Phylogenetic Relationship of the Brazilian Isolates of the Rat Lungworm Angiostrongylus Cantonensis (Nematoda: Metastrongylidae) Employing Mitochondrial COI Gene Sequence Data

Overview

Journal Parasit Vectors

Publisher Biomed Central

Specialties Parasitology
Tropical Medicine

Date 2012 Nov 8

PMID 23130987

Citations 28

Authors

Taina C C Monte

Raquel O Simoes

Ana Paula M Oliveira

Clodoaldo F Novaes

Silvana C Thiengo

Alexandre J Silva

Pedro C Estrela

Arnaldo Maldonado Jr

Affiliations

Soon will be listed here.

Abstract

Background: The rat lungworm Angiostrongylus cantonensis can cause eosinophilic meningoencephalitis in humans. This nematode's main definitive hosts are rodents and its intermediate hosts are snails. This parasite was first described in China and currently is dispersed across several Pacific islands, Asia, Australia, Africa, some Caribbean islands and most recently in the Americas. Here, we report the genetic variability among A. cantonensis isolates from different geographical locations in Brazil using mitochondrial cytochrome c oxidase subunit I (COI) gene sequences.

Methods: The isolates of A. cantonensis were obtained from distinct geographical locations of Brazil. Genomic DNAs were extracted, amplified by polymerase reaction, purified and sequenced. A partial sequence of COI gene was determined to assess their phylogenetic relationship.

Results: The sequences of A. cantonensis were monophyletic. We identified a distinct clade that included all isolates of A. cantonensis from Brazil and Asia based on eight distinct haplotypes (ac1, ac2, ac3, ac4, ac5, ac6, ac7 and ac8) from a previous study. Interestingly, the Brazilian haplotype ac5 is clustered with isolates from Japan, and the Brazilian haplotype ac8 from Rio de Janeiro, São Paulo, Pará and Pernambuco states formed a distinct clade. There is a divergent Brazilian haplotype, which we named ac9, closely related to Chinese haplotype ac6 and Japanese haplotype ac7.

Conclusion: The genetic variation observed among Brazilian isolates supports the hypothesis that the appearance of A. cantonensis in Brazil is likely a result of multiple introductions of parasite-carrying rats, transported on ships due to active commerce with Africa and Asia during the European colonization period. The rapid spread of the intermediate host, Achatina fulica, also seems to have contributed to the dispersion of this parasite and the infection of the definitive host in different Brazilian regions.

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References

Jefferies R, Shaw S, Viney M, Morgan E . Angiostrongylus vasorum from South America and Europe represent distinct lineages. Parasitology. 2009; 136(1):107-15. DOI: 10.1017/S0031182008005258. View

Blouin M . Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int J Parasitol. 2002; 32(5):527-31. DOI: 10.1016/s0020-7519(01)00357-5. View

Lima A, Dornelas Mesquita S, Santos S, Aquino E, Rosa L, Duarte F . Alicata disease: neuroinfestation by Angiostrongylus cantonensis in Recife, Pernambuco, Brazil. Arq Neuropsiquiatr. 2010; 67(4):1093-6. DOI: 10.1590/s0004-282x2009000600025. View

Eamsobhana P, Lim P, Solano G, Zhang H, Gan X, Yong H . Molecular differentiation of Angiostrongylus taxa (Nematoda: Angiostrongylidae) by cytochrome c oxidase subunit I (COI) gene sequences. Acta Trop. 2010; 116(2):152-6. DOI: 10.1016/j.actatropica.2010.07.005. View

Simoes R, Monteiro F, Sanchez E, Thiengo S, Garcia J, Costa-Neto S . Endemic angiostrongyliasis, Rio de Janeiro, Brazil. Emerg Infect Dis. 2011; 17(7):1331-3. PMC: 3381414. DOI: 10.3201/eid1707.101822. View

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S . MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28(10):2731-9. PMC: 3203626. DOI: 10.1093/molbev/msr121. View

