Skip to main content
Download PDF

Molecular investigation and clinical management of Hepatozoon Canis infection in an Indian jackal – a case report

BMC Veterinary Research volume 18, Article number: 144 (2022) Cite this article

Abstract

Background

Hepatozoonosis is a common tick-borne illness reported from all over the world. The infection has been well documented in dogs and cats, and has also been identified in wild canids and felids. India is home to many canid species; however, the incidence of Hepatozoonosis in wild canids is rarely reported. A wide variety of protocols have been discussed for the clinical management of the infection in companion animals; however, the suitability of treatment protocols in wild canids is understudied. The current case report highlights the clinical management of Hepatozoonosis in an Indian jackal and molecular investigation to provide vital insights into the epidemiology of the disease.

Case Presentation

A paraplegic Indian jackal was rescued from Melghat Tiger Reserve, Maharashtra, India. The animal had extensive decubital ulcers on the left pin bone and could not walk; however, the animal was active and dragged the hindlimb during locomotion. The vital parameters, blood and serum investigations were normal. Post physiotherapy, massage and infrared therapy, the animal could walk but started knuckling, resulting in injuries. Eight weeks into rehabilitation, the animal had a steep fall in haemoglobin concentration, platelet count, weight loss and was diagnosed with Hepatozoonosis. Considering the altered vital parameters, the jackal was rationally treated with Doxycyclin @ 20 mg/Kg O.D. (Once Daily) for 45 days along with supportive therapy. The jackal recovered after the treatment and led a normal life.

Conclusion

Mono-drug regime using Doxycycline was effective in the alleviation of H.canis infection in jackal. The drug was effective in alleviating the clinical presentation without alteration of vital parameters. The molecular investigation provided qualitative inputs in understanding the epidemiology of Hepatozoon in wild canids.

Background

Tick-borne diseases have been extensively studied in companion animals; however, the epidemiology of protozoal diseases in the wild is understudied. Ticks transmit various infections in the tropical region. The hot and humid climate of the tropics is conducive to the propagation of ticks [1]. There are numerous reports of tick-borne diseases emerging from the Indian subcontinent every year. Hepatozoonosis is a tick-borne disease of companion and wild animals. Rhipicephalus and Amblyomma species are considered important transmitting agents for infection. Recently, the role of Dermacentor reticulatus has been investigated in the transmission of multiple infections, including Hepatozoonosis in red fox (Vulpes vulpes) [2]. The infection has been reported in dogs [3] and cats [4–7]; however, few reports from the wild have been documented. The reports of wild are primarily limited to canids [8–10], ursids [11], felids [12–17], rodents [18], reptiles [19], mustelids [20] and procyonids [21]. Dogs are considered reservoirs of H. canis; they can be infested with brown dog ticks (Rhipicephalus sp.), the definitive hosts. Many species of wild felids and canids are known to be infected with Hepatozoonosis. India has reported incidences of H. canis in wild dogs (Cuon alpinus) in the recent past; however, no reports in any other wild canid species have surfaced from the region [12]. The current case report highlights the clinical management and molecular investigation of Hepatozoonosis in an Indian jackal (Canis aureus indicus).

Case presentation

An adult male Indian jackal (Canis aureus indicus) was rescued from Melghat Tiger Reserve, Maharashtra, India with a history of paraplegia due to a possible automobile accident. The animal was rationally treated at the Transit Treatment Centre and was transferred to Wildlife Research & Training Centre, Gorewada, Nagpur, for further care and rehabilitation after a couple of months. On reception the vital parameters, blood and serum values were within the normal range. The radiological examination revealed an L6 spinal fracture with L6-L7 dislocation resulting in paraplegia. The animal was treated rationally with Injection Ceftiofur Sodium @ 22 mg/Kg, Injection Methyl Prednisolone 2.2 mg/ Kg, Injection Ranitidine HCl (Hydrochloride) @ 4.4 mg total dose once a day. This was supplemented with physiotherapy and infra-red therapy. Post 15 days into rehabilitation, the jackal was found to support his weight on the hind limbs and could walk. However, it was noticed that the jackal started knuckling during the walk and resulted in lacerations and wounds.

