Prevalence of gastrointestinal and blood parasites, including Leptospira infections in stray dogs from Palakkad, Kerala: A study with relevance to public health

This study investigates the prevalence of gastrointestinal parasites, blood-borne parasites, and Leptospira infections in a sample population of stray dogs in Palakkad District, Kerala, focusing on their zoonotic risks. 100 faecal samples and 200 peripheral blood smears from dogs presented for the Animal Birth Control Program (ABC) at ABC Centre, Alathur were collected. Faecal samples were subjected to microscopic examination for parasite identification, while blood smears were stained with Field stain and inspected under a microscope for blood parasites.. The seroprevalence of Leptospira was studied using the microscopic agglutination test (MAT) assay with twelve reference serovars. Results revealed a 43% prevalence of gastrointestinal parasites, notably Ancylostoma caninum (22%), Strongyloides spp (13%), and Diphyllobothrium latum (8%). Additionally, bloodborne parasites, including microfilariae (10%) and haemo-protozoans like Babesia gibsoni (9%) and Babesia canis (0.5%), were identified. The overall serovar prevalence of Leptospira was 63.33%, with Australis being the most dominant (46.67%). This study underscores the potential public health risks posed by zoonotic parasites carried by stray dogs in this region.

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Zoonotic Transmission CycleClose ×

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Percentage: Ancylostoma caninum vs Strongyloides spp. vs Diphyllobothrium latumClose ×

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Percentage: Australis vs Bataviae vs Icterohaemorrhagiae vs JavanicaClose ×

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Introduction

Stray dog populations become integral to urban ecosystems, especially in developing countries. Without a proper control program, stray dog feces and urine can contaminate soil and water with parasites and pathogens. Dogs also serve as a reservoir for vector-borne diseases that impact both veterinary and public health. Prior studies revealed the presence of zoonotic filarial parasites like Brugia malayi and Dirofilaria repens in the dog population in Kerala and neighboring regions (Chirayath et al., 2017; Nazar et al., 2017) [8,[39][40] Moreover, common canine gastrointestinal parasites such as Ancylostoma caninum, Strongyloides spp, Diphyllobothrium, and Spirometra, cause diseases in human beings, have also been reported in the region (Devi et al., 2007; Sabu et al., 2015; George et al., 2016; Mr et al., 2017; Vini et al., 2021) [50,47,19,[35][36]64] The increasing occurrence of Leptospirosis among both humans and domestic animals in the region is also a matter of concern (James et al., 2018; Murugavelu et al., 2022) [24,37] . However, earlier studies mainly focused on the domestic dog population, and comprehensive studies among stray dogs remain limited for the prevalence of such parasites. This study seeks to bridge this gap by examining gastrointestinal parasites, blood-borne parasites, and Leptospira infections among stray dogs in Palakkad district, by analysing the samples from dogs presented for the Animal Birth Control Program at ABC Centre, Alathur. Gaining insight into the prevalence and diversity of these parasites among stray dogs helps to understand the zoonotic transmission dynamics and aids in formulating strategies for disease surveillance and control.

