It is known that wildlife is a significant element in maintaining and distributing the enzootic transmission cycles of numerous pathogens of importance to public or animal health. Wild animals from the Yucatán Peninsula, Mexico, such as rodents, bats, and some medium-sized mammals, have been registered as hosts of several pathogens, such as Rickettsia sp. (Panti-May et al., 2015), Leptospira sp. (Torres-Castro et al., 2020), Trypanosoma cruzi (Torres-Castro et al., 2021), Toxoplasma gondii (Torres-Castro et al., 2019), Leishmania sp. (Sosa-Bibiano et al., 2022), and different nematode species (Panti-May et al., 2021). All these findings reflect the need to continue with epidemiological studies that help to understand the role of wildlife in the life cycles of pathogens with zoonotic potential and to improve the knowledge about the health of their populations.
Dirofilaria immitis (Spirurida: Onchocercidae) is a parasitic nematode species widely distributed in areas with tropical and subtropical climates, such as the Yucatán Peninsula. It is colloquially known as “heartworm” and affects several wild and domestic animals belonging to different orders, such as Artiodactyla, Carnivora, Edentata, Lagomorpha, Perissodactyla, Primates, and Rodentia; however, canids and felids are its primary hosts (Simón et al., 2012; Penezić et al., 2014).
The disease caused by D. immitis, known as dirofilariasis, is recognized as a significant animal health problem due to its high prevalence and incidence rates in domiciliated dogs from endemic areas (Bolio-González et al., 2007; Caro-González et al., 2020). Likewise, in some countries in the Americas and Europe, clinical cases have been reported in people with lung conditions, so pulmonary dirofilariasis is cataloged as a disease potentially emerging due to the wide distribution of the biological vectors. Mosquitoes of the family Culicidae (Dantas-Torres & Otranto, 2013; Penezić et al., 2014) are the primary vectors and acquire infective microfilariae when feeding on the blood of infected hosts (Simón et al., 2012). Several mosquito species from the genera Aedes (Ae.), Anopheles, Culex, and Ochlerotatus have been described as probable vectors of D. immitis in endemic areas of the Americas (Dantas-Torres & Otranto, 2013).
There is evidence of D. immitis natural infection in wild animals (Simón et al., 2012; Penezić et al., 2014), including coatis (Nasua sp.) in South America (Moraes et al., 2017; Figuerêdo Duarte Moraes et al., 2022). However, epidemiological information on the involvement of this meso-mammal in the transmission cycle of D. immitis is scarce and limited worldwide (Vezzani et al., 2006), and in Mexico, the information is minimal and only in a morphological way (Caballero-Caballero, 1948). So, this study aims to report the natural infection with D. immitis in the white-nosed coati Nasua narica (colloquially known as “coati”) from Yucatán, Mexico.
Materials and Methods
We collected two carcasses (20°46′6.86″N-88°49′32.30″W and 20°45′44.59″N-88°47′9.35″W) of N. narica adult males on the Mérida-Cancún highway (Fig. 1A). Both were evaluated in situ to determine the presence of postmortem changes such as cadaveric rigidity, putrefaction, tympanism, etc., and deposited in a portable fridge with refrigerants for transport to the Faculty of Veterinary Medicine and Zootechnics of the Autonomous University of Yucatán (UADY), Mérida, Mexico, for processing. Due to the extensive damage in the carcasses (we suspected that the animals were impacted by vehicles) could not be prepared by conventional taxidermy to enter a mammal collection and obtain the corresponding record.
Fig. 1.
A) Image of one of the specimens (Nasua narica) collected on the Mérida-Cancún highway, Mexico. B) The aspect of the nematodes (arrow) collected in the heart. It can be seen that they are worms with elongated, cylindrical, and non-segmented bodies with bilateral symmetry.
In the macroscopic exploration of the heart in one specimen, two adult nematode parasites of the right ventricle (Fig. 1B) were collected and stored in 1.5 mL microcentrifuge tubes (Pirouet®, United States of America [USA]) soaked in 96 % alcohol for their subsequent identification by bioinformatics and phylogenetic analyses. Severe hemorrhages were observed in the heart (atria and ventricles); however, these findings should be taken carefully due to the probable cause of death.