The jackal exhibited fever, anaemia, depression, weight loss, rough hair coat, lethargy and inappetence on day 55 of rehabilitation (Day 0). Blood investigation revealed decreased haemoglobin concentration (6.1 g/dL), thrombocytopenia, leucocytosis and neutrophilia; peripheral blood smear examination revealed anisocytosis and the presence of gamonts in neutrophils (Fig. 1). Serum biochemistry showed hypoglycemia and elevated AST (Aspartate Aminotransferase). On day 0, 12.5% of the circulating neutrophils were found to contain gamonts. Considering the low haemoglobin concentration and altered vitals, a mono antiprotozoal therapy was employed using Doxycycline @ 20 mg/Kg body weight once a day along with supportive therapy including hepatoprotectants, iron supplements, vitamins and probiotics. The mono antiprotozoal regime was continued for 45 days, during which vital parameters were monitored on days 0, 21, 45 (Table 1) and monthly thereafter. During the course of the therapy, blood indices and clinical presentation gradually improved, and the percentage of neutrophils containing gamonts gradually improved, and the percentage of neutrophils containing gamonts gradually tapered from 12.5%, 7.66% to 0% on days 0, 21 and 45, respectively.

Fig. 1
figure 1

Blood smear examination revealed presence of gamonts in the neutrophils (indicated by arrow). Normal neutrophils can be seen in the periphery

Full size image
Table 1 Haemato-biochemical values and peripheral blood smear studies evaluated on Day 0, 21 and 45 along with normal reference values
Full size table

To further investigate the infection, DNA (Deoxyribonucleic Acid) was isolated from 100 μl of whole blood using DNeasy\(\circledR \) Blood and Tissue Kit (Mfg. Qiagen Inc, MD, USA) as per the manufacturer’s instructions and Polymerase Chain Reaction (PCR) was performed targeting the 18S ribosomal RNA gene of Hepatozoon sp [22]. An amplification of 650 bp was obtained (Fig. 2), which was sequenced using HepF and HepR primer pairs on ABI 3130 automated DNA sequencer (Mfg. Applied Biosystems, CA, USA). H. felis amplicon reported from tiger was used as a positive control, while the negative control was devoid of any template. To monitor the progression of the infection, PCR studies were repeated on days 21 and 35 (Fig. 2, Lane 1, 2 and 3). To limit relapses, blood samples were examined every month and were found to be negative consistently. The obtained sequence was submitted to the NCBI nucleotide database using the nBLAST tool. It was found to be 99.68% identical to the previously reported H. canis in dogs from India (Accession No. MH922768, MN252045). A systematic phylogenetic analysis was undertaken by including sequences of Hepatozoon identified in wild canids, ursids and felids. The sequences were selected based on similarity with the query sequence (Details in Table2). Sequences reported in domestic and wild were included without preference. Neighbour joining phylogenetic trees using the bootstrap method were constructed using Mega X software to study the topologies of the phylogenetic trees (Fig. 3) [23]. The bootstrap values (1000 replications) were analysed to ensure tree consistency.

Fig. 2
figure 2

Gel electrophoresis on 1% agarose gel. Lane 1,2 and 3 PCR reaction performed on days 35, 21 and 0 respectively, L4 1 Kb ladder, L5 Day 45 and L6 Negative control. An amplification of 650 bp obtained using HEP-F and HEP-R primer (Inokuma et al., 2002)

Full size image
Fig. 3
figure 3

Phylogenetic Analysis of Sequence by Neighbour Joining Phylogenetic Tree using Bootstrap Method (1000 replications)

Full size image
Table 2 List of sequences along with their attributes used for the neighbour-joining phylogenetic studies
Full size table

