Parasitic Pneumonia Caused by Paragonimus Spp. in a Wild Royal Bengal Tiger, Mysuru, South India
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J Parasit Dis (July-Sept 2019) 43(3):528–533 https://doi.org/10.1007/s12639-019-01112-8 SHORT COMMUNICATION Parasitic pneumonia caused by Paragonimus spp. in a wild Royal Bengal Tiger, Mysuru, South India 1 1 1 2 N. K. Dharanesha • M. Saminathan • P. Mamta • K. R. Ramesh • 3 4 4 K. J. Ananda • P. Giridhar • S. M. Byregowda Received: 17 January 2019 / Accepted: 29 March 2019 / Published online: 5 April 2019 Ó Indian Society for Parasitology 2019 Abstract Parasitic pneumonia induced by genus Parago- tegumental spines surrounded by connective tissue capsule nimus involves many species, which affects both humans as cystic encapsulation and numerous eggs in adjacent lung and animals and it is a food borne zoonotic disease. In this parenchyma. Necrosis and moderate fibrosis of lung par- report, we have described the gross and histopathological enchyma with infiltration of polymorphonuclear and findings of Paragonimus fluke infection in lungs of tiger. mononuclear inflammatory cells were observed around The postmortem examination of sub adult male wild tiger fluke as well as eggs. The squamous cell metaplasia of (Panthera tigris tigris) died in captivity was conducted, lining bronchial epithelium and atelectasis of alveoli were earlier which was rescued by Forest Department, Mysuru, also prominently seen. Karnataka, India. External examination of carcass revealed pale oral and conjunctival mucous membranes with sunken Keywords Paragonimus spp. Á Pneumonia Á eye balls. During necropsy, moderate congestion, consoli- Royal Bengal Tiger Á Metaplasia Á Mysuru dation and numerous transparent to dark encysted lesions were found in the parenchyma of all lobes of lungs visible grossly on pleural surface. Lungs were hemorrhagic with Introduction necrotic foci around the cysts. The incision of encysted lesions revealed the presence of flukes (2–3 in numbers) in Lung paragonimiasis is caused by several flukes of each cyst with brownish exudate. The lung tissues with Paragonimus genus, among these Paragonimus wester- lesions were collected in 10% formalin and haematoxylin mani is an imperative species which is involved in causa- and eosin staining was done for histopathological evalua- tion of potential food borne parasitic zoonotic disease and tion. The flukes were identified as Paragonimus spp. based it has been reported to affect around 22 million people on the morphology and micrometry. The histopathological across the world (Seco et al. 2011; Arellano et al. 2006). examination revealed presence of longitudinal sections of Paragonimus spp. is geographically distributed in Siberia, flukes in bronchial lumen (in pair) with tegument and Japan, Korea, China, Taiwan, Philippines, Indonesia, Malaysia, Thailand, Sri Lanka and India (Dharanesha et al. 2017). Human beings get infection by eating raw or & N. K. Dharanesha undercooked crayfishes (Cambaroides) and fresh water [email protected] crabs (Sinopotamon, Candidiopotamon, Sundathelphusa, 1 Division of Pathology, ICAR-Indian Veterinary Research Parathelphusa, Geohelphusa, and Ranguna), which harbor Institute, Izatnagar, Bareilly, Uttar Pradesh 243122, India encysted metacercariae in their muscle and gills and serve 2 Sri Chamarajendra Zoological Gardens, Mysuru, Karnataka, as second intermediate host in the life cycle of this fluke India (Liu et al. 2008). The immature flukes from intestine enter 3 Department of Veterinary Parasitology, Veterinary College, the abdominal cavity and cause mechanical injury to KVAFSU, Shivamogga 577204, India intestinal wall, liver, diaphragm and become adult in lungs. 4 Institute of Animal Health and Veterinary Biologicals, Even aberrant migration to ectopic locations like brain and KVAFSU, Hebbal, Bengaluru 560024, India myocardium occurs (Yokogawa et al. 1960; Madarame 123 J Parasit Dis (July-Sept 2019) 43(3):528–533 529 et al. 2009). Pigs and some smaller rodents have been snare. The large contusion wound with hemorrhages on left shown to act as paratenic hosts (Miyazaki and Hirose inner thigh at stifle joint was also noticed. Grossly, lungs 1976). The wild tigers may get infection by predating on showed congestion, consolidation, hemorrhage, areas of wild pigs or other animals which host this fluke and also by atelectasis and emphysematous changes. Trachea and ingestion of second intermediate hosts which harbor bronchi were moderately congested. Numerous transparent metacercariae. The epidemiological investigation in to dark encysted lesions were found in the parenchyma of Sumatra, Indonesia, among 10 infected tigers revealed all lung lobes which were visible on pleural surface 1596 flukes in lungs of one tiger (Kwo and Miyazaki (Fig. 1a). The extent of lesion was severe and all the lobes 