Genomic DNA was extracted from an adult female nematode by making a diagonal incision in the midportion of the body. The specimen was placed in 500 μL of a 10 % Chelex-100® (Bio-Rad®, USA) chelating resin solution, to which 20 μL of proteinase were added (Aguilar-Domínguez et al., 2019). The sample was incubated at 56° C for 12 h, and the temperature was raised to 100° C for 15 minutes to eliminate the potential PCR inhibitors and increase the degradation of the proteins. The supernatant with the DNA was placed in a new tube and frozen at −20° C until its later use.
The PCR product was purified and sequenced at Macrogen Inc., Korea. Once the partial sequence was obtained, it was compared with those sequences available in GenBank, using the Basic Local Alignment Search Tool (BLAST-n, http://www.ncbi.nlm.nih.gov). Global alignments were performed using the Clustal W algorithm, and the nucleotide substitution model was selected based on the lowest Bayesian Information Criterion (BIC). To identify the phylogenetic position of the nematode, a Maximum Likelihood phylogenetic tree was generated with a support value of 10,000 Bootstrap iterations in IQ-TREE (http://www.iqtree.org/).
Unfortunately, due to the conservation method, both nematode parasites suffered severe damage to their structure, and it was not possible to use them for photomicrography.
Ethical Approval and/or Informed Consent
This article does not contain any studies with human participants or live animals.
Results and Discussion
We recovered a sequence of 516 bp of the 18S-rRNA gene, which exhibited a coverage of 100 % and similarity of 99 % (514/516 bp) with two sequences of D. immitis collected from dogs in Japan in 2010 (GenBank accession numbers: AB973230 and AB973231).
The phylogenetic analysis grouped the sequence generated in this study with the only three sequences of D. immitis available and deposited in GenBank in a monophyletic group with a support value of 94, which had Dirofilaria repens as a sister group with a support value of 100. The sequence generated in this study was deposited in GenBank under Accession number OP811190 (Fig. 2).
Fig. 2.
Phylogenetic reconstruction based on a partial fragment of the 18S-rRNA gene of several nematode species inferred by Maximum Likelihood and based on the Kimura two parameter Model (K2) with Gamma distribution (+G). Bootstrap values are indicated at the nodes. The scale bar at the bottom represents the degree of divergence.
The role of wildlife in the maintenance and spread of D. immitis is a matter of growing speculation because it is not understood whether wildlife may act as reservoirs, sentinels, or an accidental hosts and which species are significant in the sylvatic cycle (Moroni et al., 2020). The molecular, bioinformatics and phylogenetic analysis performed with the sequence obtained from the amplified fragment of the 18S-rRNA gene show the natural infection with D. immitis in N. narica from Yucatán, Mexico; therefore, these mammals participate in the epidemiological cycle of the parasite in this region.
As far as we know, this is the first molecular description of the D. immitis natural infection in N. narica from Mexico and North America. On an international level, the records of natural infection with D. immitis in Nasua sp. have been described in Argentina (Mazza, 1926; Mancebo et al., 1992) and Brazil (Figuerêdo Duarte Moraes et al., 2022). Additionally, in the Americas, the generated sequence in this study is the first sequence of D. immitis for this mammal host.
In Yucatán, D. immitis infects actively and frequently domiciled dogs from urban and rural sites (Bolio-González et al., 2007; Caro-González et al., 2020). This epidemiological aspect is relevant because the natural infection in domiciliated dogs has been related to D. immitis transmission towards medium-sized carnivore mammals such as coatis (Nasua sp.) since, eventually, both populations of animals have accidental contact. In addition, it has been suggested that dogs and coatis are involved in the same D. immitis transmission cycle, generated and maintained by mosquito vectors that circulate in the environment they share (Moraes et al., 2017; Figuerêdo Duarte Moraes et al., 2022).
To the best of our knowledge, this is the first study where N. narica carcasses are analyzed for the detection of heart nematodes, particularly D. immitis. The few previous reports, where necropsies have been performed on other procyonids species, show a low abundance of this nematode species, with two specimens recovered on Procyon lotor in the southeastern USA (Snyder et al., 1989). In a natural transmission experiment study performed on P. lotor it was possible to identify that nematodes did not develop in the two specimens exposed to infected mosquitoes (Christensen & Shelton, 1978). In contrast, dogs used as controls demonstrated the presence of a large number of adult nematodes. Necropsies performed on dogs in endemic areas show the presence of a high number of adult nematodes (Santoro et al., 2019). Therefore the role of procyonids as incidental hosts of D. immitis should be evaluated.