Discussion and conclusion

Most of Hepatozoon spp. infection in wild and companion animals is subclinical, and it produces clinical outcomes only in very young and immunocompromised individuals [10]. Reports of death in hyenas [8] and coyotes [24] due to Hepatozoonosis highlight the need to investigate the disease among endangered wild canids. The impact of stress, habitat destruction and concurrent viral and bacterial infection on the spread of Hepatozoonosis under free-range has been studied [25]. Conventionally the diagnosis of Hepatozoonosis is primarily based on the blood smear examination; however, when the quantum of infection is scarce, the detection of infection becomes uncertain. Also, Rhipicephalus spp. transmit an array of protozoal infections, coinfection of Anaplasma platys, Ehrlichia canis, H. canis and Rickettsia monacensis has been reported in dogs [26] and wild canids [2, 27]. Molecular techniques can provide sensitive diagnostic tools for detecting protozoal diseases. When augmented with molecular tools like sequencing, qualitative inputs on the epidemiological aspects can be provided.

In the current case report, the jackal exhibited a steep fall in haemoglobin concentration, neutrophilia, leucocytosis, elevated AST levels indicative of hepatic involvement [28, 29]. During the treatment, blood parameters and corpuscular indices showed marginal improvement, with the haemoglobin concentration improving slightly from 6.1 gm/dl (Day 0) to 7.4 gm/dl (Day 45). Clinically, the animal regained its weight and began having a normal appetite and behaviour. The animal showed two instances of loose stools during treatment which was rationally treated with probiotics and diet management. The haemoglobin concentration returned to 10.5 after 90 days, probably due to concurrent blood loss from nursing injuries. Relapses of Hepatozoonosis have been reported in dogs [30, 31]. Hence, a monthly peripheral blood smear and PCR tests were conducted to rule out the relapse, which was consistently negative.

The selection of a therapeutic agent is critical in treating infection in patients with altered vital parameters. The therapeutic agent for treating Hepatozoonosis is selected based on the species of hepatozoon identified. The drugs employed vary from agent to agent; for H. americanum, a multi-drug combination of trimethoprim, pyrimethamine, clindamycin, decoquinate [32]. Also, anticoccidial agent toltrazuril has been found effective in the treatment of experimentally infected voles with H. erhardovae [33]. However, H. canis responds to a combination of imidocarb dipropionate and Doxycycline [29, 34]. Side-effects like hepatic necrosis, kidney failure and death have been reported in dogs treated with imidocarb [35], and the drug has failed to eliminate H. canis in naturally infected dogs [36]. Considering the safety and duration of treatment, mono drug therapy of Doxycycline for 45 days was opted for. The elimination of Hepatozoon infection on day 45 was confirmed by blood smear examination and PCR (Fig. 2 lane 5). It is worth pointing out that the jackal showed no deviations from normal during blood and serum examination on reception. The upsurge of infection was in coincidence with trauma and stress due to tissue injury, as reported in Lions [37]. The jackal recovered uneventfully; thus, Doxycycline has value in the clinical management of H. canis infection in wild canids with compromised vitals.

A Polymerase Chain Reaction (PCR) was carried out to confirm the finding further [22]. The amplicon of 650 bp was sequenced and submitted to National Center for Biotechnology Information (NCBI) database for reference. The sequence was allotted accession number MZ823614. In the current study, sequence analysis revealed 99.68% identity with previously reported sequences of H. canis in dogs from India (Accession No. MH922768, MN252045). There are only a couple of previously reported H. canis in wild dogs (Cuon alpinus) from India (Accession No. HQ829448, HQ829447). No reports of Hepatozoonosis from other wild species have been reported from the country. The phylogenetic analysis revealed the presence of the query sequence (MZ823614) in clade I A consisting of sequences of H. canis reported in dogs and other wildlife from India and abroad. The major clade II consisted mainly of the sequences of H. felis reported in wild felids from India, Korea, Bosnia & Herzegovina (Table2); H.silvestris and H. americanum isolated from a variety of host species including wild and domestic animals (Details provided in Table2). Plasmodium vivax formed a distinct outgroup.

