Canine vector-borne pathogens from dogs and ticks from Tamil Nadu, India
Introduction
Canine vector-borne diseases (CVBDs) are a group of diseases transmitted by several arthropod vectors, including fleas, biting and secretophagous flies, mosquitoes, sand flies and, especially, ticks (Otranto et al., 2009). In the past two decades, the distribution of CVBDs has been investigated mainly in industrialized countries of the northern hemisphere, whereas data about the occurrence and the impact of these infections in developing countries is minimal (Maggi and Kramer, 2019). India has a population of about 118 million dogs, though no reliable information is available on the exact number of stray dogs in this country (Wallace et al., 2017). Scientific data indicates that the gross domestic product per capita is, at global level, inversely proportional to the percentage of stray dogs making the burden of zoonotic parasites linked to poverty (Otranto et al., 2017). For long time, capture-neuter-vaccinate-release (CVNR) programs were endorsed by the WHO in India (Jackaman and Rowan, 2007). Nonetheless, during economic crisis these programs often do not reach a large proportion of stray dogs (Otranto et al., 2017), making these animals suitable reservoirs of several parasites of zoonotic concern (Traub et al., 2014; Sudan et al., 2015). At these conditions, untreated animals play an important role in the maintenance of tick populations such as the brown dog tick, Rhipicephalus sanguineus sensu lato (s.l.), representing a risk for the transmission of zoonotic tick-borne pathogens (Otranto et al., 2010; Dantas-Torres et al., 2012). Indeed, R. sanguineus s.l. is the most common tick species parasitizing dogs of India (Raut et al., 2006; Abd Rani et al., 2011; Sahu et al., 2013) followed by Rhipicephalus haemaphysaloides, Rhipicephalus microplus, Haemaphysalis longicornis and Haemaphysalis bispinosa (Sahu et al., 2013; Augustine et al., 2017). All of these tick species act as vectors for pathogens causing babesiosis, ehrlichiosis, hepatozoonosis and anaplasmosis (Abd Rani et al., 2011; Augustine et al., 2017; Geurden et al., 2018). In particular, babesioses by Babesia vogeli and Babesia gibsoni are evenly distributed in India due to the presences of their vectors R. sanguineus s.l. and H. longicornis, respectively (Abd Rani et al., 2011). Among Ehrlichia spp., Ehrlichia canis is the most common in canine populations of tropics and sub tropics (Shaw et al., 2001). Anaplasmosis is a prevalent disease affecting both humans and animals (Demma et al., 2005; Nicholson et al., 2010), with Anaplasma phagocytophilum and Anaplasma platys being potentially zoonotic (Maggi et al., 2013; Arraga-Alvarado et al., 2014; Vlahakis et al., 2018). Rhipicephalus sanguineus s.l. is the putative vector of A. platys (Inokuma et al., 2000), a pathogen which may infect humans (Maggi et al., 2013; Arraga-Alvarado et al., 2014), whilst Ixodes spp. act as vector of A. phagocytophilum (Parola et al., 2005). Although, Ixodes spp. have been reported from the temperate zones of Europe, Asia and North America (Parola et al., 2005), few studies described the presence of different Ixodes species (i.e., Ixodes acutitarsus and Ixodes ricinus) in different parts of India (Kaul et al., 1990; Ronghang et al., 2016). Canine hepatozoonosis is a tick-borne disease prevalent in various regions of India (Chhabra et al., 2013) with prevalence, at blood smear examination, of 11.23% for Hepatozoon canis in Tamil Nadu (Vairamuthu et al., 2014). Apart from tick-borne diseases, canine dirofilarioses are prevalent in India (Abd Rani et al., 2010) and an increasing number of Dirofilaria immitis and Dirofilaria repens infection have also been reported in human patients (Sabu et al., 2005). Leishmania donovani and Leishmania infantum cause visceral leishmaniasis (VL) in humans worldwide. Whilst L. donovani is anthroponotic, L. infantum is the main etiologic agent of zoonotic canine leishmaniosis (Costa, 2011; Ribeiro et al., 2018; Colella et al., 2019). In India, it is still not clear the role of dogs in the occurrence of cases of human leishmaniasis.
