#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Genetic characterization of Angiostrongylus larvae and their intermediate host, Achatina fulica, in Thailand


Autoři: Abdulhakam Dumidae aff001;  Pichamon Janthu aff001;  Chanakan Subkrasae aff001;  Paron Dekumyoy aff002;  Aunchalee Thanwisai aff001;  Apichat Vitta aff001
Působiště autorů: Department of Microbiology and Parasitology, Faculty of Medical Science, Naresuan University, Phitsanulok, Thailand aff001;  Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Ratchavithi Rd, Ratchathewi, Bangkok, Thailand aff002;  Centre of Excellence in Medical Biotechnology (CEMB), Faculty of Medical Science, Naresuan University, Phitsanulok, Thailand aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223257

Souhrn

Angiostrongyliasis is a parasitic disease caused by nematodes of the genus Angiostrongylus. Distribution of this worm corresponds to the dispersal of its main intermediate host, the giant African land snail Achatina fulica. Genetic characterization can help identify parasitic pathogens and control the spreading of disease. The present study describes infection of A. fulica by Angiostrongylus, and provides a genetic outlook based on sequencing of specific regions. We collected 343 land snails from 22 provinces across six regions of Thailand between May 2017 and July 2018. Artificial digestion and Baermann’s technique were employed to isolate Angiostrongylus larvae. The worm and its intermediate host were identified by sequencing with specific nucleotide regions. Phylogenetic tree was constructed to evaluate the relationship with other isolates. A. fulica from Chaiyaphum province was infected with A. cantonensis, whereas snails collected from Phrae and Chiang Rai provinces were infected with A. malaysiensis. The maximum likelihood tree based on 74 A. fulica COI sequences revealed monophyletic groups and identified two haplotypes: AF1 and AF2. Only AF1, which is distributed in all regions of Thailand, harbored the larvae of A. cantonensis and A. malaysiensis. Two mitochondrial genes (COI and cytb) and two nuclear regions (ITS2 and SSU rRNA) were sequenced in 41 Angiostrongylus specimens. The COI gene indicated that A. cantonensis was closely related to the AC10 haplotype; whereas the cytb gene revealed two new haplotypes: AC19 and AC20. SSU rRNA was useful for the identification of A. cantonensis; whereas ITS2 was a good genetic marker for differentiating between A. cantonensis and A. malaysiensis. This study provides genetic information about the parasite Angiostrongylus and its snail intermediate host. The data in this work may be useful for further study on the identification of Angiostrongylus spp., the genetic relationship between intermediate host and parasite, and control of parasites.

Klíčová slova:

Haplotypes – Phylogenetic analysis – Polymerase chain reaction – Larvae – Ribosomal RNA – Thailand – Nucleotide sequencing – Snails


Zdroje

1. Wang QP, Lai DH, Zhu XQ, Chen XG, Lun ZR. Human angiostrongyliasis. Lancet Infect Dis. 2008; 8: 621–630. doi: 10.1016/S1473-3099(08)70229-9 18922484

2. Spratt DM. Species of Angiostrongylus (Nematoda: Metastrongyloidea) in wildlife: a review. Int J Parasitol Parasites Wildl. 2015; 4: 178–189. doi: 10.1016/j.ijppaw.2015.02.006 25853051

3. Prociv P, Spratt DM, Carlisle M.S. Neuro-angiostrongyliasis: unresolved issue. Int J Parasitol. 2000; 30: 1295–1303. doi: 10.1016/s0020-7519(00)00133-8 11113256

4. Diao Z, Wang J, Qi H, Li X, Zheng X, Yin C. Human ocular angiostrongyliasis: a literature review. Trop Doct. 2011; 41: 76–78. doi: 10.1258/td.2010.100294 21296846

5. Feng Y, Nawa Y, Sawanyavisuth K, Lv Z, Wu ZD. Comprehensive review of ocular angiostrongyliasis with special reference to optic neuritis. Korean J Parasitol. 2013; 51: 613–619. doi: 10.3347/kjp.2013.51.6.613 24516263

