Molecular detection of Borrelia spp. (Spirochaetales: Borreliaceae) in ticks (Acari: Ixodidae) collected from tortoises in Java, Indonesia

##plugins.themes.bootstrap3.article.main##

HANA FAIZAH SOPHIA
SUPRIYONO
SUSI SOVIANA
DIMAS NOVIANTO
UPIK KESUMAWATI HADI

Abstract

Abstract. Sophia HF, Supriyono, Soviana S, Novianto D, Hadi UK. 2023. Molecular detection of Borrelia spp. (Spirochaetales: Borreliaceae) in ticks (Acari: Ixodidae) collected from tortoises in Java, Indonesia. Biodiveritas 24: 6852-6857. Reptiles are known hosts of various tick species, many of which are zoonotic and pose veterinary and public health risks. Amblyomma ticks frequently parasitize reptiles and are potential vectors of zoonoses. This study aimed to investigate the prevalence of tick infestations and to identify Borrelia species infections in ticks found on tortoises. One hundred six tortoise hosts in three provinces in Indonesia. DNA extraction and Borrelia species were detected using conventional PCR techniques. The results revealed the presence of nineteen hard-bodied ticks on Chelonoidis carbonarius Spix, 1824, Chelonoidis denticulatus Linnaeus, 1766, and Geochelone sulcata Miller, 1779. All the ticks collected were identified as Amblyomma sparsum Neumann 1899, and the prevalence of A. sparsum infestations on tortoises in this study was 7.55%. Borrelia spp. was detected in some of the A. sparsum ticks infesting tortoises. Subsequent sequencing unveiled two distinct reptile-associated (REP) borrelia strains. This study sheds light on the tick infestation patterns and the potential transmission of Borrelia species among tortoises kept as exotic pets in urban areas by A. sparsum ticks. The findings provide valuable insights into the bioecology of ticks and the associated health risks they pose to reptiles, thereby contributing to our understanding of zoonotic disease dynamics in the region.