Materials and Methods

100 fecal samples and 200 peripheral blood smears were collected from the stray dogs presented for the Animal Birth Control Program at the ABC Center in Alathur, Palakkad. Additionally, 30 whole blood samples were obtained from the same canine population for serum isolation to assess Leptospira serology. Fecal samples were processed using the centrifugal sedimentation method for ova concentration, followed by microscopic examination at 10X magnification, confirmed at 40X magnification. Peripheral blood smears were prepared by fixing thin blood smears with methanol for 2 minutes, followed by staining using Field stain. The smears were meticulously scrutinized under an oil immersion objective (100X magnification) to detect blood parasites. Leptospira serovar prevalence was assessed through the Microscopic Agglutination Test (MAT) assay. Dog blood samples were collected in sterile clot activator vials for serum extraction. The serum was meticulously separated from the clotted blood and transferred into two milliliter microcentrifuge tubes. MAT was performed using a panel of twelve reference serovars including Leptospira interrogans serovar Australis, Autumnalis, Bataviae, Canicola, Grippotyphosa, Icterohaemorrhagiae, Javanica, Pomona, Pyrogenes, and Leptospira serovar Djasiman, Hardjo, and Hebdomadis. Following the protocol (WOAH, 2023) [67] the assay was conducted in 96-well U-bottom microtiter plates with dilutions ranging from 1:50 to 1:6400. Each well of the microtiter plates was filled with 50 µL of PBS. Serum samples, diluted at 1:25, were added to the first well of each row and mixed thoroughly. Subsequently, serial two-fold dilutions were carried out, with eight wells in each row and 50 µL discarded from the eighth well. A consistent volume of 50 µL of a specific serovar, containing 2 X 10 8 leptospires/mL, was added to each row and incubated at 37ºC for two to four hours. The resultant dilution mixtures were examined under dark field microscopy, and the outcomes were documented. The highest dilution showing 50 percent agglutination or 50 percent reduction in free leptospires was considered the endtiter. The study revealed a high prevalence of gastrointestinal parasites, affecting 43% of the examined population of stray dogs. Among these parasites, Ancylostoma caninum, Strongyloides spp, and Diphyllobothrium latum were prominent, accounting for 22%, 13%, and 8% respectively. Blood-borne parasites, including microfilariae, showed an overall prevalence of 10%, with 8% being unsheathed microfilariae and 2% sheathed. Haemo-protozoans such as Babesia gibsoni (9%) and Babesia canis (0.5%) were also identified. Furthermore, the overall prevalence of Leptospira serovars was 63.33%, with Australis found to be the most dominant at 46.67%, followed by Bataviae and Icterohaemorrhagiae, each comprising around 20% of the studied serovars. Notably, Javanica, Grippotyphosa, and Pomona exhibited significant prevalence at approximately 10%, 3.33%, and 3.33% respectively. Furthermore, the sample also exhibited the prevalence of multiple serovars; Australis and Bataviae (20%), Australis and Icterohaemorrhagiae (10%), Australis and Grippotyphosa (3.33%), Australis, Bataviae, and Pomona (3.33%), Australis, Icterohaemorrhagiae, and Javanica (3.33%).