6. Rodriguez R, Dequi RM, Peruzzo L, Mesquita PM, Garcia E, Fornari F. Abdominal angiostrongyliasis: report of two cases with different clinical presentations. Rev Inst Med Trop Sao Paulo. 2008; 50: 339–341. doi: 10.1590/s0036-46652008000600005 19082375

7. Quirós JL, Jiménez E, Bonilla R, Arce I, Hernández C, Jiménez Y. Abdominal angiostrongyliasis with involvement of liver histopathologically confirmed: a case report. Rev Inst Med Trop Sao Paulo. 2011; 53: 219–222. doi: 10.1590/s0036-46652011000400008 21915466

8. Bhaibulaya M, Cross JH. Angiostrongylus malaysiensis (Nematoda: Metastrongylidae), a new species of rat lung-worm from Malaysia. Southeast Asian J Trop Med Public Health. 1971; 2: 527–533. 5144154

9. Rodpai R, Intapan PM, Thanchomnang T, Sanpool O, Sadaow L, Laymanivong S, et al. Angiostrongylus cantonensis and A. malaysiensis broadly overlap in Thailand, Lao PDR, Cambodia and Myanmar: a molecular survey of larvae in land snails. PLoS One. 2016; 11(8): e0161128. https://doi.org/10.1371/journal.pone.0161128 27513930

10. Ohbayashi M, Kamiya M, Bhaibulaya M. Studies on parasites fauna of Thailand. I two new metastrongylid nematodes, Angiostrongylus siamensis sp. n. and Thaistrongylus harinasutai gen. et. sp. n. (Metastrongyloidae): Angiostrongylidae from wild rats. Jpn J Vet Res. 1979; 27: 5–10. 529658

11. Eamsohana P. The rat lungworm Parastrongylus (= Angiostrongylus) cantonensis: parasitology, immunology, eosinophilic meningitis, epidemiology and laboratory diagnosis. Bangkok: Wankaew (IQ) Book Center; 2006.

12. Wan KS, Weng WC. 2004. Eosinophilic meningitis in a child raising snails as pets. Acta Trop. 2004; 90: 51–53. 14739022

13. Thiengo SC, Simões Rde O, Fernande MA, Maldonado AJr. Angiostrongylus cantonensis and rat lungworm disease in Brazil. Hawaii J Med Public Health. 2013; 72(Suppl 2): 18–22.

14. Tsai HC, Chen YS, Yen CM. Human parasitic meningitis caused by Angiostrongylus cantonensis infection in Taiwan. Hawaii J Med Public Health. 2013; 72(Suppl 2): 26–27.

15. Marquardt WC, Demaree RS, Grieve RB. Parasitology and vector biology. 2nd edn. California: Academic Press; 2000. p. 702.

16. Mead AR. The giant African snail: A problem in economic malacology. Chicago: The University of Chicago Press; 1961.

17. Venette RC, Larson M. Mini Risk Assessment Giant African Snail, Achatina fulica Bowdich [Gastropoda: Achatinidae]. 2004. Available from: http://www.aphis.usda.gov/plant_health/plant_pest_info/pest_detection/downloads/pra/afulicapra.pdf.

18. Mead AR. Pulmonates, Vol. 2B: Economic malacology with particular reference to Achatina fulica. London: Academic Press; 1979. p. 150.

19. Raut SK, Barker GM. Achatina fulica Bowdich and other Achatinidae as pests in tropical agriculture. In: Barker G.M. (Ed.). Molluscs as Crop Pests. Hamilton, New Zealand: CABI Publishing; 2002. pp. 55–114.

20. Alicata J. The presence of Angiostrongylus cantonensis in the islands of the Indian Ocean and probable role of the giant African snail, Achatina fulica, in the dispersal of the parasite to the Pacific islands. Can J Zool. 1966; 44: 1041–1049. doi: 10.1139/z66-111 5981486

21. Eamsobhana P, Yong HS, Song SL, Gan XX, Prasartvit A, Tungtrongchitr A. Molecular phylogeography and genetic diversity of Angiostrongylus cantonensis and A. malaysiensis (Nematoda: Angiostrongylidae) based on 66-kDa protein gene. Parasitol Int. 2019; 68: 24–30. doi: 10.1016/j.parint.2018.09.006 30267903