The present infection case was registered in an individual found on a highway that crosses through a dense forest; however, areas of variable extension destined for livestock and agriculture can be observed. Therefore, it is not possible to determine if this individual acquired the infection in the wild ecosystem or through indirect contact with peridomestic mosquitoes and infected dogs that accompany their owners to livestock and agricultural activities, a characteristic that is very common in dogs of people from rural municipalities from Yucatán state (Torres-Castro et al., 2022). This epidemiological aspect could influence the generation of the D. immitis transmission scenario in the populations of N. narica and other susceptible medium mammals (Moraes et al., 2017; Figuerêdo Duarte Moraes et al., 2022). Also, it has been argued that the human mobility and their domestic animals, mainly dogs, towards wild environments contributes to the exchange of zoonotic parasites such as D. immitis between different animal populations (wild and domestic) (Moraes et al., 2017).
Similarly, changes in land use, generated by activities such as urbanization, agriculture and livestock, cause the populations of Nasua sp. could coexist with wild canids that, in some endemic areas, have been described as competent hots of D. immitis (Simón et al., 2012; Penezić et al., 2014; Kotwa et al., 2019). In Yucatán, two species of wild canids are distributed: Canis latrans (colloquially known as “coyote”) and Urocyon cinereoargenteus (colloquially known as “gray fox”) (Sosa-Escalante et al., 2013). However, as far as we know, there are no records of D. immitis infection in these carnivore species, so more studies are necessary to establish their participation in the transmission cycle and spread of the parasite.
Another epidemiological factor that contributes to D. immitis transmission to atypical mammal hosts, such as Nasua sp., is the fragmentation of the natural habitat that allows adaptation to new environments and significant circulation of mosquitoes. In Yucatán, Ae. taeniorhynchus mosquitoes have been recognized as a competent vector of D. immitis (Manrique-Saide et al., 2008, 2010).
A hypothesis that should be included in future epidemiological studies is how the urbanization degree of the natural areas is modifying and influencing the transmission cycle of D. immitis through the generation of a higher rate of contact between populations of susceptible mammals, competent hots, and mosquito vectors (Worsley-Tonks et al., 2021). This wold help to know better the prevalence of D. immitis infection in coatis from the Yucatan Peninsula is substantial.
A) Image of one of the specimens (Nasua narica) collected on the Mérida-Cancún highway, Mexico. B) The aspect of the nematodes (arrow) collected in the heart. It can be seen that they are worms with elongated, cylindrical, and non-segmented bodies with bilateral symmetry.
Fig. 2.
Phylogenetic reconstruction based on a partial fragment of the 18S-rRNA gene of several nematode species inferred by Maximum Likelihood and based on the Kimura two parameter Model (K2) with Gamma distribution (+G). Bootstrap values are indicated at the nodes. The scale bar at the bottom represents the degree of divergence.