Results

Results

Discussion

Compared to the previous studies conducted in Nagpur City (G.S. Khante et al., 2009) [20] , Puducherry (Das et al., 2009), Uttar Pradesh (Sudan et al., 2015) [57] , and Andhra Pradesh (Kurumadas et al., 2020) [30] , which reported overall prevalence rates of gastrointestinal parasites in stray dogs at 75.16%, 65.64%, 88.9%, and 60.2%, respectively, the current investigation revealed a lower prevalence of 43%. While Ancylostoma caninum prevalence remained consistent across regions, with Nagpur at (22.55%) and Andhra Pradesh at (26.1%), Puducherry and Uttar Pradesh identified a notably higher rate (51.53% and 55.6%) compared to the 22% in the current study. Conversely, the present study identified a higher prevalence of Diphyllobothrium (8%) compared to the lower rates of 1.25% in Nagpur, 5.6% in Uttar Pradesh and 2.7% in Andhra Pradesh reported in earlier studies. Moreover, a higher prevalence of Strongyloides spp. was found in the recent study (13%) compared to the earlier report of 4.29% in Puducherry. Similarly, in contrast to previous studies focussing on pet dogs, the current study on stray dogs exhibited a higher overall prevalence of gastrointestinal parasites (43%) than earlier studies in Puducherry (23.30%), Ludhiana, Punjab (24.71%), Junagadh, Gujarat (21.97%), Northern Kerala (42.19%), and Southern Kerala (39.90%) ( [54,41,31] . While Ancylostoma caninum prevalence remained consistent across regions, with rates reported at 19.37%, 22.41%, 11.65%, 18.23%, and 15.22%, respectively, for the respective locations, the present study noted a comparable rate of 22%. Additionally, Strongyloides spp, Diphyllobothrium latum which accounted for 13% and 8% in the present study, were not specifically mentioned in the pet dog studies. Ancylostoma caninum, recognized as the principal cause of canine hookworm disease in most tropical and subtropical areas, is acknowledged for its significant pathogenicity among dog hookworms (Morelli et al., 2021) [34] . This infestation causes severe outcomes, notably anemia and extensive intestinal injury due to inflammation and blood loss, particularly affecting vulnerable puppies. Reactivation of dormant larvae during key reproductive stages in adult dogs, such as oestrus and gestation, poses a notable risk of transmission to newborns via colostrum, thus perpetuating the parasitic cycle (Silva et al., 2020) [52] . Additionally, infective larvae present in the environment possess the capability to penetrate human skin, inducing inflammatory responses and pruritus, leading to cutaneous larva migrans. Moreover, eosinophilic enteritis has been documented in humans due to the presence of occult adult Ancylostoma worms within the intestine, highlighting the zoonotic implications of these parasites (Croese et al., 1994; Walker et al., 1995) [9,66] . Strongyloides are nematodes, the most important one that affects dogs is S. stercoralis. Both dog-specific S. stercoralis as well as the strains sharing host range with humans are also described (Jaleta et al., 2017) [23] . In dogs, infection is often asymptomatic, but in young ones, it can cause gastrointestinal and respiratory signs, exacerbated by corticosteroids and immunodeficiency, potentially leading to severe outcomes and even death. Only female worms are parasitic in the intestine, reproducing through mitotic parthenogenesis, while free-living males and females reproduce sexually in the environment (Thamsborg et [60,63] . Strongyloides are capable of self-infection, completing their lifecycle within the host, and in puppies, the infection can lead to severe intestinal inflammation, clostridial overgrowth, and fatal diarrhea (Dillard et al., 2007) [13] . Soil-transmitted human S. stercoralis infection is prevalent in tropical and subtropical regions, with symptoms ranging from mild to severe depending on immune competency, and severe outcomes, such as fatal hyperinfection and widespread dissemination, are observed in immunocompromised individuals, often associated with predisposing conditions like liver cirrhosis, alcoholism, malnutrition, HIV, HTLV infection, and lymphoma (Fardet et al., 2006; Marco Kassalik & Mönkemüller., 2011; Schär et al., 2013) [16,48] . Diphyllobothriasis, commonly referred to as fish tapeworm infection, is transmitted from various marine and aquatic fish species to humans, mammals, and birds that consume fish (Ramana et al., 2011) [46] . According to CDC, USA, in humans, it can lead to persistent infection, with reported cases lasting up to 25 years (CDC., 2019) [7] . Adult tapeworms in the intestine rarely lead to disease in dogs and cats. The clinical presentation may be influenced by infection severity, age, health, breed, and nutritional status of the animal. Dogs may display mild diarrhea, colic, irritability, erratic appetite, lethargy, and dull coat. Severe outcomes like intestinal blockage, emaciation, and seizures may rarely seen (Peregrine, 2023) [43] . In humans, Diphyllobothriasis manifests as intermittent diarrhea, vomiting, abdominal discomfort, weakness, dizziness, and an unusual craving for salt. Similar to other tapeworm infections, Diphyllobothriasis can lead to vitamin B12 deficiency, causing megaloblastic anemia and neurological dysfunction. In rare instances infection may lead to allergic reactions, mimicking appendicitis and cholangitis or cholecystitis induced by migrating proglottids are also seen (Durrani et al., 2023; Sharma et al., 2018) [15,49] . In patients, hematological parameters like eosinophilia may vary and for detecting B12 deficiency hyper-segmentation of neutrophils appears to be a more sensitive indicator than mean cell volume (MCV) or red cell distribution width (RDW) (Thompson et al., 1989; Ramana et al., 2011; Mr et al., 2017) [46, 61, 35-36] . Reports of Diphyllobothriasis in India are limited, especially in Southern India, where the prevalence might be linked to the local consumption of fish as a dietary staple. Additionally, there's speculation that these infections might be misdiagnosed as taeniasis in some cases (Mr et al., 2017) [3536] . Microfilariasis in dogs reported in Kerala belongs to nematodes, Dirofilaria repens (unsheathed) (Nazar et al., 2017) [36][37][38][39][40] , and Brugia malayi (sheathed) (Chirayath et al., 2017) [8] . Adult D. repens worms are commonly located in subcutaneous nodules, whereas B. malayi exhibits a preference for lymphatic vessels. Microfilaria of both species is transmitted by mosquitoes. Brugia spp. is generally deemed to have minimal pathogenic significance in dogs, although instances of lymphadenomegaly and lymphedema may occasionally occur. Similarly, while most cases of D. repens in canines are asymptomatic, nonspecific clinical signs like