The case report highlights the utility of oral Doxycycline in the clinical management of Hepatozoonosis in wild canids with altered vitals. Molecular techniques are sensitive and can be effectively utilised in the monitoring of the progression of the disease. The insights provided by high throughput technologies like sequencing can help understand the epidemiology and prevalence of Hepatozoonosis. It is essential to study the dynamics of the infection in the wild to ensure the survival of the endangered wildlife. Further investigation in sympatric canids species in the wild and captivity can provide critical insights on Hepatozoonosis.

Availability of data and materials

The sequence identified in the study is available in the public domain database of nCBI under accession no. mZ823614. https://www.ncbi.nlm.nih.gov/nuccore/MZ823614

Abbreviations

O.D.:

Once Daily

HCl:

Hydrochloride

PCR:

Polymerase Chain Reaction

DNA:

Deoxyribonucleic Acid

AST:

Aspartate Aminotransferase

NCBI:

National Center for Biotechnology Information

References

  1. Githeko AK, Lindsay SW, Confalonieri UE, Patz JA. Climate change and vector-borne diseases: a regional analysis. Bull World Health Organ. 2000; 78:1136–47.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Mierzejewska EJ, DwuŻnik D, Koczwarska J, Stańczak Ł, Opalińska P, Krokowska-Paluszak M, Wierzbicka A, Górecki G, Bajer A. The red fox (Vulpes vulpes), a possible reservoir of Babesia vulpes, B. canis and Hepatozoon canis and its association with the tick Dermacentor reticulatus occurrence. Ticks Tick-borne Dis. 2021; 12(1):101551.

    Article  PubMed  Google Scholar 

  3. Anderson M, Turcitu MA, Stefanache M, Tamba P, Barbuceanu F, Chitimia L. First evidence of Anaplasma platys and Hepatozoon canis co-infection in a dog from Romania–a case report. Ticks Tick-borne Dis. 2013; 4(4):317–9.

    Article  Google Scholar 

  4. Braga ÍA, de Souza Ramos DG, Marcili A, Melo AL, Taques II, Amude AM, Chitarra CS, Nakazato L, Dutra V, de Campos Pacheco R, Aguiar DM. Molecular detection of tick-borne protozoan parasites in a population of domestic cats in midwestern Brazil. Ticks Tick-borne Dis. 2016; 7(5):1004–9.

    Article  PubMed  Google Scholar 

  5. André MR, Herrera HM, de Jesus Fernandes S, de Sousa KC, Gonçalves LR, Domingos IH, de Macedo GC, Machado RZ. Tick-borne agents in domesticated and stray cats from the city of Campo Grande, State of Mato Grosso do Sul, midwestern Brazil. Ticks Tick-borne Dis. 2015; 6(6):779–86.

    Article  PubMed  Google Scholar 

  6. Díaz-Regañón D, Villaescusa A, Ayllón T, Rodríguez-Franco F, Baneth G, Calleja-Bueno L, García-Sancho M, Agulla B, Sainz Á. Molecular detection of Hepatozoon spp and Cytauxzoon sp. in domestic and stray cats from Madrid, Spain. Parasites Vectors. 2017; 10(1):112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. East ML, Wibbelt G, Lieckfeldt D, Ludwig A, Goller K, Wilhelm K, Schares G, Thierer D, Hofer H. A Hepatozoon species genetically distinct from H. canis infecting spotted hyenas in the Serengeti ecosystem, Tanzania. J Wildl Dis. 2008; 44(1):45–52.

    Article  CAS  PubMed  Google Scholar 

  8. Giannitti F, Diab SS, Uzal FA, Fresneda K, Rossi D, Talmi-Frank D, Baneth G. Infection with a Hepatozoon sp. closely related to Hepatozoon felis in a wild Pampas gray fox (Lycalopex–Pseudalopex–gymnocercus) co-infected with canine distemper virus. Vet Parasitol. 2012; 186(3-4):497–502.

    Article  PubMed  Google Scholar 

  9. Garrett JJ, Kocan AA, Reichard MV, Panciera RJ, Bahr RJ, Ewing SA. Experimental infection of adult and juvenile coyotes with domestic dog and wild coyote isolates of Hepatozoon americanum (Apicomplexa: Adeleorina). J Wildl Dis. 2005; 41(3):588–92.