Aguilar-Domínguez, M., Sánchez-Montes, S., Esteve-Gassent, M.D., Barrientos-Salcedo, C., Pérez de León, A., Romero-Salas, D. (2019): Genetic structure analysis of Amblyomma mixtum populations in Veracruz State, Mexico. Ticks Tic Borne Dis, 10(1): 86 – 92. DOI: 10.1016/j.ttbdis.2018.09.004Aguilar-DomínguezM.Sánchez-MontesS.Esteve-GassentM.D.Barrientos-SalcedoC.Pérez de LeónA.Romero-SalasD.2019Genetic structure analysis of Amblyomma mixtum populations in Veracruz State, MexicoTicks Tic Borne Dis101869210.1016/j.ttbdis.2018.09.004Abierto DOISearch in Google Scholar
Bolio-González, M.E., Rodríguez-Vivas, R.I., Sauri-Arceo, C.H., Gutiérrez-Blanco, E., Ortega-Pacheco, A., Colin-Flores, R.F. (2007): Prevalence of the Dirofilaria immitis infection in dogs from Merida, Yucatan, Mexico. Vet Parasitol, 148(2): 166 – 169. DOI: 10.1016/j.vetpar.2007.05.019Bolio-GonzálezM.E.Rodríguez-VivasR.I.Sauri-ArceoC.H.Gutiérrez-BlancoE.Ortega-PachecoA.Colin-FloresR.F.2007Prevalence of the Dirofilaria immitis infection in dogs from Merida, Yucatan, MexicoVet Parasitol148216616910.1016/j.vetpar.2007.05.019Abierto DOISearch in Google Scholar
Caballero-Caballero E. (1948): Helminthological studies of the onchocercal region of Mexico and the Republic of Guatemala. Nematoda. 4th part Filarioidea. [Estudios helmintológicos de la región oncocercosa de México y de la República de Guatemala. Nematoda. 4ª parte Filarioidea.] An Inst Méx, 19(1): 137 – 151. (In Spanish)Caballero-CaballeroE.1948Helminthological studies of the onchocercal region of Mexico and the Republic of Guatemala. Nematoda. 4th part Filarioidea. [Estudios helmintológicos de la región oncocercosa de México y de la República de Guatemala. Nematoda. 4ª parte Filarioidea.]An Inst Méx191137151(In Spanish)Search in Google Scholar
Caro-González, J.A., Bolio-González, M.E., Escobedo-Ortegón, F.J., Manrique-Saide, P., Rodríguez-Vivas, R.I., Rodríguez-Buenfil, J.C., Sauri-Arceo, C.H. (2011): Prevalence of Dirofilaria immitis infection in dogs from Celestun, Mexico, using polymerase chain reaction test. Vector Borne Zoonotic Dis, 11(2): 193 – 196. DOI: 10.1089/vbz.2009.0171Caro-GonzálezJ.A.Bolio-GonzálezM.E.Escobedo-OrtegónF.J.Manrique-SaideP.Rodríguez-VivasR.I.Rodríguez-BuenfilJ.C.Sauri-ArceoC.H.2011Prevalence of Dirofilaria immitis infection in dogs from Celestun, Mexico, using polymerase chain reaction testVector Borne Zoonotic Dis11219319610.1089/vbz.2009.0171Abierto DOISearch in Google Scholar
Christensen, B.M., Shelton, M.E. (1978): Laboratory observations on the insusceptibility of raccoons to Dirofilaria immitis. J Wild Dis, 14(1): 22 – 23. DOI: 10.7589/0090-3558-14.1.22ChristensenB.M.SheltonM.E.1978Laboratory observations on the insusceptibility of raccoons to Dirofilaria immitisJ Wild Dis141222310.7589/0090-3558-14.1.22Abierto DOISearch in Google Scholar
Dantas-Torres, F., Otranto, D. (2013): Dirofilariosis in the Americas: a more virulent Dirofilaria immitis? Parasit Vectors, 6(1): 288 – 296. DOI: 10.1186/1756-3305-6-288Dantas-TorresF.OtrantoD.2013Dirofilariosis in the Americas: a more virulent Dirofilaria immitis?Parasit Vectors6128829610.1186/1756-3305-6-288Abierto DOISearch in Google Scholar
Figuerêdo Duarte Moraes, M., de Souza Pollo, A., Lux Hoppe, E.G. (2022): Filarids (Spirurida: Onchocercidae) in wild carnivores and domestic dogs from the Brazilian Atlantic Forest. PLoS Negl Trop Dis, 16(3): e0010213. DOI: 10.1371/journal.pntd.0010213Figuerêdo Duarte MoraesM.de Souza PolloA.Lux HoppeE.G.2022Filarids (Spirurida: Onchocercidae) in wild carnivores and domestic dogs from the Brazilian Atlantic ForestPLoS Negl Trop Dis163e001021310.1371/journal.pntd.0010213Abierto DOISearch in Google Scholar
