ribeiro AA, Passamani M,
Demétrio GR, Chiarello AG. 2014. Factors associat-
vectors and wild reservoirs in forest fragments
ed with the seroprevalence of leishmaniasis in dogs
inside the city. living around Atlantic forest fragments. PLoS One 9:
e104003.
de Andrade HM, Reis AB, dos Santos SL, Volpini ÂC,
ACKNOWLEDGMENTS
Marques MJ Romanha AJ. 2006. Use of PCR-RFLP
Our study was financed by the Brazilian agency to identify Leishmania species in naturally-infected
for research and development the ‘‘Bahia Re- dogs. Vet Parasitol 140:231–238.
search Foundation’’ (FAPESB; grant no. PRO- de Araújo VA, Boité MC, Cupolillo E, Jansen AM, Roque
NEM: 498/2011-PNE 0002/2011) and by the ALR. 2013. Mixed infection in the anteater Taman-
‘‘Brazilian Coordination for Improvement of dua tetradactyla (Mammalia: Pilosa) from Pará State,
Higher Education Personnel’’ (CAPES; MSc Brazil: Trypanosoma cruzi, T. rangeli and Leishmania
degree scholarship for I. Trüeb). The authors infantum. Parasitology 140:455–460.
thank Karen Vasconcelos for technical assistance. de la Fuente ALC, Dias-Lima A, Lopes CM, Emperaire
L, Walter A, Ferreira A, Sherlock I, Noireau F. 2008.
LITERATURE CITED Behavioral plasticity of Triatominae related to habitat
selection in northeast Brazil. J Med Entomol 45:14–
Avila H, Goncalves AM, Nehme NS, Morel CM, Simpson 19.
L. 1990. Schizodeme analysis of Trypanosoma cruzi Dias-Lima AG, Sherlock ÍA. 2000. Sylvatic vectors
stocks from South and Central America by analysis of invading houses and the risk of emergence of cases
PCR-amplified minicircle variable region sequences. of Chagas disease in Salvador, State of Bahia,
Mol Biochem Parasitol 42:175–187. Northeast Brazil. Mem Inst Oswaldo Cruz 95:611–
Barrouin-Melo SM, Laranjeira DF, de Andrade Filho FA, 613.
Trigo J, Julião FS, Franke CR, Aguiar PHP, dos- Epstein JH, Price JT. 2009. The significant but under-
Santos WLC, Pontes-de-Carvalho L. 2006. Can studied impact of pathogen transmission from
spleen aspirations be safely used for the parasitolog- humans to animals. Mt Sinai J Med 76:448–455.
ical diagnosis of canine visceral leishmaniosis? A Ferreira PRB, Larangeira DF, de Oliveira LS, Malta
study on asymptomatic and polysymptomatic animals. MCC, Gomes MC, Bastos BL, Portela RW, Bar-
Vet J 171:331–339. rouin-Melo SM. 2013 Indirect ELISA test for the
TRÜEB ET AL.—TRYPANOSOMA CRUZI AND LEISHMANIA SP. INFECTION IN BRAZIL 9

serological diagnosis of visceral leishmaniasis in wild guayanus (Didelphimorphia: Didelphidae) of Brazil.


