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A Survey of Canine Filarial Diseases of Veterinary and Public Health Significance in India

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A Survey of Canine Filarial Diseases of Veterinary and Public Health Significance in India Megat Abd Rani et al. Parasites & Vectors 2010, 3:30 http://www.parasitesandvectors.com/content/3/1/30 RESEARCH Open Access A survey of canine filarial diseases of veterinary and public health significance in India Puteri Azaziah Megat Abd Rani1*, Peter J Irwin2, Mukulesh Gatne3, Glen T Coleman1, Linda M McInnes2, Rebecca J Traub1 Abstract Background: Dirofilaria spp., Acanthocheilonema spp. and Brugia spp. have all been reported in Indian dogs. In previous studies, diagnosis was made by morphological identification only. This is the first geographically stratified cross-sectional study in India to determine the prevalence and geographical distribution of canine filarial species of veterinary and public health importance, using a combination of conventional and molecular diagnostic techniques. Results: A total of 139 from 525 dogs (26.5%; 95% CI 22.7, 30.3) were positive for microfilariae. The most common species of canine filaria identified in this study was A. reconditum (9.3%) followed by D. repens (6.7%) and D. immitis (1.5%). Three out of 525 dogs were found to have mixed infections on PCR. The morphological and molecular evidence on the sequence of the 18S gene and phylogenetic analysis of the ITS-2 region provided strong evidence that the canine microfilariae discovered in the Himalayan city of Ladakh belong to a novel species of Acanthocheilonema. Two dogs in Ladakh were also found to have mixed infections of the novel species described above and a unique microfilaria which morphologically resembled Microfilaria auquieri Foley, 1921. Conclusions: At least six species of filarial nematode are now known to infect dogs in India, two of which were reported for the first time in this study. The study also confirms and extends the geographical distribution of canine heartworm (D. immitis) which overlaps with D. repens, emphasising the importance for veterinary clinicians and diagnostic laboratories to utilise immunodiagnostic tests that will not cross-react between those two filarial species. From a public health viewpoint, the distribution and prevalences of these nematodes warrant an appropriate prophylaxis to be administered to dogs. Background Diagnostic methods for filarial infections include isola- Filariasis in dogs is caused by several species of filariids. tion of adult worms followed by morphological identifi- Dirofilaria immitis, the most pathogenic canine filarid is cation, morphological observation of circulating responsible for heartworm disease in dogs. Both D. microfilariae by stained blood smears, direct wet smears, repens and Acanthocheilonema spp. develop into adult modified Knott’stechniqueandtheWylie’s filtration worms in the subcutaneous tissue resulting in skin technique [2,3]. Histochemical or immuno-histochemical nodules. Adults of Brugia spp. are usually recovered staining of circulating microfilariae has also been per- from the mandibular, retropharyngeal and axillary lym- formed [4-6]. Detection of circulating antigen with com- phatics. Most infections with D. repens, Acanthocheilo- mercial test kits is currently available and widely used nema spp. and Brugia spp. are of minimal veterinary for D. immitis [7,8]. Molecular diagnostic approaches clinical significance, however all canine filariae have the are also increasingly utilised for research and surveil- potential to infect humans and remain important from a lance purposes [9,10]. public health perspective [1,2]. In India, Dirofilaria spp., Acanthocheilonema spp. and Brugia spp., have all been reported in dogs [6,11-13]. Previous reports on filarial infections in India are sum- * Correspondence: [email protected] marisedinTable1.Basedontheselimitednumberof 1 School of Veterinary Science, The University of Queensland, Queensland studies, it is currently accepted that D. immitis is 4072, Australia © 2010 Megat Abd Rani et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Megat Abd Rani et al. Parasites & Vectors 2010, 3:30 Page 2 of 11 http://www.parasitesandvectors.com/content/3/1/30 Table 1 Previous reported prevalences of canine filarial medical and veterinary importance (and therefore the species in different location in India diseases they transmit) is highly dependent on climate Northeast India Southern India [17]. The study was stratified to include four climatic Mizoram Orissa Kolkata Kerala Karnataka zones of India. The locations of the places sampled n = 240 n=7 n = 3200 n = 160 n = 400 represent a unique climatic condition of their own, Dirofilaria immitis 34% 57% 3% 0% 