Kotwa, J.D., Jardine, C.M., Berke, O., Pearl, D.L., Mercer, N.J., Peregrine, A.S. (2019): Prevalence and distribution of Dirofilaria immitis infection in wild canids in southern Ontario. Vet Parasitol Reg Stud Reports, 18: 100349. DOI: 10.1016/j.vprsr.2019.100349KotwaJ.D.JardineC.M.BerkeO.PearlD.L.MercerN.J.PeregrineA.S.2019Prevalence and distribution of Dirofilaria immitis infection in wild canids in southern OntarioVet Parasitol Reg Stud Reports1810034910.1016/j.vprsr.2019.100349Abierto DOISearch in Google Scholar
Mancebo, O., Russo, A., Bulman, G., Carabajal, L., Villavicencio de Mancebo, V. (1992): Dirofilaria immitis: Characteristics, prevalence and diagnosis of heartworm in the canine population in urban, suburban and rural areas of the Province of Formosa (Argentina) and description of the disease in the common coati (Nasua solitaria). [Dirofilaria immitis: Características, prevalencia y diagnóstico de la dirofilariasis en la población canina en áreas urbanas, suburbanas y rurales de la Prov. de Formosa (Argentina) y descripción de la enfermedad en el coatí común (Nasua solitaria).] Pet's, 8: 95 – 117 (In Spanish)ManceboO.RussoA.BulmanG.CarabajalL.Villavicencio de ManceboV.1992Dirofilaria immitis: Characteristics, prevalence and diagnosis of heartworm in the canine population in urban, suburban and rural areas of the Province of Formosa (Argentina) and description of the disease in the common coati (Nasua solitaria). [Dirofilaria immitis: Características, prevalencia y diagnóstico de la dirofilariasis en la población canina en áreas urbanas, suburbanas y rurales de la Prov. de Formosa (Argentina) y descripción de la enfermedad en el coatí común (Nasua solitaria).]Pet's895117(In Spanish)Search in Google Scholar
Manrique-Saide, P., Bolio-González, M., Sauri-Arceo, C., Dzib-Florez, S., Zapata-Peniche, A. (2008): Ochlerotatus taeniorhynchus: a probable vector of Dirofilaria immitis in coastal areas of Yucatan, Mexico. J Med Entomol, 45(1): 169 – 171. DOI: 10.1603/0022-2585(2008)45[169:otapvo]2.0.co;2Manrique-SaideP.Bolio-GonzálezM.Sauri-ArceoC.Dzib-FlorezS.Zapata-PenicheA.2008Ochlerotatus taeniorhynchus: a probable vector of Dirofilaria immitis in coastal areas of Yucatan, MexicoJ Med Entomol45116917110.1603/0022-2585(2008)45[169:otapvo]2.0.co;2Abierto DOISearch in Google Scholar
Manrique-Saide, P., Escobedo-Ortegón, J., Bolio-González, M., Sauri-Arceo, C., Dzib-Florez, S., Guillermo-May, G., Ceh-Pavía, E., Lenhart, A. (2010): Incrimination of the mosquito, Aedes taeniorhynchus, as the primary vector of heartworm, Dirofilaria immitis, in coastal Yucatan, Mexico. Med Vet Entomol, 24(4): 456 – 460. DOI: 10.1111/j.1365-2915.2010.00884.xManrique-SaideP.Escobedo-OrtegónJ.Bolio-GonzálezM.Sauri-ArceoC.Dzib-FlorezS.Guillermo-MayG.Ceh-PavíaE.LenhartA.2010Incrimination of the mosquito, Aedes taeniorhynchus, as the primary vector of heartworm, Dirofilaria immitis, in coastal Yucatan, MexicoMed Vet Entomol24445646010.1111/j.1365-2915.2010.00884.xAbierto DOISearch in Google Scholar
Mazza, S. (1926): On a coati heart filarid (Dirofilaria nasuae n. sp.). [Sobre un filarídeo del corazón de coatí (Dirofilaria nasuae n. sp.)] Bol Inst Clin Quir, 2: 273 – 279 (In Spanish)MazzaS.1926On a coati heart filarid (Dirofilaria nasuae n. sp.). [Sobre un filarídeo del corazón de coatí (Dirofilaria nasuae n. sp.)]Bol Inst Clin Quir2273279(In Spanish)Search in Google Scholar