pruritus, itching, and asthenia may be present on occasion. Additionally, cases of alopecic regions with hyperpigmentation and an unusual instance of diffuse dermatitis linked to D. repens have also been documented (Nawa et al., 2023) [38] . B. malayi causes lymphatic filariasis in humans while the D ripens can cause subcutaneous, intramuscular, and ocular dirofilariasis. All such cases were reported from the state of Kerala (Mohankumar & Patil, 2017; Nazar et al., 2017; Felix et al., 2023; Joseph et al., 2023) [33, 39-40, 17, 25] . Additionally, D. repens causing eosinophilic meningitis (Poppert et al., 2009; Jyotsna et al., 2021) [26] as well as intra-oral infections from Sri Lanka (Tilakaratne & Pitakotuwage, 2003) were also reported. Without intervention, D. repens can persist for approximately eighteen months (Pampiglione et al., 2001) [42] . Earlier reports suggest the prevalence of microfilariasis in Kerala and adjacent regions varies from 3.9% to 44.3% (Kamran et al., 2020; Malatesh et al., 2019; Radhika et al., 2001) [27,32,45] . The current finding of 10% prevalence rate of microfilariasis, comprising 8% unsheathed and 2% sheathed microfilariae, aligns closely with the results documented by (Chirayath et al., 2017) [8] , who reported an overall prevalence of 8.1% among dogs in Kerala, with 6.6% unsheathed and 1.8% sheathed microfilariae. Canine Babesiosis is mainly a tick-borne disease caused by intraerythrocytic parasites of the genus Babesia, belonging to the apicomplexan group. In Kerala, both large Babesia B. canis vogeli and small Babesia B. gibsoni were reported to cause disease in dogs (Augustine et al., 2017) [2] . The nature and severity of disease progression depend on the species of Babesial organisms, age, immune status, concurrent disease, and animal health status. The disease is characterized by erythrolysis, hemolytic anemia, splenomegaly, and thrombocytopenia (Boozer & Macintire, 2003; Vishwakarma et al., 2019) [5,65] . While canine Babesiosis is typically not deemed zoonotic, other species such as Babesia divergens, which affects cattle in Europe, and Babesia microti, found in small rodents in the USA, have the potential to infect humans as well (Vishwakarma et al., 2019) [65] . Based on complimentary factors and in an overlapping manner canine Babesiosis may turn out to cause acute renal failure (ARF), acute respiratory distress syndrome (ARDS), coagulopathy, hepatopathy, jaundice, immune-mediated hemolytic anemia (IMHA), pancreatitis, hypotension, myocardial pathology, cerebral babesiosis, and shock. Rare complications may involve gastrointestinal disturbances, ocular issues, muscle pain, upper respiratory symptoms, extremity necrosis, and fluid retention (Vishwakarma et al., 2019) [65] . Compared to blood smear examination higher prevalence of Babesiosis is reported using molecular methods of diagnosis. Various studies in different parts of India reported up to 84% prevalence of B. gibsoni and up to 16% of B. canis based on the season, climatic conditions, and tick activity (Singh et al., 2014; Bhaskaran Ravi et al., 2016; Bordoloi et al., 2022) [53,4,6] . In Kerala, (Jain et al., 2017) reported 47.3% of B. gibsoni using molecular techniques, while, detected only 26.63% using light microscopy and concluded the effectiveness of the molecular technique over the latter. (Singh et al., 2014) [53] also reported such disparity using conventional (6.54%) and molecular methods (15.42%) for diagnosing B canis. Similarly, (Preena et al., 2019) [44] reported Babesia gibsoni infections at 13.9% and B. canis infections at 0.60% from dogs in Kannur, Kerala. Hence it can be assumed from the present study that compared to the domestic population in Kerala stray dogs selected in this study carry a low burden of Babesiosis. On the other hand, the real prevalence may be much higher if examined via molecular techniques at least in the case of small babesiosis B. gibsoni. Leptospirosis, a widely spread zoonotic disease caused by pathogenic strains of Leptospira bacteria, affects numerous mammals, including humans, and is mainly transmitted via exposure to infected urine or contaminated surroundings. Rodents are crucial contributors to disease transmission by harboring the organism in their renal tubules for life and shedding it in their urine. Similarly, dogs, acting as hosts and reservoirs for multiple leptospiral serovars, play a significant role in disease transmission, amplifying environmental exposure and augmenting the risk of increased human infection. Studying transmission dynamics across animals and humans and understanding prevalent serogroups-serovars is crucial for vaccine development and prevention strategies. (Balboni et al., 2022; Smith et al., 2022; Sykes et al., 2010) [3,56,59] Environmental factors such as urbanization, poor waste management, and climate shifts escalate interactions among rodents, stray and domestic dogs, other domestic animals, and wildlife, heightening canine exposure to diverse pathogenic Leptospira strains. The extensive diversity of more than 250 pathogenic Leptospira serovars highlights variations in host susceptibility and disease severity. This underscores the importance of identifying the infecting serovars to understand disease transmission and guide vaccination strategies effectively. Moreover, the introduction of new serovars through importing animals and the influence of expanding pet populations significantly affect the prevalence of local serovars, thus impacting disease dynamics (Smith et al., 2022) [56] Prior studies in the domestic dog population indicate that canine Leptospirosis in Kerala witnessed dynamic shifts in serovar prevalence (Indu et al., 2004) [21] underscored Pomona, Canicola, and Icterohaemorrhagiae as prevalent serovars, followed by (G. Abhinay, 2012) [18] emphasis on Australis, Pomona, Grippotyphosa, and Icterohaemorrhagiae, while (Ambily et al., 2013) [1] highlighted Autumnalis, Australis, and Pomona. (Soman et al., 2014) [55] emphasized Pomona and Australis, while, (Shaji et al., 2019) [51] demonstrated Pyrogenes, Grippotyphosa, and Bataviae as prominent serovars. (Divya et al., 2021) [14] [58] . The disease in humans may manifest in either anicteric or icteric forms. Symptoms in anicteric presentation encompass fever, myalgia, vomiting, diarrhea, occasionally arthralgia, acalculous cholecystitis, and pancreatitis. Subsequently, an immune phase might ensue, characterized by nuchal rigidity, aseptic meningitis, and uveitis. In contrast, Weil's disease, or icteric Leptospirosis, occurs in a minority of patients and presents with jaundice, myocarditis, rhabdomyolysis, renal failure, acute respiratory distress syndrome (ARDS) and disseminated intravascular coagulation (DIC) (Daher et [10,12,28,29] .