    Article  PubMed  Google Scholar 

  10. Pawar RM, Poornachandar A, Arun AS, Manikandan S, Shivaji S. Molecular prevalence and characterization of Hepatozoon ursi infection in Indian sloth bears (Melursus ursinus). Vet Parasitol. 2011; 182(2-4):329–32.

    Article  CAS  PubMed  Google Scholar 

  11. Pawar RM, Poornachandar A, Srinivas P, Rao KR, Lakshmikantan U, Shivaji S. Molecular characterization of Hepatozoon spp. infection in endangered Indian wild felids and canids. Vet Parasitol. 2012; 186(3-4):475–9.

    Article  CAS  PubMed  Google Scholar 

  12. Furtado MM, Metzger B, de Almeida Jácomo AT, Labruna MB, Martins TF, O’Dwyer LH, Paduan KD, Porfírio GE, Silveira L, Sollmann R, Taniwaki SA. Hepatozoon spp. infect free-ranging jaguars (Panthera onca) in Brazil. J Parasitol. 2017; 103(3):243–50.

    Article  CAS  PubMed  Google Scholar 

  13. Hodžić A, Mrowietz N, Cezanne R, Bruckschwaiger P, Punz S, Habler VE, Tomsik V, Lazar J, Duscher GG, Glawischnig W, Fuehrer HP. Occurrence and diversity of arthropod-transmitted pathogens in red foxes (Vulpes vulpes) in western Austria, and possible vertical (transplacental) transmission ofHepatozoon canis. Parasitology. 2018; 145(3):335–44.

    Article  PubMed  Google Scholar 

  14. Tateno M, Sunahara A, Nakanishi N, Izawa M, Matsuo T, Setoguchi A, Endo Y. Molecular survey of arthropod-borne pathogens in ticks obtained from Japanese wildcats. Ticks Tick-borne Dis. 2015; 6(3):281–9.

    Article  PubMed  Google Scholar 

  15. Rafiqi SI, Kumar S, Reena KK, Garg R, Ram H, Karikalan M, Mahendran K, Pawde AM, Sharma AK, Banerjee PS. Molecular characterization of Hepatozoon sp. and Babesia sp. isolated from endangered Asiatic Lion (Panthera leo persica). Indian J Anim Sci. 2018; 88:662–6.

    CAS  Google Scholar 

  16. Kubo M, Jeong A, Kim SI, Kim YJ, Lee H, Kimura J, Agatsuma T, Sakai H, Yanai T. The first report of Hepatozoon species infection in leopard cats (Prionailurus bengalensis) in Korea. J Parasitol. 2010; 96(2):437–9.

    Article  PubMed  Google Scholar 

  17. Kamani J, Harrus S, Nachum-Biala Y, Gutiérrez R, Mumcuoglu KY, Baneth G. Prevalence of Hepatozoon and Sarcocystis spp. in rodents and their ectoparasites in Nigeria. Acta Trop. 2018; 187:124–8.

    Article  PubMed  Google Scholar 

  18. Ujvari B, Madsen T, Olsson M. High prevalence of Hepatozoon spp. (Apicomplexa, Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. J Parasitol. 2004; 90(3):670–2.

    Article  PubMed  Google Scholar 

  19. Guardone L, Ebani VV, Verin R, Nardoni S, Consolazione A, Bennett M, Mancianti F. Molecular detection of arthropod-borne pathogens in Eurasian badgers (Meles meles) from the United Kingdom. Animals. 2020; 10(3):446.

    Article  PubMed Central  Google Scholar 

  20. Meneses A, Alvarado G, Runnebaum M, Herrera M, Gutiérrez-Espeleta G, Chaves A. First Report of Hepatozoon procyonis in Raccoons from Costa Rica. Rev Cien Veterinarias. 2016; 34(1):51–4.

    Article  Google Scholar 

  21. Inokuma H, Okuda M, Ohno K, Shimoda K, Onishi T. Analysis of the 18S rRNA gene sequence of a Hepatozoon detected in two Japanese dogs. Vet Parasitol. 2002; 106(3):265–71.