Moraes, M.F.D., da Silva, M.X., Magalhães-Matos, P.C., de Albuquerque, A.C.A., Tebaldi, J.H., Mathias, L.A., Lux Hoppe, E.G. (2017): Filarial nematodes with zoonotic potential in ring-tailed coatis (Nasua nasua Linnaeus, 1766, Carnivora: Procyonidae) and domestic dogs from Iguaçu National Park, Brazil. Vet Parasitol Reg Stud Reports, 8: 1 – 9. DOI: 10.1016/j.vprsr.2017.01.003MoraesM.F.D.da SilvaM.X.Magalhães-MatosP.C.de AlbuquerqueA.C.A.TebaldiJ.H.MathiasL.A.Lux HoppeE.G.2017Filarial nematodes with zoonotic potential in ring-tailed coatis (Nasua nasua Linnaeus, 1766, Carnivora: Procyonidae) and domestic dogs from Iguaçu National Park, BrazilVet Parasitol Reg Stud Reports81910.1016/j.vprsr.2017.01.003Abierto DOISearch in Google Scholar
Moroni, B., Rossi, L., Meneguz, P.G., Orusa, R., Zoppi, S., Robetto, S., Marucco, F., Tizzani, P. (2020): Dirofilaria immitis in wolves recolonizing northern Italy: are wolves competent hosts? Parasit Vectors, 13(1): 482. DOI: 10.1186/s13071-020-04353-2MoroniB.RossiL.MeneguzP.G.OrusaR.ZoppiS.RobettoS.MaruccoF.TizzaniP.2020Dirofilaria immitis in wolves recolonizing northern Italy: are wolves competent hosts?Parasit Vectors13148210.1186/s13071-020-04353-2Abierto DOISearch in Google Scholar
Mullin, P.G., Harryis, T.S., Powers, T.O. (2005): Phylogenetic relationships of Nygolaimina and Dorylaimina (Nematoda: Dorylaimida) inferred from small subunit ribosomal DNA sequences. Nematology, 7(1), 59 – 79. DOI: 10.1163/1568541054192199MullinP.G.HarryisT.S.PowersT.O.2005Phylogenetic relationships of Nygolaimina and Dorylaimina (Nematoda: Dorylaimida) inferred from small subunit ribosomal DNA sequencesNematology71597910.1163/1568541054192199Abierto DOISearch in Google Scholar
Panti-May, J.A., Torres-Castro, M., Hernández-Betancourt, S., Dzul-Rosado, K., Zavala-Castro, J., López-Avila, K., Tello-Martín, R. (2015): Detection of Rickettsia felis in wild mammals from three municipalities in Yucatan, Mexico. Ecohealth, 12(3): 523 – 527. DOI: 10.1007/s10393-014-1003-2Panti-MayJ.A.Torres-CastroM.Hernández-BetancourtS.Dzul-RosadoK.Zavala-CastroJ.López-AvilaK.Tello-MartínR.2015Detection of Rickettsia felis in wild mammals from three municipalities in Yucatan, MexicoEcohealth12352352710.1007/s10393-014-1003-2Abierto DOISearch in Google Scholar
Panti-May, J.A., Hernández-Mena, D.I., Ruiz-Piña, H.A., Torres-Castro, M.A., Hernández-Betancourt, S.F., Vidal-Martínez, V.M. (2021): Morphological and molecular identification of nematodes in the tayra Eira barbara from Campeche, Mexico. Helminthologia, 58(3): 315 – 322. DOI: 10.2478/helm-2021-0034Panti-MayJ.A.Hernández-MenaD.I.Ruiz-PiñaH.A.Torres-CastroM.A.Hernández-BetancourtS.F.Vidal-MartínezV.M.2021Morphological and molecular identification of nematodes in the tayra Eira barbara from Campeche, MexicoHelminthologia58331532210.2478/helm-2021-0034Abierto DOISearch in Google Scholar
Penezić, A., Selaković, S., Pavlović, I., Ćirović, D. (2014): First findings and prevalence of adult heartworms (Dirofilaria immitis) in wild carnivores from Serbia. Parasitol Res, 113(9): 3281 – 3285. DOI: 10.1007/s00436-014-3991-9PenezićA.SelakovićS.PavlovićI.ĆirovićD.2014First findings and prevalence of adult heartworms (Dirofilaria immitis) in wild carnivores from SerbiaParasitol Res11393281328510.1007/s00436-014-3991-9Abierto DOISearch in Google Scholar