Conclusion

This study conducted among stray dogs in Palakkad, Kerala, revealed a noteworthy prevalence of zoonotic gastrointestinal and bloodborne parasites alongside Leptospira infections. With a 43% prevalence of gastrointestinal parasites, prominent findings included Ancylostoma caninum, Strongyloides spp, and Diphyllobothrium latum. Blood-borne parasites like Babesia gibsoni (9%) and Babesia canis (0.5%) were identified, along with a 10% microfilariae prevalence. Comparisons with earlier studies in various regions highlighted variability in parasite prevalence rates, emphasizing the dynamic nature of disease epidemiology among stray dog populations. The study's insights into zoonotic implications underscore the necessity for vigilant monitoring and robust control measures, providing valuable information for veterinary practitioners, public health officials, and policymakers to devise targeted interventions to mitigate zoonotic risks associated with stray dogs in urbansemi-urban ecosystems. These findings serve as a supplementary resource, emphasizing the urgency of continued surveillance, public awareness, and collaborative efforts in addressing the multifaceted challenges posed by zoonotic parasites carried by stray dogs in Kerala's urban settings.

Figures and tables from the paper

Parasite	No. of positive samples	Percentage
Ancylostoma caninum	22	22
Strongyloides spp.	13	13
Diphyllobothrium latum	8	8
Total no. of faecal samples	100

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Prevalence of gastrointestinal parasites in stray dogs,

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Microfilaria (unsheathed)	16	8
Microfilaria (sheathed)	4	2
Babesia gibsoni	18	9
Babesia canis	1	0.5
Total no. of blood samples	200

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Prevalence of Leptospira serovars in stray dogs, Palakkad

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Serovar	No. of samples positive	Percentage
Australis	14	46.67
Bataviae	6	20
Icterohaemorrhagiae	6	20
Javanica	3	10
Grippotyphosa	1	3.33
Pomona	1	3.33
Total positive	19	63.33
Total no. of samples	30

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Prevalence of Leptospira serovars in stray dogs, Palakkad