canids. Pesq Vet Bras 33:528–534. Vet Parasitol 176:112–119.
Grisotti M. 2010. Emerging infectious diseases and the Ramirez LE, Lages-Silva E, Alvarenga-Franco F, Matos
emergence of diseases: A conceptual revision and A, Vargas N, Fernandes O, Zingales B. 2002. High
new issues. Cien Saude Colet 15:1095–1104. prevalence of Trypanosoma rangeli and Trypanoso-
Herrera L. 2014. Trypanosoma cruzi, the causal agent of ma cruzi in opossums and triatomids in a formerly-
Chagas disease: Boundaries between wild and endemic area of Chagas’ disease in Southeast Brazil.
domestic cycles in Venezuela. Front Public Health Acta Trop 84:189–198.
2:259. Reis NR, Peracchi AL, Pedro WA, Lima IP. 2011.
Instituto Brasileiro de Geografia e Estatı́stica. 2015. Brazilian mammals. Londrina State University Press,
cidades@ Bahia Salvador. http://cidades.ibge.gov.br/ Londrina, Brazil, 437 pp.
xtras/perfil.php?codmun¼292740. Accessed July Ribeiro G Jr, Gurgel-Gonçalves R, Reis RB, dos Santos
2016. CG, Amorim A, Andrade SG, Reis MG. 2015.
Leça-Júnior NF, Almeida VA, Carvalho FS, Albuquerque Frequent house invasion of Trypanosoma cruzi-
GR, Silva FL. 2013. First report of Trypanosoma infected triatomines in a suburban area of Brazil.
cruzi infection in naturally infected dogs from PLoS Negl Trop Dis 9:e0003678.
southern Bahia, Brazil. Rev Bras Parasitol Vet 22: Rocha MN, Margonari C, Presot IM, Soares RP. 2010.
182–185. Evaluation of 4 polymerase chain reaction protocols
Magalhães-Junior JT, Mota TF, Larangeira DF, Dias- for cultured Leishmania spp. typing. Diagn Microbiol
Lima AG, Franke CR, Barrouin-Melo SM. 2012. Infect Dis 68:401–409.
[First report of Evandromia sallesi and Evandromyia Roque AL, Jansen AM. 2014. Wild and synanthropic
cortelezzii (Diptera: Psychodidae) occurrence in reservoirs of Leishmania species in the Americas. Int
metropolitan region of Salvador, Bahia State, Brazil]. J Parasitol Parasites Wildl 3:251–262.
Rev Baian Saud Public 36:979–985. Portuguese. Rosypal AC, Smith T, Alexander A, Weaver M, Stewart R,
Maia Z, Viana V, Muniz E, Gonçalves LO, Mendes CM, Houston A, Gerhold R, Van Why R, Dubey JP. 2014.
Mehta SR, Badaro R. 2016. Risk factors associated Serologic survey of antibodies to Trypanosoma cruzi
with human visceral leishmaniasis in an urban area of in coyotes and red foxes from Pennsylvania and
Bahia, Brazil. Vector-Borne Zoonot Dis 16:368–376. Tennessee. J Zoo Wildl Med 45:991–993.
Marcelino AP, Ferreira EC, Avendanha JS, Costa CF, Salomón OD, Feliciangeli MD, Quintana MG, Afonso
Chiarelli D, Almeida G, Moreira EC, Leite RC, dos MMS, Rangel EF. 2015. Lutzomyia longipalpis
Reis JK, Gontijo CM. 2011. Molecular detection of urbanisation and control. Mem Inst Oswaldo Cruz
Leishmania brasiliensis in Rattus norvegicus in an 110:831–846.
area endemic for cutaneous leishmaniasis in Brazil. Santiago MEB, Vasconcelos RO, Fattori KR, Munari DP,
Vet Parasitol 183:54–58. Michelin AF, Lima VMF. 2007. An investigation of
Margonari C, Soares RP, Andrade-Filho JD, Xavier DC, Leishmania spp. in Didelphis spp. from urban and
Saraiva L, Fonseca AL, Silva RA, Oliveira ME, peri-urban areas in Bauru (São Paulo, Brazil). Vet
Borges EC, Sanguinette CC, et al. 2010. Phleboto- Parasitol 150:283–290.
mine sand flies (Diptera: Psychodidae) and Leish- Soares RP, Margonari C, Secundino NC, Macêdo ME, da
mania infection in Gafanhoto Park, Divinópolis, Costa SM, Rangel EF, Pimenta PF, Turco SJ. 2010.
Brazil. J Med Entomol 47:1212–1219. Differential midgut attachment of Leishmania (Vi-
McFarlane R, Sleigh A, McMichael T. 2012. Synanthropy annia) braziliensis in the sand flies Lutzomyia
of wild mammals as a determinant of emerging (Nyssomyia) whitmani and Lutzomyia (Nyssomyia)
infectious diseases in the Asian-Australasian region. intermedia. J Biomed Biotechnol 2010:439174.
EcoHealth 9:24–35. Soares RPP, Turco SJ. 2003. Lutzomyia longipalpis
Mota EA, Guimarães AC, Santana OO, Sherlock Í, Hoff (Diptera: Psychodidae: Phlebotominae): A review.
R, Weller TH. 1990. A nine year prospective study of An Acad Bras Cienc 75:301–330.
Chagas’ disease in a defined rural population in Souza CF, Borges MA, Andrade AJ. 2009. Contribution to
northeast Brazil. Am J Trop Med Hyg 42:429–440. the knowledge of the phlebotomine sand flies fauna
Navea-Pérez HM, Dı́az-Sáez V, Corpas-López V, Merino- (Diptera: Psychodidae) of Timóteo Municipality,
Espinosa G, Morillas-Márquez F, Martı́n-Sánchez J. Minas Gerais, Brazil. Neotrop Entomol 38:267–271.
2015. Leishmania infantum in wild rodents: Reser- Thompson RCA, Lymbery AJ, Smith AA. 2010 Parasites,
voirs or just irrelevant incidental hosts? Parasitol Res emerging disease and wildlife conservation. Int J
114:2363–2370. Parasitol 40:1163–1170.
Quintal APN, Ribeiro ES, Rodrigues FP, Rocha FS,
Floeter-Winter LM, Nunes CM. 2011. Leishmania Submitted for publication 26 January 2017.
spp. in Didelphis albiventris and Micoureus para- Accepted 26 May 2017.

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