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Trypanosoma Found in Synanthropic Mammals from Urban Forests of Parana´, Southern Brazil

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Trypanosoma Found in Synanthropic Mammals from Urban Forests of Parana´, Southern Brazil VECTOR-BORNE AND ZOONOTIC DISEASES Volume XX, Number XX, 2019 ª Mary Ann Liebert, Inc. DOI: 10.1089/vbz.2018.2433 Trypanosoma Found in Synanthropic Mammals from Urban Forests of Parana´, Southern Brazil Ricardo Nascimento Drozino,1 Fla´vio Haragushiku Otomura,2 Janaina Gazarini,3 Moˆnica Lu´cia Gomes,1 and Max Jean de Ornelas Toledo1 Abstract Trypanosoma cruzi is a parasitic protozoan that infects a diversity of hosts constituting the cycle of enzootic transmission in wild environments and causing disease in humans (Chagas disease) and domestic animals. Wild mammals constitute natural reservoirs of this parasite, which is transmitted by hematophagous kissing bugs of the family Reduviidae. T. cruzi is genetically subdivided into six discrete typing units (DTUs), T. cruzi (Tc)I to TcVI. In Brazil, especially in the state of Parana´, TcI and TcII are widely distributed. However, TcII is less frequently found in wild reservoirs and triatomine, and more frequently found in patients. The goal of this study was to investigate the natural occurrence of T. cruzi in wild synanthropic mammals captured in urban forest fragments of the Atlantic Forest of Parana´, southern Brazil. In this way, 12 opossums and 35 bats belonging to five species were captured in urban forest parks of the city of Maringa´, Parana´, an area considered endemic for Chagas disease. PCR-kinetoplast DNA molecular diagnostic reveals Trypanosoma sp. infection in 12 (100%) Didelphis albiventris and 10 (40%) Artibeus lituratus. In addition to demonstrating the presence of Trypano- soma in the two groups of mammals studied, we obtained an isolate of the parasite genotyped as TcII by amplification of the cytochrome oxidase II gene by PCR, followed by restriction fragment length polymorphism with AluI, and confirmed by PCR of rDNA 24Sa. This is the first record of the encounter in wild mammals of Trypanosoma DNA (in A. lituratus) and T. cruzi DTU TcII (in D. albiventris) in the state of Parana´. Keywords: Trypanosoma cruzi II, Didelphis albiventris, Artibeus lituratus, natural infection, Parana´ endemic area Introduction Atlantic Forest biome, TcII is the most frequently isolated (95%) DTU in human patients with chronic infection (Gas- rypanosoma cruzi (Kinetoplastida, Trypanosomati- parim et al. 2018), as well as in the triatomine species Pan- Tdae), the etiologic agent of Chagas disease or American strongylus megistus and Triatoma sordida, but not in wild Downloaded by SENCKENBERG/ZEITSCHRIFTEN from www.liebertpub.com at 07/23/19. For personal use only. trypanosomiasis, is a parasitic protozoan capable of infecting mammals (Abolis et al. 2011). In this state, TcI has been a diversity of hosts, constituting a wild enzootic transmission isolated, in these same species of triatomines, both in pure cycle through vectors in humans and domestic animals. The and mixed infections with TcII, as well as the marsupial species is subdivided into discrete typing units (DTUs), from Didelphis albiventris. T. cruzi (Tc)I to TcVI, as well as Tcbat (Marcili et al. 2009, Mammals of the orders Chiroptera and Didelphimorphia Zingales et al. 2009, 2012, Lima et al. 2015). Another re- are well-known reservoirs of T. cruzi and other trypanoso- cently proposed classification system separates T. cruzi into matids. With ample population abundance, accentuated sy- just three groups, from mtTcI to mtTcIII, based on mito- nanthropism, and high mobility, these animals play an chondrial genes (Barnabe´ et al. 2016). All DTUs are found in important role in the distribution of diverse species of path- a diverse array of mammalian hosts, representing seven dif- ogens (De Oliveira et al. 2010, Hamilton et al. 2012, Brook ferent orders, and in triatomine insects (Reduviidae, Triato- and Dobson 2015, da Costa et al. 2015). These mammals’ minae) throughout all states and biomes in Brazil (Jansen species demonstrate the highly complex ecological interac- et al. 2015). However, in the state of Parana´, which is 97.8% tions found in the T. cruzi transmission cycle, being necessary 1Department of Basic Health Sciences, Universidade Estadual de Maringa´, Maringa´, Brazil. 2Biological Sciences Sector, Universidade Estadual do Norte do Parana´, Bandeirantes, Brazil. 3College of Biological and Environmental Sciences, Universidade Federal da Grande Dourados, Dourados, Brazil. 