0% based on information produced by The World Meteor- Dirofilaria repens 0% 14% 0% 7% 21% ological Organization [18]. Ladakh in India’sfarnorth *Data obtained from [52,29,24,30,6] (3000 m altitude), experiences a temperature that rarely exceeds 27°C in summer, while in winter tem- geographically restricted to India’s north-east and D. peratures drop to minus 20°C. Mumbai’s climate can repens to India’s south, with an overlapping area cen- be described as tropical with a high level of humidity. trally. There are no reports of D. immitis occurring else- The mean average temperature for Mumbai ranges where in India, despite anecdotal evidence to suggest its from 16°C during winter to 30°C in summer. The cli- occurrence in Delhi (Sharma, personal communication, mate of Delhi is a monsoon-influenced humid subtro- July 2008, Delhi). This accepted view is questionable as pical climate with average temperatures range from competent mosquito vectors for D. immitis,belonging 7°C during its dry winter to 39°C in summer. Sikkim’s to the genera Culex, Aedes and Anopheles, that also hap- climate can be described as subtropical highland with pen to act as vectors for D. repens, are present all over mild temperatures range from 25°C in summer to 4°C India [14]. Moreover, a case of human pulmonary dirofi- in winter [19]. lariasis due to D. immitis was reported in Mumbai in To facilitate the fieldwork, collaborations were estab- 1989 [15], which casts further doubt on its currently lished with Vets Beyond Borders, Jeevaashram, Krish- accepted geographical distribution. Recently, 16 out of naashram, Bombay Veterinary College and In Defence 75 microfilaraemic dogs were shown to harbour B. of Animals India. These organisations allowed us access malayi by researchers at the Kerala Agricultural Univer- to stray and refuge dogs through their Animal Birth sity’s College of Veterinary and Animal Sciences using Control (ABC) and rabies vaccination programs. In morphological and immunodiagnostic criteria [13]. these programs stray dogs are impounded, vaccinated, However, since B. ceylonensis is endemic in Sri Lanka surgically neutered and released back to their original this finding needs to be confirmed using PCR as the location [20]. The purpose of this program is to stabilise microfilariae cannot be differentiated morphologically the street dog population and to help control the spread from B. malayi and it is likely the ELISA test cross- of rabies. Capillary and whole blood samples were col- reacts among Brugia spp. [16]. lected from 525 dogs from four different cities (Figure In previous reported studies, microfilarial identifica- 1), namely Gangtok and Jorethang in Sikkim (n = 101), tion relied on morphological assessment only. Despite Ladakh (n = 100) in Jammu and Kashmir, Delhi (n = the availability of published measurements of various 162) and Mumbai (n = 162). Blood samples were sub- microfilariae, the inadequacy of morphological diagnosis jected to normal-thin and buffy-coat smears, air-dried was demonstrated by Rishniw and colleagues (2006) [9] and fixed in 100% ethanol and later stained with Giemsa when microfilariae initially identified as A. reconditum for microscopic screening. Whole blood samples were were later determined to be D. immitis by molecular also applied onto QIAcard FTA® Four Spots (Qiagen) methods. Morphological identification of microfilariae for molecular-based screening later. not only requires experienced personnel but it may be difficult to detect multiple infections with more than Microscopic examination of blood films one species of filarial worms [2]. Stained blood films were examined under ×200 and A geographically stratified cross-sectional study was ×400 objective lens for microfilariae. The microfilariae undertaken to determine the prevalence and geographi- were measured using Olympus BH-2 microscope (Japan) cal distribution of canine filarial species of veterinary calibrated eye micrometer and photographed using and public health importance in India using a combina- Olympus DP12 digital microscope camera (Japan). tion of conventional and molecular diagnostic techniques. DNA extraction of adult D. immitis and blood from QIAcard FTA® Methods DNA from an adult worm of D. immitis (courtesy of Study site Murdoch University) was extracted using the tissue India features a wide range of climatic zones, ranging sample protocol of the MasterPure DNA purification kit from montane (cold, wet alpine regions) and semi-arid (Epicentre) according to the manufacturer’s instructions regions to the wet tropics. The ecology of vectors of and utilised as a positive control for this study. Megat Abd Rani et al. Parasites & Vectors 2010, 3:30 Page 3 of 11 http://www.parasitesandvectors.com/content/3/1/30
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