    Article  CAS  PubMed  Google Scholar 

  22. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018; 35(6):1547–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kocan AA, Cummings CA, Panciera RJ, Mathew JS, Ewing SA, Barker RW. Naturally occurring and experimentally transmitted Hepatozoon americanum in coyotes from Oklahoma. J Wildl Dis. 2000; 36(1):149–53.

    Article  CAS  PubMed  Google Scholar 

  24. Penzhorn BL, Kjemtrup AM, López-Rebollar LM, Conrad PA. Babesia leo n. sp. from lions in the Kruger National Park, South Africa, and its relation to other small piroplasms. J Parasitol. 2001; 87(3):681–5.

    Article  CAS  PubMed  Google Scholar 

  25. Lauzi S, Maia JP, Epis S, Marcos R, Pereira C, Luzzago C, Santos M, Puente-Payo P, Giordano A, Pajoro M, Sironi G. Molecular detection of Anaplasma platys, Ehrlichia canis, Hepatozoon canis and Rickettsia monacensis in dogs from Maio Island of Cape Verde archipelago. Ticks Tick-borne Dis. 2016; 7(5):964–9.

    Article  PubMed  Google Scholar 

  26. Silva MR, Mattoso CR, Costa A, Saito ME, Tchaicka L, O’Dwyer LH. Rangelia vitalii and Hepatozoon canis coinfection in pampas fox Lycalopex gymnocercus from Santa Catarina State, Brazil. Rev Bras Parasitol Vet. 2018; 27:377–83.

    PubMed  Google Scholar 

  27. Baneth G, Weigler B. Retrospective case-control study of Hepatozoonosis in dogs in Israel. J Vet Intern Med. 1997; 11(6):365–70.

    Article  CAS  PubMed  Google Scholar 

  28. Thakur N, Chethan GE, Akhilesh AL, Kumari P, Shehzad M, Rajesh JB, Mahendran K, De UK, Banerjee PS. Therapeutic management of Hepatozoon canis induced acute hepatitis in a dog. J Entomol Zool Stud. 2018; 6(4):1037–9.

    Google Scholar 

  29. Attipa C, Neofytou K, Yiapanis C, Martínez-Orellana P, Baneth G, Nachum-Biala Y, Brooks-Brownlie H, Solano-Gallego L, Tasker S. Follow-up monitoring in a cat with leishmaniosis and coinfections with Hepatozoon felis and ‘Candidatus Mycoplasma haemominutum’. J Feline Med Surg Open Rep. 2017; 3(2):2055116917740454.

    Google Scholar 

  30. Skeldon N, Klaassen J, Hinds M. Diagnosis of Hepatozoon canis. Vet Rec. 2017; 180(5):124.

    Article  PubMed  Google Scholar 

  31. Allen KE, Little SE, Johnson EM, Hostetler J, Panciera RJ, Ewing SA. Treatment of Hepatozoon americanum infection: review of the literature and experimental evaluation of efficacy. Vet Ther Res Appl Vet Med. 2010; 11(4):E1–8.

    Google Scholar 

  32. Krampitz HE, Haberkorn A. Experimental treatment of Hepatozoon infections with the anticoccidial agent toltrazuril. J Vet Med Ser B. 1988; 35(1-10):131–7.

    Article  CAS  Google Scholar 

  33. Sarma K, Monda DB, Saravanan M, Kumar M, Mahendran K. Haemato-biochemical changes in Hepatozoon canis infected dog before and after therapeutic management. J Vet Parasitol. 2012; 26(1):35–8.

    Google Scholar 

  34. Abdullah AS, Sheikh-Omar AR, Baggot JD, Zamri M. Adverse effects of imidocarb dipropionate (Imizol\({\circledR }\)) in a dog. Vet Res Commun. 1984; 8(1):55–9.

    Article  CAS  PubMed  Google Scholar 

  35. Sasanelli M, Paradies P, Greco B, Eyal O, Zaza V, Baneth G. Failure of imidocarb dipropionate to eliminate Hepatozoon canis in naturally infected dogs based on parasitological and molecular evaluation methods. Vet Parasitol. 2010; 171(3-4):194–9.