1968). In India, most cases of pulmonary paragonimiasis in both right and left lungs were affected. The incised cyst were reported more frequently from humans rather than in showed oozing of brownish exude and presence of flukes animals which was misinterpreted as tuberculosis and 2–3 in number (Fig. 1b). The coffee bean shaped flukes majority were recorded in north eastern states compared to collected from cystic lesions were identified as Parago- southern India with very less cases particularly in wild nimus spp based on the morphological characters and animals (Singh et al. 2009). In south part of the country, micrometry (Fig. 1d). The flukes were 9.5 mm long and lung fluke infection was reported in dogs from Coorg in 4.5 mm wide. The oral and ventral suckers were almost Madras Presidency way back in Rao (1935). Recently, same sized placed in anterior aspect of the body. The pulmonary paragonimiasis in a female wild Royal Bengal intestinal caeca extended up to the posterior end. The lobed tiger (Panthera tigris tigris) has been reported from testes were adjacent from each other located at the poste- Mysuru, Karnataka, India by Dharanesha et al. (2017). rior end, and the lobed ovaries were placed in median aspect and slightly posterior to acetabulum (Fig. 1e). The eggs were 94 lm long and 60 lm wide in morphometry. Methods The yellowish brown colored eggs with oval shape, thick shelled and often asymmetrical ends, one end slightly A male wild tiger (Panthera tigris tigris), aged about flattened and the other end with operculum were found in 18 months was rescued from snare (trap) at Bekkesodluru fecal sample (Fig. 1c). These findings were similar to adjoining Lakshmanthirtha by Forest Department, Pon- morphological characters described by Soulsby (1982). nampet Range, Virajpet Division in the month of January, The pericardial cavity showed increased pericardial fluid of 2017. The tiger died 2 days later in captivity at Chamundi turbid nature. The epicardial surface showed petechial Animal Conservation, Rescue and Rehabilitation Centre, hemorrhages. Liver was severely congested and gall Koorghalli, Mysuru, Karnataka, India. The necropsy was bladder was engorged with bile. The cortex of both the conducted as per the standard procedure and systematic kidneys and spleen were congested. The focal hemorrhages examination was carried out. The lungs were congested, and ulcers in the mucosa of small and large intestines were emphysematous with discrete raised transparent to dark noticed. encysted lesions. Lung cysts were incised, flukes were The histopathological examination revealed presence of removed and collected in phosphate buffered saline (PBS) paired adult flukes in the bronchial lumen (Fig. 2a) as for identification. From the affected part of lungs, tissue fibrous encapsulation and characterized by hemorrhage, slices of 5–10 mm thickness were collected in 10% neutral loss of cilia, desquamation and proliferation of lining buffered formalin (NBF) for histopathological examina- epithelium, transmural and peribronchial infiltration of tion. About 5–10 g of fecal material from intestine was also inflammatory cells, mainly mononuclear cells like macro- collected in a container. The formalin fixed tissues were phages and plasma cells (Fig. 3a). The flukes had charac- processed, sectioned at 4–5 micron thickness and stained teristic serrated tegument with spines (Fig. 2b). The with haematoxylin and eosin (H&E) for histopathological squamous metaplasia of lining bronchial epithelium was evaluation. conspicuous and intriguing histopathological finding (Fig. 3c, d). Alveoli were filled with inflammatory exudate, hemorrhage with hyperplasia of lining alveolar cells, Results and discussion thickening of septal connective tissue and alveolar atelec- tasis were evident (Fig. 3b). Adjacent to fluke, yellowish External examination of sub adult male tiger showed fair eggs were found as large aggregations surrounded by body condition, weighed around 64.9 kg, pale oral and fibrous encapsulation, mononuclear cell infiltration and conjunctival mucous membranes with sunken eye balls. fibrous tissue proliferation (Fig. 2c, d). External examination of the carcass revealed deep necrosed The fluke-provoked lung lesions could be due to direct wound accumulated with pus in left and right forelimb mechanical injury during migration in lung before encys- (near carpal joint) along with bruises and edema due to tation, toxic metabolites, also by eggs and damage induced 123 530 J Parasit Dis (July-Sept 2019) 43(3):528–533 123 J Parasit Dis (July-Sept 2019) 43(3):528–533 531 b Fig. 1 a Lungs congested, emphysematous, and pneumonic with gross pathological findings in lungs such as numerous discrete raised transparent to dark encysted lesions (arrow). b Incision cystic lesions with congestion, hemorrhage, necrosis, of encysted lesions contained