Santoro, M., Miletti, G., Vangone, L., Spadari, L., Reccia, S., Fusco, G. (2019): Heartworm Disease (Dirofilaria immitis) in two roaming dogs from the urban area of Castel Volturno, Southern Italy. Front Vet Sci, 6: 270 – 274. DOI: 10.3389/fvets.2019.00270SantoroM.MilettiG.VangoneL.SpadariL.RecciaS.FuscoG.2019Heartworm Disease (Dirofilaria immitis) in two roaming dogs from the urban area of Castel Volturno, Southern ItalyFront Vet Sci627027410.3389/fvets.2019.00270Abierto DOISearch in Google Scholar
Simón, F., Siles-Lucas, M., Morchón, R., González-Miguel, J., Mellado, I., Carretón, E., Montoya-Alonso, J.A. (2012): Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clin Microbiol Rev, 25(3): 507 – 544. DOI: 10.1128/CMR.00012-12SimónF.Siles-LucasM.MorchónR.González-MiguelJ.MelladoI.CarretónE.Montoya-AlonsoJ.A.2012Human and animal dirofilariasis: the emergence of a zoonotic mosaicClin Microbiol Rev25350754410.1128/CMR.00012-12Abierto DOISearch in Google Scholar
Snyder, D.E., Hamir, A.N., Hanlon, C.A., Rupprecht, C.E. (1989): Dirofilaria immitis in a raccoon (Procyon lotor). J Wildl Dis, 25(1): 130 – 131. DOI: 10.7589/0090-3558-25.1.130SnyderD.E.HamirA.N.HanlonC.A.RupprechtC.E.1989Dirofilaria immitis in a raccoon (Procyon lotor).J Wildl Dis25113013110.7589/0090-3558-25.1.130Abierto DOISearch in Google Scholar
Sosa-Bibiano, E.I., Sánchez-Martínez, L.A., López-Ávila, K.B., Chablé-Santos, J.B., Torres-Castro, J.R., Fernández-Figueroa, E.A., Rangel-Escareño, C., Loría-Cervera, E.N. (2022): Leishmania (Leishmania) mexicana infection in wild rodents from an emergent focus of cutaneous Leishmaniasis in Yucatan, Mexico. J Trop Med, 2022: 8392005. DOI: 10.1155/2022/8392005Sosa-BibianoE.I.Sánchez-MartínezL.A.López-ÁvilaK.B.Chablé-SantosJ.B.Torres-CastroJ.R.Fernández-FigueroaE.A.Rangel-EscareñoC.Loría-CerveraE.N.2022Leishmania (Leishmania) mexicana infection in wild rodents from an emergent focus of cutaneous Leishmaniasis in Yucatan, MexicoJ Trop Med2022839200510.1155/2022/8392005Abierto DOISearch in Google Scholar
Sosa-Escalante, J.E., Pech-Canché, J.M., Mac Swiney, M.C., Hernández-Betancourt, S. (2013): Terrestrial mammals of the Yucatan peninsula, Mexico: richness, endemism and risk. [Mamíferos terrestres de la península de Yucatán, México: riqueza, endemismo y riesgo.] Rev Mex Biodiversidad, 84(3): 949 – 969. DOI: 10.7550/rmb.33285 (In Spanish)Sosa-EscalanteJ.E.Pech-CanchéJ.M.Mac SwineyM.C.Hernández-BetancourtS.2013Terrestrial mammals of the Yucatan peninsula, Mexico: richness, endemism and risk. [Mamíferos terrestres de la península de Yucatán, México: riqueza, endemismo y riesgo.]Rev Mex Biodiversidad84394996910.7550/rmb.33285(In Spanish)Abierto DOISearch in Google Scholar
Torres-Castro, M., Muñoz-Dueñas, D., Hernández-Betancourt, S., Bolio-González, M., Noh-Pech, H., Peláez-Sánchez, R., Sosa-Escalante, J. (2019): Infection with Toxoplasma gondii (Eucoccidiorida: Sarcocystidae) in bats of Campeche and Yucatán, Mexico. [Infección con Toxoplasma gondii (Eucoccidiorida: Sarcocystidae) en murciélagos de Campeche y Yucatán, México.] Rev Biol Trop, 67(3): 633 – 642. DOI: 10.15517/RBT.V67I2.35147 (In Spanish)Torres-CastroM.Muñoz-DueñasD.Hernández-BetancourtS.Bolio-GonzálezM.Noh-PechH.Peláez-SánchezR.Sosa-EscalanteJ.2019Infection with Toxoplasma gondii (Eucoccidiorida: Sarcocystidae) in bats of Campeche and Yucatán, Mexico. [Infección con Toxoplasma gondii (Eucoccidiorida: Sarcocystidae) en murciélagos de Campeche y Yucatán, México.]Rev Biol Trop67363364210.15517/RBT.V67I2.35147(In Spanish)Abierto DOISearch in Google Scholar