Global occurrence of ticks and their ability to cause diseases in dogs and transmit zoonotic pathogens warrant the regular screening of dogs for tick infestation. As dogs live in close proximity to humans, tick collection is advocated in order to screen both dogs and ticks for the presence of zoonotic tick-borne pathogens (Shaw et al., 2001; Baneth, 2004; Otranto et al., 2014). Due to the limited number of scientific articles in the international literature available on CVBDs in feral/stray dogs from India (Irwin et al., 2004; Abd Rani et al., 2010), this study aimed to assess the occurrence of ticks, pathogens they may carry and CVBD-causing agents in dogs from Tamil Nadu, India.
Section snippets
Sampling procedures
From October to December 2018, a total of 230 free-ranging dogs were visited as a part of CVNR program (Fig. 1) and none of dogs exhibited apparent clinical signs. Dogs were located in four different areas of Chennai, Tamil Nadu (i.e., Pulianthope and Vepery in North Chennai - 13° 8′ 39.9948′′ N and 79° 53′ 38.4180′′ E; Velachery and Adyar in South Chennai - 12° 50′ 3.0264′′ N and 79° 42′ 13.1184′′ E) and their categorical age, sex and breed data were recorded. Each dog was checked for ticks
Results
Of the 230 dogs examined, 229 (99.6%; 95% CI: 97.51–99.9) were infested by ticks with a mean intensity of 5.6 (95% CI: 5.2–6.1). From a total of 1294 ticks collected, 1230 (95%) were adults (i.e., 644 males and 586 females), 62 (4.8%) nymphs and 2 larvae. Ticks were morphologically identified as R. sanguineus s.l. (98.3%) and R. haemaphysaloides (1.7%) (Fig. 2), being six animals (2.6%) coinfested with both species.
Data on sex, age and breed of sampled animals are reported in Table 2 along with
Discussion
Data from the current study suggests that ticks and tick-borne pathogens are highly prevalent among stray dogs in South India, posing a risk to humans. The hot and humid tropical climate conditions of South India, especially in Tamil Nadu, represent an ideal environment for the survival and propagation of ticks and tick-borne pathogens (Patra et al., 2018). Indeed, this geographical area is characterized by a moderate winter, with an average temperature of 26–29 °C and relative humidity of
Conclusions
Despite the worldwide distribution of H. canis and A. platys, limited information is available on the genetic diversity of these parasites. Similarly, the vectorial role of R. sanguineus s.l. for A. platys and A. phagocytophilum has not been thoroughly explored. These data fill gaps in the knowledge of canine vector-borne pathogens among stray dogs in South India including the first report of B. malayi, A. phagocytophilum and D. sp. “hongkongensis” from the state of Tamil Nadu. High prevalence
Funding sources
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Declaration of Competing Interest
The authors declare no competing interest.
References (85)
- et al.
A survey of canine tick-borne diseases in India
Parasit. Vectors
(2011) - et al.
Canine vector borne diseases in India: a review of the literature and identification of existing knowledge gap
Parasit. Vectors
(2010) - et al.
Case report: molecular evidence of Anaplasma platys infection in two women from Venezuela
Am. J. Trop. Med. Hyg.
(2014) - et al.
Molecular identification of Babesia spp. in naturally infected dogs of Kerala, South India
J. Parasitic Dis.
(2017) - et al.
Evaluation of multiplex PCR assay for detection of Babesia spp, Ehrlichia canis and Trypanosoma evansi in dogs
Acta Trop.
(2018) - et al.
Transmission of Hepatozoon canis to dogs by naturally fed or per cutaneously injected Ripicephalus sanguineus ticks
J. Parasitol.
(2001) Tick borne infections of animals and humans: a common ground invited review
Int. J. Parasitol.
(2004)- et al.
Molecular detection of Anaplasma platys infection in dogs in Chennai, Tamil Nadu, India. A pioneer report
J. Entomol. Zool. Stud.
(2017) - et al.
Geographic distribution of babesiosis among dogs in the United States and association with dog bites: 150 cases (2000–2003)
J. Am. Vet. Med. Assoc.
(2005) - et al.
Seroprevalence of canine dirofilariasis, granulocytic anaplasmosis and lyme borreliosis of public health importance in dogs from India´S North East
Vet. World
(2014)