Abstract
Linguatula serrata is an important zoonotic parasite with worldwide distribution. The objective of the present study was to investigate the molecular characterization and phylogenetic analysis of nymphal stage of L. serrata from camels, goats and sheep in Iran. The mesenteric lymph nodes were collected from various ruminants including goats, sheep and camels at Isfahan and Shiraz slaughterhouses and the nymphs were identified using morphological characteristics. After DNA extraction, the 18 S rRNA and Cox1 genes were amplified by polymerase chain reaction. The sequencing of the genes was conducted using specific primers and a capillary DNA analyzer. The comparison of amplified sequences with existing data confirmed the presence of L. serrata with 99.6–100% nucleotide sequence similarity. Based on 18 S rRNA and Cox1 sequences, two isolates collected from sheep revealed 100% and 99.9% sequence identity, respectively. Also, three isolates from camel had 99.64–100% and 99.7–100% homology. Two isolates from sheep had 100% identity in their 18SrRNA gene and were categorized together, but showed 99.9% similarity in the Cox1 gene, not clustering together. Phylogenetic analysis of the Cox1 gene classified nearly all the isolates into L. arctica clade. It can be concluded that 18 S rRNA and Cox1 genes sequencing can be a proper method for the analysis of phylogenetic relationships of L. serrata among different hosts in different parts of Iran, possibly helpful for infection control and prevention.
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References
Alborzi A, Molayan PH, Akbari M (2013) Prevalence of Linguatula serrata nymphs in mesenteric lymph nodes of cattle and buffaloes slaughtered in Ahvaz abattoir, Iran. Iran J Parasitol 8:327
Beaver PC, Jung ROC, Cup EW (1984) Crustacea, linguatulid, millipeds, centipeds, scorpions, spiders, ticks and mites. In: Beaver PC, Jung ROC, Cup EW (eds) Clinical parasitology, 9st edn. Lea and Febiger, Philadelphia, pp 572–573
Christoffersen M, De Assis JE (2013) A systematic monograph of the recent Pentastomida, with a compilation of their host. Zool Med Leiden 87:1–206
Drabick JJ (1987) Pentastomiasis. Rev Infect Disease 9:1087–1094
EL-Hassan AM, Eltoum IA, ELAsha BMA (1991) The Marrara syndrome: isolation of Linguatula serrata nymphs from a patient and the viscera of goats. Trans R Soc Trop Med Hyg 85:309
Felsenstein J (1992) Estimating effective population size from samples of sequences: a bootstrap Monte Carlo integration method. Genome Res 60:209–220
Fonseca VG, Carvalho GR, Nichols B et al (2014) Metagenetic analysis of patterns of distribution and diversity of marine meiobenthic eukaryotes. Glob Ecol Biogeogr 1293–1302
Ghorashi SA, Tavassoli M, Peters A et al (2016) Phylogenetic relationships among Linguatula serrata isolates from Iran based on 18S rRNA and mitochondrial Cox1 gene sequences. Acta Parasitol 61:195–200
Gjerde B (2013) Phylogenetic position of Linguatula arctica and Linguatula serrata (Pentastomida) as inferred from the nuclear 18S rRNA gene and the mitochondrial cytochrome c oxidase subunit I gene. Parasitol Res 112:3517–3525
Haddadzadeh H, Athari SS, Hajimohammadi B (2009) The first record of Linguatula serrata infection of two-humped camel (Camelus bactrinus) in Iran. Iran J Parasitol 4:59–61
Hajipour N, Tavassoli M (2019) Prevalence and associated risk factors of Linguatula serrata infection in definitive and intermediate hosts in Iran and other countries: a systematic review. Vet Parasitol Reg Stud 16:100288
Hajipour N, Tavassoli M, Tayefi-Nasrabadi H et al (2016) Comparative evaluation of somatic proteins of the Nymphal Stage of Linguatula serrata isolated from goats and cattle in Northwest Iran. Bulg J Vet Med 19:242–246
Koehsler M, Walochnik J, Georgopoulos M et al (2011) Linguatula serrata tongue worm in human eye, Austria. Emerg Infect Diseases 17:870