22. Foronda P, Lopez-Gonzalez M, Miquel J, Torres J, Segovia M, Abreu-Acosta N, et al. Finding of Parastrongylus cantonensis (Chen, 1935) in Rattus rattus in Tenerife, Canary Islands (Spain). Acta Trop. 2010; 114: 123–127. doi: 10.1016/j.actatropica.2010.02.004 20153283

23. Liu CY, Zhang RL, Chen MX, Li J, Ai L, Wu CY, et al. Characterization of Angiostrongylus cantonensis isolates from China by sequences of internal transcribed spacers of nuclear ribosomal DNA. J Anim Vet Adv. 2011; 10: 593–596.

24. Fontanilla IK, Wade CM. The small subunit (SSU) ribosomal (r) RNA gene as a genetic marker for identifying infective 3rd juvenile stage Angiostrongylus cantonensis. Acta Trop. 2008; 105: 181–186. doi: 10.1016/j.actatropica.2007.10.007 18061130

25. Eamsobhana P, Lim PE, Yong HS. Phylogenetics and systematics of Angiostrongylus lungworms and related taxa (Nematoda: Metastrongyloidea) inferred from the nuclear small subunit (SSU) ribosomal DNA sequences. J Helminthol. 2015; 89: 317–325. doi: 10.1017/S0022149X14000108 24622302

26. Vitta A, Srisongcram N, Thiproaj J, Wongma A, Polsut W, Fukruksa C, et al. Phylogeny of Angiostrongylus cantonensis in Thailand based on cytochrome c oxidase subunit I gene sequence. Southeast Asian J Trop Med Public Health. 2016; 47: 377–386. 27405119

27. Dusitsittipon S, Thaenkham U, Watthanakulpanich D, Adisakwattana P, Komalamisra C. Genetic differences in the rat lungworm, Angiostrongylus cantonensis (Nematoda: Angiostrongylidae), in Thailand. J Helminthol. 2015; 89: 545–551. doi: 10.1017/S0022149X14000388 24933508

28. Yong HS, Eamsobhana P, Song SL, Prasartvit A, Lim PE. Molecular phylogeography of Angiostrongylus cantonensis (Nematoda: Angiostrongylidae) and genetic relationships with congeners using cytochrome b gene marker. Acta Trop. 2015; 148: 66–71. doi: 10.1016/j.actatropica.2015.04.020 25930187

29. Schotman CYL. Data sheet on the Giant African Land Snail Achatina fulica Bowdich (Mollusca: Achatinidae). In: PROVEG No. 19. FAO Regional Office of Latin America and the Caribbean Plant Quarantine Action Program. 1989. pp. 16–21.

30. Jena C, Sarkar S, Jalaja N. Krupanidhi S. Molecular phylogenetic relations of Achatina fulica based on partial sequence of COI gene. Natl Acad Sci Lett 2017; 40(2). https://doi.org/10.1007/s40009-017-0538-5

31. Tokiwa T, Harunari T, Tanikawa T, Komatsu N, Koizumi N, Tung KC, et al. Phylogenetic relationships of rat lungworm, Angiostrongylus cantonensis, isolated from different geographical regions revealed widespread multiple lineages. Parasitol Int. 2012; 61: 431–436. doi: 10.1016/j.parint.2012.02.005 22387862

32. Kumar S, Stecher G, Tamura K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016; 33: 1870–1874. doi: 10.1093/molbev/msw054 27004904

33. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012; 61: 539–542. https://doi.org/10.1093/sysbio/sys029 22357727

34. Yong HS, Song SL, Eamsobhana P, Goh SY, Lim PE. Complete mitochondrial genome reveals genetic diversity of Angiostrongylus cantonensis (Nematoda: Angiostrongylidae). Acta Trop. 2015; 152: 157–164. doi: 10.1016/j.actatropica.2015.09.001 26348256

35. Ayyagari VS, Sreerama K. Evaluation of haplotype diversity of Achatina fulica (Lissachatina) [Bowdich] from Indian sub-continent by means of 16S rDNA sequence and its phylogenetic relationships with other global populations. 3 Biotech. 2017; 7(4): 252. https://doi.org/10.1007/s13205-017-0877-4 28721680

36. Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010; 10: 564–567. doi: 10.1111/j.1755-0998.2010.02847.x 21565059

37. Harinasuta C, Setasuban P, Radomyos P. Observations on Angiostrongylus cantonensis in rats and mollusks in Thailand. J Med Assoc Thai. 1965; 48: 158–172.

