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).
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.
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).
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.
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