Lazo R, Hidalgo E, Lazo J et al (1999) Ocular linguatuliasis in Ecuador: Case report and morphometric study of the larva of Linguatula serrata. Am J Trop Med Hyg 60:405–409
Lie AA, Liu Z, Hu SK et al (2014) Investigating microbial eukaryotic diversity from a global census: insights from a comparison of pyrotag and full-length sequences of 18S rRNA gene sequences. Appl Environ Microbiol 80(14):4363–4373
Mohammadi MA, Bamorovat M, Sharifi I et al (2020) Linguatula serrata in cattle in southeastern Iran: epidemiological, histopathological and phylogenetic profile and its zoonotic importance. Vet Parasitol Reg Stud 22:100465
Mohanta UK, Itagaki T (2017) Molecular characterization and phylogeny of Linguatula serrata (Pentastomida: Linguatulidae) based on the nuclear 18S rDNA and mitochondrial cytochrome c oxidase I gene. J Vet Med Sci 79:398–402
Møller OS (2009) Branchiura (Crustacea)-survey of historical literature and taxonomy. Arthropod Syst Phyol 67:41–55
Naude T, Pant S, Tavassoli M et al (2018) The complete mitochondrial genome of Linguatula serrata (tongue worm) isolated from a dog and phylogenetic analysis. Mitochondrial DNA Part B 3:357–358
Oluwasina OS, ThankGod OE, Augustine OO et al (2014) Linguatula serrata (Porocephalida: Linguatulidae) infection among client-owned dogs in Jalingo, North Eastern Nigeria: prevalence and public health implications. J Parasitol Res 2014; 1–5
Oryan A, Sadjjadi S, Mehrabani D et al (2008) The status of Linguatula serrata infection of stray dogs in Shiraz, Iran. Comp Clin Path 17:55–60
Raele DA, Petrella A, Troiano P, Cafiero MA (2022) Linguatula serrata (Fröhlich, 1789) in Gray Wolf (Canis lupus) from Italy: a neglected zoonotic parasite. Pathogens 11(12):1523
Razavi S, Shekarforoush SS, Izadi M (2004) Prevalence of Linguatula serrata nymphs in goats in Shiraz, Iran. Small Rumin Res 54:213–217
Rezaei F, Tavassoli M, Mahmoudian A (2011) Prevalence of Linguatula serrata infection among dogs (definitive host) and domestic ruminants (intermediate host) in the North West of Iran. Vet Med 56:561–567
Rezaei F, Tavassoli M, Javdani M (2012) Prevalence and morphological characterizations of Linguatula serrata nymphs in camels in Isfahan Province, Iran. Vet Res Forum 3:61–65
Sambrook J, Russell DW (2006) Purification of nucleic acids by extraction with phenol: chloroform. CSH Protoc. prot4455.
Shakerian A, Shekarforoush S, Rad HG (2008) Prevalence of Linguatula serrata nymphs in one-humped camel (Camelus dromedarius) in Najaf-Abad, Iran. Res Vet Sci 84:243–245
Shekarforoush SS, Razavi S, Izadi M (2004) Prevalence of Linguatula serrata nymphs in sheep in Shiraz, Iran. Small Rumin Res 52:99–101
Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Villedieu E, Sanchez R, Jepson R et al (2017) Nasal infestation by Linguatula serrata in a dog in the UK: a case report. J Small Anim Pract 58:183–186
Young E (1975) Pentastomiasis (Armillifer and Linguatula sp.) infestations of wild animals in the Kruger National Park. J S Afr Vet Assoc 46:335–336
Acknowledgements
We would like to thank Shiraz University for providing of facilities and financial supports. Our thanks are also extended to Dr Ehsan Rakhshanderoo, Dr Hossein Malekpour and Rasoul Sorbi for their kind assistance.
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This study was supported by a Grant from by Shiraz University, Iran.
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Yektaseresht, A., Razavi, S.M., Sebdani, M.M. et al. Molecular characterization and phylogenetic analysis of Linguatula serrata isolated from camels, sheep and goats in Iran. J Parasit Dis 47, 410–415 (2023). https://doi.org/10.1007/s12639-023-01587-6
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DOI: https://doi.org/10.1007/s12639-023-01587-6