Torres-Castro, M., Febles-Solís, V., Hernández-Betancourt, S., Noh-Pech, H., Estrella, E., Peláez-Sánchez, R., Panti-May, A., Herrera-Flores, B., Reyes-Hernández, B., Sosa-Escalante, J. (2020): Pathogenic Leptospira in bats from Campeche and Yucatán, Mexico [Leptospira patógenas en murciélagos de Campeche y Yucatán, México.] Rev MVZ Córdoba, 25(2): e1815. DOI: 10.21897/rmvz.1815 (In Spanish)Torres-CastroM.Febles-SolísV.Hernández-BetancourtS.Noh-PechH.EstrellaE.Peláez-SánchezR.Panti-MayA.Herrera-FloresB.Reyes-HernándezB.Sosa-EscalanteJ.2020Pathogenic Leptospira in bats from Campeche and Yucatán, Mexico [Leptospira patógenas en murciélagos de Campeche y Yucatán, México.]Rev MVZ Córdoba252e181510.21897/rmvz.1815(In Spanish)Abierto DOISearch in Google Scholar
Torres-Castro, M., Cuevas-Koh, N., Hernández-Betancourt, S., Noh-Pech, H., Estrella, E., Herrera-Flores, B., Panti-May, J. A., Waleckx, E., Sosa-Escalante, J., Peláez-Sánchez, R. (2021). Natural infection with Trypanosoma cruzi in bats captured in Campeche and Yucatán, México. Biomedica, 41(Supl1): 131 – 140. DOI: 10.7705/biomedica.5450Torres-CastroM.Cuevas-KohN.Hernández-BetancourtS.Noh-PechH.EstrellaE.Herrera-FloresB.Panti-MayJ. A.WaleckxE.Sosa-EscalanteJ.Peláez-SánchezR.2021Natural infection with Trypanosoma cruzi in bats captured in Campeche and Yucatán, MéxicoBiomedica41Supl113114010.7705/biomedica.5450Abierto DOISearch in Google Scholar
Torres-Castro, M., Reyes-Novelo, E., Bolio-González, M., Lugo-Caballero, C., Dzul-Rosado, K., Colunga-Salas, P., Sánchez-Montes, S., Noh-Pech, H., Puerto, F.I., Rodríguez-Vivas, R.I. (2022): Epidemiological study of the occurrence of typhus group Rickettsia natural infection in domiciliated dogs from a rural community in south-eastern Mexico. Animals (Basel), 12 (20): 2885. DOI: 10.3390/ani12202885Torres-CastroM.Reyes-NoveloE.Bolio-GonzálezM.Lugo-CaballeroC.Dzul-RosadoK.Colunga-SalasP.Sánchez-MontesS.Noh-PechH.PuertoF.I.Rodríguez-VivasR.I.2022Epidemiological study of the occurrence of typhus group Rickettsia natural infection in domiciliated dogs from a rural community in south-eastern MexicoAnimals (Basel)1220288510.3390/ani12202885Abierto DOISearch in Google Scholar
Vezzani, D., Eiras, D.F., Wisnivesky, C. (2006): Dirofilariasis in Argentina: historical review and first report of Dirofilaria immitis in a natural mosquito population. Vet Parasitol, 136(3–4): 259 – 273. DOI: 10.1016/j.vetpar.2005.10.026VezzaniD.EirasD.F.WisniveskyC.2006Dirofilariasis in Argentina: historical review and first report of Dirofilaria immitis in a natural mosquito populationVet Parasitol1363–425927310.1016/j.vetpar.2005.10.026Abierto DOISearch in Google Scholar
Worsley-Tonks, K.E.L., Gehrt, S.D., Anchor, C., Escobar, L.E., Craft, M.E. (2021): Infection risk varies within urbanized landscapes: the case of coyotes and heartworm. Parasit Vectors, 14(1): 464. DOI: 10.1186/s13071-021-04958-1Worsley-TonksK.E.L.GehrtS.D.AnchorC.EscobarL.E.CraftM.E.2021Infection risk varies within urbanized landscapes: the case of coyotes and heartwormParasit Vectors14146410.1186/s13071-021-04958-1Abierto DOISearch in Google Scholar