Ronquist F, Teslenko M, van der Mark P, Ayres D, Darling A, Hohna S . MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012; 61(3):539-42. PMC: 3329765. DOI: 10.1093/sysbio/sys029. View

Caldeira R, Mendonca C, Goveia C, Lenzi H, Graeff-Teixeira C, Lima W . First record of molluscs naturally infected with Angiostrongylus cantonensis (Chen, 1935) (Nematoda: Metastrongylidae) in Brazil. Mem Inst Oswaldo Cruz. 2007; 102(7):887-9. DOI: 10.1590/s0074-02762007000700018. View

Graeff-Teixeira C, da Silva A, Yoshimura K . Update on eosinophilic meningoencephalitis and its clinical relevance. Clin Microbiol Rev. 2009; 22(2):322-48, Table of Contents. PMC: 2668237. DOI: 10.1128/CMR.00044-08. View

10.

Bowles J, Blair D, McManus D . Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol. 1992; 54(2):165-73. DOI: 10.1016/0166-6851(92)90109-w. View

11.

Thompson J, Higgins D, Gibson T . CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22):4673-80. PMC: 308517. DOI: 10.1093/nar/22.22.4673. View

12.

Morassutti A, Graeff-Teixeira C . Interface Molecules of Angiostrongylus cantonensis: Their Role in Parasite Survival and Modulation of Host Defenses. Int J Inflam. 2012; 2012:512097. PMC: 3321291. DOI: 10.1155/2012/512097. View

13.

Foronda P, Lopez-Gonzalez M, Miquel J, Torres J, Segovia M, Abreu-Acosta N . Finding of Parastrongylus cantonensis (Chen, 1935) in Rattus rattus in Tenerife, Canary Islands (Spain). Acta Trop. 2010; 114(2):123-7. DOI: 10.1016/j.actatropica.2010.02.004. View

14.

Ohlweiler F, Guimaraes M, Takahashi F, Eduardo J . Current distribution of Achatina fulica, in the state of São Paulo including records of Aelurostrongylus abstrusus (Nematoda) larvae infestation. Rev Inst Med Trop Sao Paulo. 2011; 52(4):211-4. DOI: 10.1590/s0036-46652010000400009. View

15.

Graeff-Teixeira C . Expansion of Achatina fulica in Brazil and potential increased risk for angiostrongyliasis. Trans R Soc Trop Med Hyg. 2007; 101(8):743-4. DOI: 10.1016/j.trstmh.2007.03.012. View

16.

Martin-Alonso A, Foronda P, Quispe-Ricalde M, Feliu C, Valladares B . Seroprevalence of Angiostrongylus cantonensis in wild rodents from the Canary Islands. PLoS One. 2011; 6(11):e27747. PMC: 3215735. DOI: 10.1371/journal.pone.0027747. View

17.

Chen C, Kuo C, Lo C, Huang M, Wang Y, Wang W . Eosinophilic meningoencephalitis caused by Angiostrongylus cantonesis. QJM. 2011; 107(7):573-5. DOI: 10.1093/qjmed/hcr261. View

18.

Tokiwa T, Harunari T, Tanikawa T, Komatsu N, Koizumi N, Tung K . Phylogenetic relationships of rat lungworm, Angiostrongylus cantonensis, isolated from different geographical regions revealed widespread multiple lineages. Parasitol Int. 2012; 61(3):431-6. DOI: 10.1016/j.parint.2012.02.005. View

19.

Lunn J, Lee R, Smaller J, MacKay B, King T, Hunt G . Twenty two cases of canine neural angiostrongylosis in eastern Australia (2002-2005) and a review of the literature. Parasit Vectors. 2012; 5:70. PMC: 3361490. DOI: 10.1186/1756-3305-5-70. View

20.

Thiengo S, Maldonado A, Mota E, Torres E, Caldeira R, Carvalho O . The giant African snail Achatina fulica as natural intermediate host of Angiostrongylus cantonensis in Pernambuco, northeast Brazil. Acta Trop. 2010; 115(3):194-9. DOI: 10.1016/j.actatropica.2010.01.005. View