1 2 DROZINO ET AL. the conduction of studies that evaluate its dynamics in the Wild mammal capture context of the One Health concept, triad that encompasses The campaigns were held once a month in the following humans, domestic animals, wildlife, and the changing eco- periods: from September 2014 to December 2015. Bats systems in which they live (Thompson 2013, Pinazo and were captured with mist nets, conditioned in cloth sacs, and Gascon 2015). identified at the species level. Opossums of the species In this study, a preliminary investigation into the presence D. albiventris were captured using Tomahawk Live Traps Trypanosoma of in free-range wild mammals was accom- baited with fruits and peanut butter. These methods were plished in Atlantic Forest remnants situated in urban areas, an approved by the Instituto Chico Mendes de Conservac¸a˜oda ´ environment not still explored in the state of Parana. Biodiversidade—Ministe´rio do Meio Ambiente, Brazil (no. 42881) and by the Ethics Committee in Animal Experi- Materials and Methods mentation (CEUA) at Universidade Estadual de Maringa´ Study area (UEM) (no. 023/2014). Wild mammals were captured in two urban forests frag- Blood collection and hemocultures ments, in 23°25¢39¢ of latitude south and 51°55¢51† of lon- gitude west, and in 23°23¢27¢ of latitude south and 51°56¢34† Opossums and bats were anesthetized with 4.0 mg/kg of longitude west. Both, remnants of the Atlantic Forest bi- chloridrate of xylazine and 20.0 mg/kg body weight chlori- ome of the city of Maringa´, located in the northeast of Parana´, drate of ketamine for blood collection. Approximately southern Brazil, and an area considered endemic for Chagas 0.5 mL of whole blood obtained by cardiac puncture in the disease (Fig. 1). bats and from the tail medium vein in the opossums was Downloaded by SENCKENBERG/ZEITSCHRIFTEN from www.liebertpub.com at 07/23/19. For personal use only. FIG. 1. Map highlighting the two capture points located in the urban area of the Municipality of Maringa´, state of Parana´, Southern Brazil. TRYPANOSOMA IN WILD MAMMALS OF URBAN FOREST 3 placed in Novy, McNeal, and Nicolle medium, and covered PCR of rDNA 24Sa with an overlay of liver infusion tryptose (LIT) medium PCR amplification of rDNA 24Sa using D71 (5¢-AAGGT containing 10% fetal bovine serum. Another 0.2 mL was GCGTCGACAGTGTGG-3¢) and D72 (5¢-TTTTCAGAATG stored in microtubes containing 400 lL of 0.2 M ethylene- GCCGAACAGT-3¢) primers as previously described by diaminetetraacetic acid (EDTA) and 6.0 M guanidine solu- Souto et al. (1996). Amplified fragments were resolved on tion for the extraction and amplification of blood DNA 6% polyacrylamide gel, stained with silver, and analyzed according to Miyamoto et al. (2006). according to Sa´ et al. (2016). Molecular analysis for detection of Trypanosoma DNA Results DNA was extracted by the phenol/chloroform method and Detection of the kDNA minicircle in Trypanosoma precipitated with addition of ethanol and sodium acetate (Ma- cedo et al. 1992). PCR amplification was performed with oli- PCR-kDNA revealed that all samples of captured gonucleotides number 121 (5¢-AAATAATGTACGGG(T/G) D. albiventris (n = 12, 100%) exhibited a fragment of GAGATGCATGA-3¢) and number 122 (5¢-GGTT CGATTG 330 bp kDNA minicircle from Trypanosoma.Ofthe35 GGGTTGGTGTAATATA-3¢) according to the protocol of examined bat species, PCR-kDNA also detected this Gomes et al. (1998) modified by Miyamoto et al. (2006). These same fragment in 10/25 (40%) Artibeus lituratus caught. sequences amplify a specific fragment of *330 base pairs (bp) In other species of captured bats, Sturnira lilium (n = 4), of kinetoplast DNA (kDNA) from Trypanosoma sp. The am- Carollia perspicillata (n = 3), Pygoderma bilabiatum plification products were analyzed using 4.5% polyacrylamide (n = 2), and Platyrrhinus lineatus (n = 1), this fragment gel electrophoresis, stained with silver, and digitally recorded. was not detected (Table 1). This high rate of positivity in PCR was not observed in hemocultures, and in only 1/12 (8.3%) opossums was positive in this technique, allowing Isolation and genotyping of T. cruzi to obtain a T. cruzi isolate (Table 1). Parasites from a unique positive hemoculture, with low manipulation to avoid clonal selection, were amplified in LIT Genotyping of DTU of T. cruzi isolate medium until the exponential phase. This material was The isolate was genotyped by analysis of mitochondrial centrifuged and washed with Krebs-Ringer-Tris/pH 7.2 so- COII gene polymorphisms. The PCR/RFLP-COII showed lution buffer three times. The obtained mass was then re- two bands, the first at *80 bp referring to the species T. cruzi suspended in 500 lL of lysis solution (0.5 M EDTA, 5 M and the second at 250 bp, which consistently classifies the sodium chloride and 1% sodium dodecyl sulfate) supple- isolate as TcII (Fig. 2A). mented with 10 mg/mL of proteinase K (Invitrogen) at 37°C The result of PCR amplification of the rDNA 24Sa showed overnight. DNA extraction was performed by the phe- a band of *125 bp compatible with the TcII and TcVI ge- ´ nol/chloroform method after Sa et al. (2016). notypes. Although this marker is not able to distinguish these two genotypes, it was used to confirm the DTU of the isolate PCR/restriction fragment length polymorphism (Zingales et al. 2009, 2012). The profiles generated by the cytochrome oxidase II genetic analyzes of COII and rDNA 24Sa together, allowed to classify the T. cruzi isolate obtained as TcII (Fig. 2B). Differentiation of T. cruzi isolates (TcI to TcVI) was done by amplification of the cytochrome oxidase II (COII) gene by Discussion PCR, followed by restriction fragment length polymorphism (RFLP) with AluI (de Freitas et al.
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