    Article  CAS  PubMed  Google Scholar 

  36. Munson L, Terio KA, Kock R, Mlengeya T, Roelke ME, Dubovi E, Summers B, Sinclair AR, Packer C. Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. PloS ONE. 2008; 3(6):e2545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Farkas R, Solymosi N, Takács N, Hornyák Á, Hornok S, Nachum-Biala Y, Baneth G. First molecular evidence of Hepatozoon canis infection in red foxes and golden jackals from Hungary. Parasites Vectors. 2014; 7(1):1–7.

    Article  Google Scholar 

  38. Mitková B, Hrazdilová K, Steinbauer V, D’Amico G, Mihalca AD, Modrý D. Autochthonous Hepatozoon infection in hunting dogs and foxes from the Czech Republic. Parasitol Res. 2016; 115(11):4167–71.

    Article  PubMed  Google Scholar 

  39. Battisti E, Zanet S, Khalili S, Trisciuoglio A, Hertel B, Ferroglio E. Molecular survey on vector-borne pathogens in alpine wild carnivorans. Front Vet Sci. 2020; 7:1.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Ortuño A, Castellà J, Criado-Fornelio A, Buling A, Barba-Carretero JC. Molecular detection of a Hepatozoon species in stray cats from a feline colony in North-eastern Spain. Vet J. 2008; 177(1):134–5.

    Article  CAS  PubMed  Google Scholar 

  41. Nimisha M, Devassy JK, Pradeep RK, Pakideery V, Sruthi MK, Pious A, Kurbet PS, Amrutha BM, Chandrasekhar L, Deepa CK, Ajithkumar KG. Ticks and accompanying pathogens of domestic and wild animals of Kerala, South India. Exp Appl Acarol. 2019; 79(1):137–55.

    Article  CAS  PubMed  Google Scholar 

  42. Akyuz M, Kirman R, Guven E. Morphological and molecular data of Hepatozoon ursi in two brown bears (Ursus arctos) in Turkey. Folia Parasitol. 2020; 67:032.

    Article  CAS  Google Scholar 

  43. Orkun Ö, Emir H. Identification of tick-borne pathogens in ticks collected from wild animals in Turkey. Parasitol Res. 2020; 119(9):3083–91.

    Article  PubMed  Google Scholar 

  44. Moustafa MA, Sasaki A, Shimozuru M, Nakao R, Sashika M, Yamazaki K, Koike S, Tanaka J, Tamatani H, Yamanaka M, Ishinazaka T. Molecular detection of apicomplexan protozoa in Hokkaido brown bears (Ursus arctos yesoensis) and Japanese black bears (Ursus thibetanus japonicus). Parasitology Research. 2020; 119(11):3739–53.

    Article  PubMed  Google Scholar 

  45. Giannelli A, Latrofa MS, Nachum-Biala Y, Hodžić A, Greco G, Attanasi A, Annoscia G, Otranto D, Baneth G. Three different Hepatozoon species in domestic cats from southern Italy. Ticks Tick-borne Dis. 2017; 8(5):721–4.

    Article  PubMed  Google Scholar 

  46. Tateno M, Sunahara A, Nakanishi N, Izawa M, Matsuo T, Setoguchi A, Endo Y. Molecular survey of arthropod-borne pathogens in ticks obtained from Japanese wildcats. Ticks Tick-borne Dis. 2015; 6(3):281–9.

    Article  PubMed  Google Scholar 

  47. Kegler K, Nufer U, Alic A, Posthaus H, Olias P, Basso W. Fatal infection with emerging apicomplexan parasite Hepatozoon silvestris in a domestic cat. Parasites Vectors. 2018; 11(1):1–5.

    Article  Google Scholar 

  48. Hodžić A, Alić A, Prašović S, Otranto D, Baneth G, Duscher GG. Hepatozoon silvestris sp. nov.: morphological and molecular characterization of a new species of Hepatozoon (Adeleorina: Hepatozoidae) from the European wild cat (Felis silvestris silvestris). Parasitology. 2017; 144(5):650–61.