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1. Ambily R, Mini M, Joseph S, Krishna SV, Abhinay G. Canine leptospirosis-a seroprevalence study from Kerala. Veterinary World. 2013;6(1):42-44. DOI: 10.5455/vetworld.2013.42-44
2. Augustine S, Sabu L, Lakshmanan B. Molecular identification of Babesia spp. in naturally infected dogs of Kerala, South India. Journal of Parasitic Diseases. 2017;41(2):459-462. DOI: 10.1007/S12639-016-0827-9
3. Balboni A, Mazzotta E, Boniotti MB, et al. Outbreak of Leptospira borgpetersenii Serogroup Sejroe Infection in Kennel: The Role of Dogs as Sentinel in Specific Environments. International Journal of Environmental Research and Public Health. 2022;19(7):3906. DOI: 10.3390/ijerph19073906
4. Bhaskaran Ravi L, Bhoopathy D, Subbiah V. Escalations in the incidence of canine babesiosis over a period of 8 years (2006-2013) in Chennai, Tamil Nadu, India. Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology. 2016;40(4):1239. DOI: 10.1007/S12639-015-0659-Z
5. Boozer AL, Macintire DK. Canine babesiosis. The Veterinary Clinics of North America. Small Animal Practice. 2003;33(4):885-904. DOI: 10.1016/S0195-5616(03)00039-1
6. Bordoloi G, Kumar Boro P, Sharma M, et al. Prevalence of canine babesiosis in Lakhimpur and Dhemaji districts of Assam and adjoining areas of Eastern Himalayan foothills in Arunachal Pradesh, India. Pharma Innovation Journal. 2022;SP-11(2):500-502. Retrieved from http://www.thepharmajournal.com
7. CDC. CDC -DPDx -Diphyllobothriasis. Centres for Disease Control and Prevention, Global Health, Division of Parasitic Diseases and Malaria. 2019, May 14. Retrieved from https://www.cdc.gov/dpdx/diphyllobothriasis/index.html
8. Chirayath D, Alex PC, George S, Panicker VP. Identification of Brugia malayi in dogs in Kerala, India. Tropical Biomedicine. 2017;34(4).
9. Croese J, Loukas A, Opdebeeck J, Prociv P. Occult enteric infection by Ancylostoma caninum: A previously unrecognized zoonosis. Gastroenterology. 1994;106(1):312. DOI: 10.1016/S0016-5085(94)93907-1
10. Daher EF, Lima RSA, Silva Júnior GB, et al. Clinical presentation of leptospirosis: a retrospective study of 201 patients in a metropolitan city of Brazil. The Brazilian Journal of Infectious Diseases. 2010;14(1):3-10. DOI: 10.1016/S1413-8670(10)70002-7
11. Davies P, Aoyagi Y. Leptospirosis presenting as acute acalculous cholecystitis. Clinical Case Reports. 2017;5(11):1775. DOI: 10.1002/CCR3.1173
12. Divya D, Joseph S, Mini M, Nair RS, Davis KJ. Seroprevalence of Leptospirosis in Animals in Thrissur District of Kerala. International Journal of Current Microbiology and Applied Sciences. 2021;10(03):16161620. DOI: 10.20546/ijcmas.2021.1003.203
13. Fardet L, Généreau T, Cabane J, Kettaneh A. Severe strongyloidiasis in corticosteroid-treated patients. Clinical Microbiology and Infection. 2006;12(10):945-947. DOI: 10.1111/j.1469-0691.2006.01443.x
14. Felix V, Anilkumar L, Niyas M, Abbas A, John KE, Varma SR, Chakkikavil J. Dirofilariasis Presenting as Orbital Abscess Complicating Ethmoid Sinusitis. Indian Journal of Otolaryngology and Head and Neck Surgery: Official Publication of the Association of Otolaryngologists of India. 2023;75(4):3636-3638. DOI: 10.1007/s12070-023-04021-8
15. Abhinay G, Joseph SJ, Abhinay R. Seroprevalence of Canine Leptospirosis. The Indian Veterinary Journal. 2012;89(2):72-73.
16. Indu S, Saseendranath MR, Baby K, Venkatraman KS, Neduncheiliyan S. Seroprevalence of Leptospirosis among dogs in Thrissur. In: Journal of Veterinary and Animal Sciences. 2004, 35.
17. Jain KJ, Lakshmanan B, Syamala K, Praveena JE, Aravindakshan T. High prevalence of small Babesia species in canines of Kerala, South India. Veterinary World. 2017;10(11):1319. DOI: 10.14202/VETWORLD.2017.1319-1323
18. Jaleta TG, Zhou S, Bemm FM, Schär F, Khieu V, Muth S, et al. Different but overlapping populations of Strongyloides stercoralis in dogs and humans-Dogs as a possible source for zoonotic strongyloidiasis. PLOS Neglected Tropical Diseases. 2017;11(8):e0005752. DOI: 10.1371/JOURNAL.PNTD.0005752
