Canine heartworm: natural infection along remote coastal area of Rio de Janeiro Dirofilariose canina: infecção natural ao longo de área costeira remota do Rio de Janeiro

Copyright Santos Filho et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License which permits unrestricted non-commercial use, distribution, and reproduction in any medium provided the original work is properly cited. Canine heartworm: natural infection along remote coastal area of Rio de Janeiro Dirofilariose canina: infecção natural ao longo de área costeira remota do Rio de Janeiro

In Brazil, D. immitis is one of the most prevalent arthropod-borne disease in dogs, with an approximate prevalence of 23.1% (Labarthe et al., 2014). Rio de Janeiro is a coastal state and has a favorable climate for vector mosquitoes to develop (Bendas et al., 2019). The prevalence of infected dogs varies according to the region due to climate and population characteristics. Examples of this variation in prevalence can be seen in the following cities: Armação dos Búzios (62.2%), Niterói (58.6%), Cabo Frio (27.5%) and Mangaratiba (16.3%) (Labarthe et al., 2014).
Different mosquito species have been reported as heartworm disease vectors in Rio de Janeiro. Ochletotatus taeniorhynchus and Ochletotatus scapularis were identified as possible vectors in the coastal lowlands of Rio de Janeiro (Lourenço-de-Oliveira & Deane, 1995) and have been subsequently confirmed as primary heartworm vectors (Labarthe et al., 1998b). In the same area, Culex quinquefasciatus was considered as secondary vector (Labarthe et al., 1998b). Aedes aegypti from Rio de Janeiro presents vectorial competence for heartworm disease (Serrão et al., 2001). However, its epidemiological role in the transmission of the disease in Rio de Janeiro remains to be clarified.
Infected animals can be asymptomatic or demonstrate symptoms related to the presence of the parasites (Bowman & Atkins, 2009). These symptoms can be mild, such as coughing and reduced physical activity. When left untreated, symptoms may progress to dyspnea, syncope, congestive heart failure and even death (Atwell et al., 1988).
Heartworm infection is confirmed by the detection and identification of microfilariae or by the detection of the D. immitis antigen in blood samples (American Heartworm Society, 2020). The presence of D. immitis in infected dogs signals the presence of mosquito vectors. These mosquito species may vector heartworm or other pathogens to different host species, including humans. Therefore, a heartworm-infected dog may be a useful sentinel to warn of human mosquito-borne health hazards (Cancrini et al., 2003;Gratz, 2004;Mitchell, 1995). The concept of One Health in Veterinary Science represents more than just the impact of zoonoses on human health; it should be deeply considered and studied in a broader perspective. The presence of infected animals with pathogens vectored by eclectic mosquitoes that may vector human pathogens highlights this concept (Backer & Miller, 2016;Racloz et al., 2006;Schmidt, 2009).
In order to identify the presence of an infection where it is infrequent and neglected and to show the importance of canine heartworm surveillance, two autochthonous cases of canine heartworm disease occurred in Seropédica, Rio de Janeiro, Brazil, are described.

Patient 1
A 2-year-old mixed breed intact male dog presented for clinical care at the small animal veterinary hospital of the Universidade Federal Rural do Rio de Janeiro in November 2016. The patient was presented for a routine check-up. The pet's owner reported that the animal had lived outdoors in Seropédica (22°44'29.3"S 43°42'03.5"W) (Figure 1), since he was born and had never traveled elsewhere. The dog was in good health. Upon pulmonary auscultation, harsh expiratory sounds were detected. Thoracic radiographs and blood work (complete blood cell counts, clinical biochemistry, microfilariae and heartworm antigen tests) were performed. The dog tested positive for microfilariae and heartworm antigens. No other changes were observed in blood work. X-rays showed slight bronchial and interstitial patterns suggesting bronchopathy. After diagnosis of the heartworm infection, echocardiography was performed, and it revealed the presence of parallel lines in the main pulmonary artery, further confirming infection with D. immitis.

Patient 2
A 7-year-old German Shepherd intact male dog presented at the small animal veterinary hospital of the Universidade Federal Rural do Rio de Janeiro in October 2017 for preoperative evaluation of a lump in the paw. At this visit, microfilariae were detected as a result of cytology. The owner reported that the animal lived outdoors in Seropédica (22°44'10.7"S 43°41' 44.4"W) (Figure 1), had contact with free-roaming dogs, and had never been taken elsewhere. During thoracic auscultation, a grade I/VI murmur in the mitral area and harsh respiratory sounds were detected. According to the pet's owner, the patient experienced sporadic episodes of coughing, but never showed signs of dyspnea. The dog tested positive for D. immitis antigen, but no microfilariae were detected. A diffuse bronchial pattern was detected on radiography, and Doppler echocardiography showed the presence of parallel lines in the main pulmonary artery, which further confirmed infection with D. immitis.