    Article  CAS  PubMed  Google Scholar 

  49. Starkey LA, Panciera RJ, Paras K, Allen KE, Reiskind MH, Reichard MV, Johnson EM, Little SE. Genetic diversity of Hepatozoon spp. in coyotes from the south-central United States. J Parasitol. 2013; 99(2):375–8.

    Article  PubMed  Google Scholar 

  50. Li Y, Wang C, Allen KE, Little SE, Ahluwalia SK, Gao D, Macintire DK, Blagburn BL, Kaltenboeck B. Diagnosis of canine Hepatozoon spp. infection by quantitative PCR. Vet Parasitol. 2008; 157(1-2):50–8.

    Article  CAS  PubMed  Google Scholar 

  51. Albrecht L, Merino EF, Hoffmann EH, Ferreira MU, de Mattos Ferreira RG, Osakabe AL, Dalla Martha RC, Ramharter M, Durham AM, Ferreira JE, Del Portillo HA. Extense variant gene family repertoire overlap in Western Amazon Plasmodium falciparum isolates. Mol Biochem Parasitol. 2006; 150(2):157–65.

    Article  CAS  PubMed  Google Scholar 

  52. Cyntia K. The Merck veterinary manual. White Station: Merck & Company, Incorporated; 2011.

    Google Scholar 

Download references

Acknowledgments

The authors acknowledge the kind approval of the Principal Chief Conservator of Forest (Wildlife) & Chief Wildlife Warden, Maharashtra State, for carrying out the research work. Forest Development Corporation of Maharashtra Ltd., Nagpur and Office of the Divisional Manager, Gorewada Project, Nagpur, for the facilities provided for the research. Director, Wildlife Research & Training Centre to facilitate the research work at WRTC, Gorewada, Nagpur.

Funding

The authors self-funded the study. The Corresponding author is not in receipt of any funding from research agencies in India or abroad.

Author information

Authors and Affiliations

  1. Wildlife Research & Training Centre, Gorewada, MAFSU, Nagpur Opp. Hindustan Lever Godown Square, Mahurzhari Road, Fetri, Nagpur, 441501, India

    S.M. Kolangath, S.V. Upadhye, V.M. Dhoot, M.D. Pawshe & A.S. Shalini

  2. Department of Biotechnology & Biochemistry, Saint Francis DeSales College, Seminary Hills, Nagpur, 440006, India

    R.M. Kolangath

Authors
  1. S.M. Kolangath
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S.V. Upadhye
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V.M. Dhoot
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M.D. Pawshe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A.S. Shalini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R.M. Kolangath
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KSM major contributor and involved in all phases of research, including writing the manuscript, performing the PCR, sequencing. USV and DVM supervised the study, collected samples, transported them to the lab, contributed to writing, PMD and SAS assisted in the clinical management of the Indian jackal. KRM performed phylogenetic analysis and assisted in manuscript preparation. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to S.M. Kolangath.

Ethics declarations

Ethics approval and consent to participate

The study is a clinical case, and the sample was drawn for diagnosis and treatment of the animal presented to Wildlife Research & Training Centre, Gorewada, Nagpur; hence does not draw the ethical committee approval. However, as per the existing Wildlife Protection Act, 1972 permission from Principal Chief Conservator of Forest (Wildlife), Maharashtra State was sought to vide No. Desk-22(8)/Res/CR-59(19-20)/3838/19-20, Nagpur, date 15 January 2020 for the study and publication of scientific findings. All the sample collection during the study has been executed as per ARRIVE guidelines.

Consent for publication

Not Applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kolangath, S., Upadhye, S., Dhoot, V. et al. Molecular investigation and clinical management of Hepatozoon Canis infection in an Indian jackal – a case report. BMC Vet Res 18, 144 (2022). https://doi.org/10.1186/s12917-022-03213-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12917-022-03213-8

Keywords

BMC Veterinary Research

ISSN: 1746-6148

Contact us