38. Setasuban P, Vajrasthira S, Harinasuta C. The preliminary observations on natural infection of rat lungworm (Angiostrongylus cantonensis) in rodents and intermediate host in Thailand. J Med Assoc Thai. 1968; 51: 156–157.

39. Pipitgool V, Sithithaworn P, Pongmuttasaya P, Hinz E. Angiostrongylus infections in rats and snails in northeast Thailand. Southeast Asian J Trop Med Public Health. 1997; 28: 190–193.

40. Tesana S, Srisawangwong T, Sithithaworn P, Laha T, Andrews R. Prevalence and intensity of infection with third stage larvae of Angiostrongylus cantonensis in mollusks from northeast Thailand. Am J Trop Med. Hyg. 2009; 80: 983–987. 19478262

41. Kim JR, Hayes KA, Yeung NW, Cowie RH. Correction: Diverse gastropod hosts of Angiostrongylus cantonensis, the rat lungworm, globally and with a focus on the Hawaiian Islands. PLOS One. 2018; 13(2): e0193556. https://doi.org/10.1371/journal.pone.0193556 29470538

42. Lv S, Zhang Y, Liu H-X, Hu L, Yang K, Steinmann P, et al. Invasive snails and an emerging infectious disease: eesults from the first national survey on Angiostrongylus cantonensis in China. PLoS Negl Trop Dis. 2009; 3(2): e368. https://doi.org/10.1371/journal.pntd.0000368 19190771

43. Kerdpreedee S. The giant African snail. Kasikorn. 1956; 29: 511–516.

44. Upatham S, Kruatrachue M, Baidikul V. Cultivation of the giant African snail, Achatina fulica. J Sci Soc. Thailand. 1988; 14: 25–40.

45. Fontanilla IKC, Sta. Maria IMP, Garcia JRM, Ghate H, Naggs F, Wade CM. Restricted genetic variation in populations of Achatina (Lissachatina) fulica outside of East Africa and the Indian Ocean Islands points to the Indian Ocean Islands as the earliest known common source. PLoS One. 2014; 9(9): e105151. https://doi.org/10.1371/journal.pone.0105151 25203830

46. Monte TC, Simões RO, Oliveira AP, Novaes CF, Thiengo SC, Silva AJ, et al. Phylogenetic relationship of the Brazilian isolates of the rat lungworm Angiostrongylus cantonensis (Nematoda: Metastrongylidae) employing mitochondrial COI gene sequence data. Parasit Vectors. 2012; 5: 248. https://doi.org/10.1186/1756-3305-5-248. 23130987

47. Eamsobhana P, Lim PE, Solano G, Zhang H, Gan X, Yong HS. Molecular differentiation of Angiostrongylus taxa (Nematoda: Angiostrongylidae) by cytochrome c oxidase subunit I (COI) gene sequences. Acta Trop. 2010; 116: 152–156. doi: 10.1016/j.actatropica.2010.07.005 20654571

48. Červená B, Modrý D, Fecková B, Hrazdilová K, Foronda P, Alonso AM, et al. Low diversity of Angiostrongylus cantonensis complete mitochondrial DNA sequences from Australia, Hawaii, French Polynesia and the Canary Islands revealed using whole genome next-generation sequencing. Parasit Vectors. 2019; 12(1): 241. https://doi.org/10.1186/s13071-019-3491-y. 31097040

49. Jefferies R, Shaw SE, Viney ME, Morgan ER. Angiostrongylus vasorum from South America and Europe represent distinct lineages. Parasitology. 2009; 136: 107–115. doi: 10.1017/S0031182008005258 19126274


Článok vyšiel v časopise

PLOS One


2019 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#