##plugins.themes.bootstrap3.article.details##

References
Andoh M, Sakata A, Takano A, Kawabata H, Fujita H, Une Y, Goka K, Kishimoto T, Ando S. 2015. Detection of Rickettsia and Ehrlichia spp. in ticks associated with exotic reptiles and amphibians imported into Japan. PLoS ONE 10 (7): e0133700. DOI: 10.1371/journal.pone.0133700.
Bizhga B, Sönmez B, Bardhaj L, Sherifi K, Gündemir O, Duro S. 2022. Hyalomma aegyptium the dominant hard tick in tortoises Tesdudo hermanni boettgeri found in different regions of Albania. Intl J Parasitol: Parasite Wildl 17: 199-204. DOI: 10.1016/j.ijppaw.2022.02.002.
Colunga-Salas P, Sánchez-Montes S, Ochoa-Ochoa LM, Grostieta E, Becker I. 2021. Molecular detection of the reptile-associated Borrelia group in Amblyomma dissimile. Mex Med Vet Entomol 35 (2): 202-206. DOI: 10.1111/mve.12478.
Dantas-Torres F, Martins TF, Muñoz-Leal S, Onofrio VC, Barros-Battesti DM. 2019. Ticks (Ixodida: Argasidae, Ixodidae) of Brazil: Updated species checklist and taxonomic keys. Ticks Tick-Borne Dis 10: 101252. DOI: 10.1016/j.ttbdis.2019.06.012.
Dantas-Torres F, Otranto D. 2016. Best practices for preventing vector-borne diseases in dogs and humans. Trend Parasitol 32 (1): 43-55. DOI: 10.1016/j.pt.2015.09.004.
Gofton AW, Popa-Baez A, Takano A, Soennichsen K, Michie M, Short M, Supriyono, Pascoe J, Cusbert S, Mulley R. 2023. Characterisation and comparative genomics of three new Varanus-associated Borrelia spp. from Indonesia and Australia. Parasites Vectors 16 (1): 317. DOI: 10.1186/s13071-023-05937-4.
Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Pena A, Horak IG, Shao R, Barker SC. 2014. The Hard Ticks of The World (Acari: Ixodida: Ixodidae). Springer, Dordrecht. DOI: 10.1007/978-94-007-7497-1.
Güner ES, Watanabe, M., Hashimoto N, Kadosaka T, Kawamura Y, Ezaki T, Kawabata H, Imai Y, Kaneda K, Masuzawa T. 2004. Borrelia turcica sp. nov., isolated from the hard tick Hyalomma aegyptium in Turkey. Intl J Syst Evol Microbiol 54 (5): 1649-1652. DOI: 10.1099/ijs.0.03050-0.
Halajian A, Palomar AM, Portillo A, Heyne H, Luus-Powell WJ, Oteo JA. 2016. Investigation of Rickettsia, Coxiella burnetii and Bartonella in ticks from animals in South Africa. Ticks Tick-Borne Dis 7 (2): 361-366. DOI: 10.1016/j.ttbdis.2015.12.008.
Hilderink MH, de Winter II. 2021. No need to beat around the bushmeat-the role of wildlife trade and conservation initiatives in the emergence of zoonotic diseases. Heliyon 7 (7): 1-10. DOI: 10.1016/j.heliyon.2021.e07692.
Horak IG, Heyne H, Williams R, Gallivan GJ, Spickett AM, Bezuidenhout JD, Estrada-Peña A. 2018. The Ixodid Ticks (Acari: Ixodidae) of Southern Africa. Springer, Cham. DOI: 10.1007/978-3-319-70642-9.
Kaenkan W, Nooma W, Chelong I-A, Baimai V, Trinachartvanit W, Ahantarig A. 2020. Reptile-associated Borrelia spp. in Amblyomma ticks. Thail Ticks Tick-Borne Dis 11: 101315. DOI: 10.1016/j.ttbdis.2019.101315.
Katmono WD, Prayoga SF, Oktaviana V, Fikri F. 2019. Laporan kasus: Amblyomma sp. pada ular sanca kembang (Python reticulatus) di Banyuwangi Reptile Community. Jurnal Medik Veteriner 2 (2): 140-144. DOI: 10.20473/jmv.vol2.iss2.2019.140-144. [Indonesian]
Kho KL, Koh FX, Tay ST. 2015. Molecular evidence of potential novel spotted fever group rickettsiae, Anaplasma and Ehrlichia species in Amblyomma ticks parasitizing wild snakes. Parasites Vectors 8: 112. DOI: 10.1186/s13071-015-0719-3.
Kireçci E, Özer A, Balkaya ?, Tani? H, Sümeyra D. 2013. Identification of ticks on tortoises (Testudo graeca) and investigation of some pathogens in these ticks in Kahramanmara?, Turkey. KSU J Nat Sci 16 (1): 42-46.
Kr?mar S, Klobu?ar A, Vucelja M, Boljfeti? M, Ku?ini? M, Madi? J, Cvek M, Ma?ari? BB. 2022. DNA barcoding of hard ticks (Ixodidae), notes on distribution of vector species and new faunal record for Croatia. Tick Tick-Borne Dis 13 (3): 101920. DOI: 10.1016/j.ttbdis.2022.101920.
Luo J, Ren QY, Chen Z, Liu WG, Qu ZQ, Xiao RH, Chen RG, Lin H, Wu ZG, Luo JX, Yin H, Wang H. 2019. Comparative analysis of microRNA profiles between wild and cultured Haemaphysalis longicornis (Acari, Ixodidae) ticks. Parasite 26 (18): 1-9. DOI: 10.1051/parasite/2019018.