19. James S, Sathian B, Teijlingen EVan, Asim M. Outbreak of Leptospirosis in Kerala. Nepal Journal of Epidemiology. 2018;8(4):745-747. DOI: 10.3126/nje.v8i4.23876
20. Joseph M, Krishna MM, Vijayan A. Human Subcutaneous Dirofilariasis. Cureus. 2023;15(3):e35879. DOI: 10.7759/cureus.35879
21. Jyotsna AS, Vinayan KP, Biswas L, Haridas S, Roy AG, Suresh P, et al. Eosinophilic Meningitis and Intraocular Infection Caused by Dirofilaria sp. Genotype Hongkong -Volume 27, Number 5-May 2021 -Emerging Infectious Diseases journal -CDC. Emerging Infectious Diseases. 2021;27(5):1532-1534. DOI: 10.3201/EID2705.203599
22. Kamran A, Kj A, Ds M. Canine microfilariosis in and around Shivamogga, Karnataka: A Epidemiological study. Journal of Entomology and Zoology Studies. 2020;8(4):2097-2099. http://www.entomoljournal.com
23. Karnik ND, Patankar AS. Leptospirosis in Intensive Care Unit. Indian Journal of Critical Care Medicine: PeerReviewed, Official Publication of Indian Society of Critical Care Medicine. 2021;25(Suppl 2):S134. DOI: 10.5005/JP-JOURNALS-10071-23852
24. Khan R, Quaiser S, Khan F. Anicteric leptospirosis: An unusual cause of acute pancreatitis. Community Acquired Infection. 2015;2. DOI: 10.4103/2225-6482.166085
25. Kurumadas R, Chennuru S, Krovvidi S, Pattipati M. Assessing risk factors associated with prevalence of canine gastrointestinal parasitic zoonoses in Andhra Pradesh, India. The Indian Journal of Animal Sciences. 2020;90(6):851-855. DOI: 10.56093/IJANS.V90I6.104980
26. Malatesh DS, Kamran CA, Ananda KJ, Udupa G, Ramesh K, Rao PTS, et al. Epidemiological Studies on Canine Microfilariosis due to Dirofilaria repens in and around Mangalore-a Coastal Region of Karnataka. International Journal of Current Microbiology and Applied Sciences. 2019;8(9):714-721. DOI: 10.20546/ijcmas.2019.809.086
27. Mohankumar A, Patil RT. Intramuscular Gravid Dirofilaria repens Infection in Human-An Unusual Presentation. International Journal of Research Studies in Microbiology and Biotechnology. 2017;3:2454-9428. DOI: 10.20431/2454-9428.0304001
28. Mr A, Lodhi I, Kuknoor GR, Katakol S. A rare case of Diphyllobothriasis and Megaloblastic anaemia in a middle-aged lady from South India. Indian Journal of Microbiology Research. 2017a;4(4):471-472. DOI: 10.18231/2394-5478.2017.0105
29. Murugavelu M, Menon KV, Latha C, Jolly D, Vinodkumar K. Seroprevalence of leptospirosis among slaughtered cattle in Thrissur, Kerala#. Journal of Veterinary and Animal Sciences. 2022;53(1). DOI: 10.51966/jvas.2022.53.1.65-69
30. Nawa Y, Shigehiko U, Genchi C, Yoshida A, Gruntmeir J, Kelly M, et al. Cutaneous filarioid nematodes of dogs in the United States: Are they emerging, neglected, or underdiagnosed parasites? [Internet]; c2023. DOI: 10.3389/fvets.2023.1128611
31. Nimisha M, Kariyappa R, Kurbet PS, Amrutha BM, Varghese A, Deepa CK, Priya MN, Lakshmanan B, Ajith Kumar KG, Ravindran R. Parasitic Diseases of Domestic and Wild Animals in Northern Kerala: A Retrospective Study based on Clinical Samples. International Journal of Current Microbiology and Applied Sciences. 2017;6(11):2381-2392. DOI: 10.20546/ijcmas.2017.611.282
32. Pampiglione S, Rivasi F, Angeli G, Boldorini R, Incensati RM, Pastormerlo M, Pavesi M, Ramponi A. Dirofilariasis due to Dirofilaria repens in Italy, an emergent zoonosis: report of 60 new cases. Histopathology. 2001;38(4):344-354. DOI: 10.1046/J.1365-2559.2001.01099.X
33. Preena P, Sarangom SB, Ramesh Kumar KV, Seeja S, Rajalekshmi S. Hematological alterations in large Babesia species infection in dogs of Kannur District of Kerala. Journal of Veterinary and Animal Sciences. 2019;17(3):22-30. DOI: 10.1007/S12639-021-01404-Y/METRICS
34. Radhika R, Subramax~ian H, Saseeiidranath MR. PREVALENCE OF Dirofilaria repens IN DOGS IN THRISSUR (KERALA, INDIA)*. Journal of Veterinary and Animal Sciences. 2001;32:46-48.
35. Sabu L, Lakshmanan B, Devada K, Sundaresh Kumar P. Occurrence of human sparganosis in Kerala. Journal of Parasitic Diseases. 2015;39(4):777-779. DOI: 10.1007/s12639-014-0421-y
36. Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, et al. Strongyloides stercoralis: Global Distribution and Risk Factors. PLOS Neglected Tropical Diseases. 2013;7(7):e2288. DOI: 10.1371/JOURNAL.PNTD.0002288
37. Sharma K, Wijarnpreecha K, Merrell N. Diphyllobothrium latum Mimicking Subacute Appendicitis. Gastroenterology Research. 2018;11(3):235. DOI: 10.14740/GR989W
38. Sheela Devi C, Srinivasan S, Murmu U, Barman P, Kanungo R. A rare case of Diphyllobothriasis from Pondicherry, South India. Indian Journal of Medical Microbiology. 2007;25(2):152-156. DOI: 10.1159/000205559
39. Shaji S, John K, Joseph S, Ravishankar C, JA, RR, et al. Seroprevalence of Leptospirosis in dogs in Wayanad. Journal of Veterinary and Animal Sciences. 2019;50(1):54-56.
40. Silva V, Silva J, Gonçalves M, Brandão C, Vieira e Brito N. Epidemiological survey on intestinal helminths of stray dogs in Guimarães, Portugal. Journal of Parasitic Diseases. 2020;44(4):869-876. DOI: 10.1007/s12639-020-01252-2
41. Singh A, Singh H, Singh NK, Singh ND, Rath SS. Canine Babesiosis in Northwestern India: Molecular Detection and Assessment of Risk Factors. BioMed Research International; c2014. DOI: 10.1155/2014/741785
42. Singh Harkirat, Haque M, Jyoti S, N.K., R. Occurrence of Parasitic Infections in Dogs in and Around Ludhiana, Punjab (India). Applied Biological Research Volume. 2012;14(1):108-110.
43. Soman M, Jayaprakasan V, Mini M. Epidemiological study on human and canine leptospirosis in Central and North Kerala; c2014. DOI: 10.14202/vetworld.2014.759764
44. Sudan V, Jaiswal AK, Shanker D, Kanojiya D, Sachan A. Prevalence of endoparasitic infections of non-descript dogs in Mathura, Uttar Pradesh. Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology. 2015;39(3):491. DOI: 10.1007/S12639-013-0383-5
45. Sykes JE, Francey T, Schuller S, Stoddard RA, Cowgill LD, Moore GE. Updated ACVIM consensus statement on leptospirosis in dogs. Journal of Veterinary Internal Medicine. 2023;37(6):1966-1982. DOI: 10.1111/JVIM.16903
46. Sykes JE, Hartmann K, Lunn KF, Moore GE, Stoddard RA, Goldstein RE. ACVIM Consensus Statement 2010 ACVIM Small Animal Consensus Statement on Leptospirosis: Diagnosis, Epidemiology, Treatment, and Prevention; c2010. DOI: 10.1111/j.1939-1676.2010.0654.x
47. Thamsborg SM, Ketzis J, Horii Y, Matthews JB. Strongyloides spp. infections of veterinary importance. In Parasitology. 2017;144(3):274-284. DOI: 10.1017/S0031182016001116
48. Thompson WG, Cassino C, Bahitz L, Meola T, Berman R, Lipkin M, et al. Hypersegmented neutrophils and vitamin B12 deficiency. Hypersegmentation in B12 deficiency. Acta Haematologica. 1989;81(4):186-191. DOI: 10.1159/000205559
49. Tilakaratne WM, Pitakotuwage TN. Intra-oral Dirofilaria repens infection: report of seven cases. Journal of Oral Pathology & Medicine. 2003;32(8):502-505. DOI: 10.1034/J.1600-0714.2003.00183.X
50. Unterköfler MS, Eipeldauer I, Merz S, Pantchev N, Hermann J, Brunthaler R, et al. Strongyloides stercoralis infection in dogs in Austria: two case reports. Parasites and Vectors. 2022;15(1):1-9. DOI: 10.1186/S13071-02205270-2/FIGURES/4
51. Vini V, Antony S, Jacob T, Sasimohan A, Jacob AM, Idikula MJ, et al. A fatal combination of disseminated strongyloidiasis with two bacterial infections in an immunocompromised host Case Report. Access Microbiology. 2021;3:246. DOI: 10.1099/acmi.0.000246
52. Walker NI, Croese J, Clouston AD, Parry M, Loukas A, Prociv P. Eosinophilic enteritis in northeastern Australia. Pathology, association with Ancylostoma caninum, and implications. The American Journal of Surgical Pathology. 1995;19(3):328-337. DOI: 10.1097/00000478-199503000-00011
53. WOAH. Terrestrial Manual Online Access -WOAH - World Organisation for Animal Health. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Twelfth Edition 2023, Leptospirosis (Chapter 3.01.12.). [Internet]; c2023. Available from: https://www.woah.org/en/what-we-do/standards/codesand-manuals/terrestrial-manual-online-access/