Discussion
The municipality of Seropédica is part of the Metropolitan region of Rio de Janeiro, RJ. Canine heartworm infection is known to occur in most districts of the city of Rio de Janeiro (Labarthe et al., 1997), although there are information gaps in other areas of the municipality. Seropédica is one of those areas where no survey has been conducted.
Seropédica shares a tropical climate with Rio de Janeiro city (Lohmann et al., 1993), is only 20 km away from the Atlantic Ocean, and is adjacent to Mário Xavier National Forest. Despite having similar environmental characteristics as the Rio de Janeiro lowlands, where canine infections are frequent (prevalence ranges from 2.7% to 58.6%) (Labarthe et al., 1997(Labarthe et al., , 2014, and having a Veterinary School, canine heartworm infection has received little attention (Genchi & Kramer, 2020).
Many environmental changes, including urban improvements that have impacted the national forest, have taken place in the past 10 years (Farias et al., 2020). It is reasonable to expect that these impacts would have diminished the natural vector population density and, as a consequence, reduced heartworm prevalence (Clements, A. N., 1999). Paradoxically, the number of opportunistic heartworm cases reported here suggests that the canine infection rate has increased (Traversa, D. et al., 2010). Therefore, other factors may be important and must be identified.
Canine population mobility is part of the modern way of life. Therefore, it would not be surprising to learn that the students of the local university travel back and forth between Seropédica and endemic areas with their dogs unprotected (Alirol et al., 2011) . This behavior is known to spread heartworm disease to naive neighborhoods (American Heartworm Society [AHS], 2020). Another factor to be considered is environmental disturbances in nearby forests. Since the most efficient heartworm vector mosquito species in Rio de Janeiro lowlands are known to be the sylvatic Ochlerotatus taeniorhynchus and Ochlerotatus scapularis (Labarthe et al., 1998a;Macêdo et al., 1998), environmental changes that have occurred in the forest may have displaced those vectors, forcing them to colonize new areas.
In addition, global warming favors mosquitoes, allowing them to produce higher numbers of new generations over a given time, thereby increasing local population density (Campbell-Lendrum et al., 2015). As environmental temperatures rise, the heartworm extrinsic cycle is accelerated, resulting in more efficacious and faster transmission (Carvalho et al., 2002;Christensen & Hollander, 1978;Knight & Lok, 1998;Ferreira, A. F. et al., 1999).
Other mosquito synanthropic species that may play a vector role in this geographic area are Aedes aegypti and Aedes albopictus. Although their heartworm vector capacity throughout Brazil is unknown, both species are endemic in Seropédica (Sanavria et al., 2017), and they have been shown to naturally vector heartworm in different areas of the world (Ahid & Lourenço-de-Oliveira, 1999;Cancrini et al., 2003;Comiskey & Wesson, 1995;Ledesma & Harrington, 2011;Nayar & Knight, 1999;Serrão et al., 2001).
Once these variables are considered, the presence of microfilaremic dogs, high density of competent synanthropic vector mosquito populations, and unprotected dogs exposed to the mosquitoes, it can be suggested that heartworm is becoming native to the area.
In an area where canine heartworm disease is rare, clinical signs may be misinterpreted when they are unspecific. In Seropédica, where both dogs described above have lived all their lives, one was 2-year-old that had the infection detected because he was presented with harsh lung sounds. This finding is rare at such a young age (Rozanski, 2020), although frequent in canine heartworm infections (Alberigi et al., 2020;Bowman & Atkins, 2009). The older heartworm-infected dog presented would have gone undetected if microfilariae had not been present in the cytology, and his clinical signs could have been misinterpreted as senile bronchitis (Rozanski, 2020).
Considering that the socioeconomic condition of the residents of Seropédica is poor, resources there are focused mainly on human needs (Silva et al., 2020). Therefore, pet infection prophylaxis is often not maintained, leaving animals to become potential reservoirs of parasites that may be a threat to human health.
These factors highlight the need for continuous surveillance of canine infections, keeping in mind that biomes are mistreated constantly, and that pets may be good hazard sentinels. Nature changes as a reaction to insults, repeatedly eliciting new life cycle characteristics that may impact human and non-human animal well-being. Therefore, veterinarians need to be updated and diligently work to prevent and detect infections such as heartworm disease.

Conclusion
These two case reports demonstrate that infection with D. immitis can occur even in places where it is not usually found, provided that there are favorable climatic conditions for the presence of vectors and hosts. In these environments, veterinarians must prioritize diagnosis and prevention of infections.