Mofokeng LS, Smit NJ, Cook CA. 2022. Molecular detection of tick-borne bacteria from Amblyomma (Acari: Ixodidae) ticks collected from reptiles in South Africa. Microorganisms 10 (10): 1923. DOI: 10.3390/microorganisms10101923.
Morales-Diaz J, Colunga-Salas P, Romero-Salas D, Sánchez-Montes S, Estrada-Souza IM, Ochoa-Ochoa LM, Becker I, Flores-Primo A, Cruz-Romero A. 2020. Molecular detection of reptile-associated Borrelia in Boa constrictor (Squamata: Boidae) from Veracruz. Mex Acta Trop 205: 105422. DOI: 10.1016/j.actatropica.2020.105422.
Nicholson WL, Sonenshine DE, Noden BH, Brown RN. 2019. Ticks (Ixodida). In: Mullen GR, Durden LA (eds). Medical and Veterinary Entomology. 3rd ed. Academic Press, London. DOI: 10.1016/B978-0-12-814043-7.00027-3.
Ogrzewalska M, Machado C, Rozental T, Forneas D, Cunha LE, de Lemos ERS. 2019. Microorganisms in the ticks Amblyomma dissimile Koch 1844 and Amblyomma rotundatum Koch 1844 collected from snakes in Brazil. Med Vet Entomol 33 (1): 154-161. DOI: 10.1111/mve.12341.
Omondi D. Masiga DK, Fielding BC, Kariuki E, Ajamma YU, Mwamuye MM, Ouso DO, Villinger J. 2017. Molecular detection of tick-borne pathogen diversities in ticks from livestock and reptiles along the shores and adjacent islands of Lake Victoria and Lake Baringo. Kenya. Front Vet Sci 4: 73. DOI: 10.3389/fvets.2017.00073.
Panetta JL, Šíma Sima R, Calvani NED, Hajdušek O, Chandra S, Panuccio J, Šlapeta J. 2017. Reptile-associated Borrelia species in the goanna tick (Bothriocroton undatum) from Sydney, Australia. Parasites Vectors 10 (1): 616. DOI: 10.1186/s13071-017-2579-5.
Parola P, Raoult D. 2001. Ticks and tick-borne bacterial diseases in humans: An emerging infectious threat. Clin Infect Dis 32 (6): 897-928. DOI: 10.1086/319347.
Putranto DI, Yuda P, Zahida F. 2016. Keanekaragaman reptil impor di Yogyakarta. Biota 1 (3):117-125. DOI: 10.24002/biota.v1i3.1228. [Indonesian]
Santodomingo A, Cotes-Perdomo A, Foley J, Castro LR. 2018. Rickettsial infection in ticks (Acari: Ixodidae) from reptiles in the Colombian Caribbean. Ticks Tick-Borne Dis 9 (3): 623-628. DOI: 10.1016/j.ttbdis.2018.02.003.
Suardana IW. 2015. Buku Ajar Zoonosis: Penyakit Menular dari Hewan ke Manusia. PT Kanisius, Depok. [Indonesian]
Sumrandee C, Hirunkanokpun S, Grubhoffer L, Baimai V, Trinachartvanit W, Ahantarig A. 2014. Phylogenetic relationships of Francisella-like endosymbionts detected in two species of Amblyomma from snakes in Thailand. Ticks Tick-Borne Dis 5 (1): 29-32. DOI: 10.1016/j.ttbdis.2013.08.001.
Supriyono, Takano A, Kuwata R, Shimoda H, Hadi UK, Setiyono A, Agungpriyono S, Maeda S. 2019. Detection and isolation of tick-borne bacteria (Anaplasma spp., Rickettsia spp., and Borrelia spp.) in Amblyomma varanense ticks on lizard (Varanus salvator). Microbiol Immunol 63 (8): 1-6. DOI: 10.1111/1348-0421.12721.
Takano A, Fujita H, Kadosaka T, Konnai S, Tajima T, Watanabe H, Ohnishi M, Kawabata H. 2011. Characterization of reptile-associated Borrelia sp. in the vector tick, Amblyomma geoemydae, and its association with Lyme disease and relapsing fever Borrelia spp. Environ Microbiol Rep 3 (5): 632-637. DOI: 10.1111/j.1758-2229.2011.00280.x.
Trinachartvanit W, Hirunkanokpun S, Sudsangiem R, Lijuan W, Boonkusol D, Baimai V, Ahantarig A. 2016. Borrelia sp. phylogenetically different from Lyme disease- and relapsing fever-related Borrelia spp. in Amblyomma varanense from Python reticulatus. Parasites Vectors 9: 359. DOI: 10.1186/s13071-016-1629-8.
Walker JB. 1991. A review of ixodid ticks (Acari, Ixodidae) occurring in southern Africa. Onderstepoort 1 Vet Res 58 (2): 81-105.
Wang G. 2015. Borrelia burgdorferi and Other Borrelia Species. In: Tang, YW, Sussman M, Liu D, Poxton I, Schwartzman J (eds). Molecular Medical Microbiology (Second Edition). Academic Press, London. DOI: 10.1016/B978-0-12-397169-2.00104-9.

Most read articles by the same author(s)