First identification of the benzimidazole resistance-associated F200Y SNP in the beta-tubulin gene in Ascaris lumbricoides
Autoři:
Luis Fernando Viana Furtado aff001; Celi da Silva Medeiros aff001; Luciana Werneck Zuccherato aff001; William Pereira Alves aff001; Valéria Nayara Gomes Mendes de Oliveira aff001; Vivian Jordania da Silva aff001; Guilherme Silva Miranda aff001; Ricardo Toshio Fujiwara aff001; Élida Mara Leite Rabelo aff001
Působiště autorů:
Departamento de Parasitologia, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
aff001
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0224108
Souhrn
The main control strategy for Ascaris lumbricoides is mass drug administration (especially with benzimidazoles), which can select strains of parasites resistant to treatment. Mutations in the beta-tubulin isotype-1 gene at codons 167, 198 and 200 have been linked to benzimidazole resistance in several nematodes. The mutation in codon 200 is the most frequent in different species of parasites, as previously observed in Necator americanus and Trichuris trichiura; however, this mutation has never been found in populations of A. lumbricoides. This study aimed to screen for single nucleotide polymorphisms (SNPs) in the beta-tubulin isotype-1 gene at codon 200 in A. lumbricoides. We developed a technique based on an amplification refractory mutation system (ARMS-PCR) for the analysis of 854 single A. lumbricoides eggs collected from 68 human stool samples from seven Brazilian states. We detected the mutation in codon 200 at a frequency of 0.5% (4/854). This is the first report of this mutation in A. lumbricoides. Although the observed frequency is low, its presence indicates that these parasite populations have the potential to develop high levels of resistance in the future. The methodology proposed here provides a powerful tool to screen for the emergence of anthelmintic resistance mutations in parasitic nematode populations.
Klíčová slova:
Helminths – Mutation detection – Polymerase chain reaction – Ascaris lumbricoides – Amplification-refractory mutation system analysis – Benzimidazoles – Genetic annealing – Veterinary parasitology
Zdroje
1. WHO. Investing to overcome the global impact of neglected tropical diseases. Third WHO report on neglected tropical diseases. Geneva: World Health Organization, 2015.
2. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014;7: 37. doi: 10.1186/1756-3305-7-37 24447578
3. Jourdan PM, Lamberton PHL, Fenwick A, Addiss DG. Soil-transmitted helminth infections. Lancet. 2018;391(10117): 252–265. doi: 10.1016/S0140-6736(17)31930-X 28882382
4. Kwa MS, Veenstra JG, Roos MH. Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in beta-tubulin isotype 1. Mol Biochem Parasitol. 1994;63(2): 299–303. doi: 10.1016/0166-6851(94)90066-3 7911975
5. Prichard R. Genetic variability following selection of Haemonchus contortus with anthelmintics. Trends Parasitol. 2001;17(9): 445–453. 11530357
6. Ghisi M, Kaminsky R, Maser P. Phenotyping and genotyping of Haemonchus contortus isolates reveals a new putative candidate mutation for benzimidazole resistance in nematodes. Vet Parasitol. 2007;144(3–4): 313–320. doi: 10.1016/j.vetpar.2006.10.003 17101226
7. Diawara A, Drake LJ, Suswillo RR, Kihara J, Bundy DA, Scott ME, et al. Assays to detect beta-tubulin codon 200 polymorphism in Trichuris trichiura and Ascaris lumbricoides. PLoS Negl Trop Dis. 2009;3(3): e397. doi: 10.1371/journal.pntd.0000397 19308251
8. Rashwan N, Scott M, Prichard R. Rapid Genotyping of β-tubulin Polymorphisms in Trichuris trichiura and Ascaris lumbricoides. PLoS Negl Trop Dis. 2017;11(1): e0005205. doi: 10.1371/journal.pntd.0005205 28081124
9. McKay GJ, Cooke LR. A PCR-based method to characterise and identify benzimidazole resistance in Helminthosporium solani. FEMS Microbiol Lett. 1997;152(2): 371–378. doi: 10.1111/j.1574-6968.1997.tb10454.x 9231430
10. Diawara A, Halpenny CM, Churcher TS, Mwandawiro C, Kihara J, Kaplan RM, et al. Association between response to albendazole treatment and beta-tubulin genotype frequencies in soil-transmitted helminths. PLoS Negl Trop Dis. 2013;7(5): e2247. doi: 10.1371/journal.pntd.0002247 23738029
11. Zuccherato LW, Furtado LF, Medeiros CDS, Pinheiro CDS, Rabelo ÉM. PCR-RFLP screening of polymorphisms associated with benzimidazole resistance in Necator americanus and Ascaris lumbricoides from different geographical regions in Brazil. PLoS Negl Trop Dis. 2018;12(9): e0006766. doi: 10.1371/journal.pntd.0006766 30222749
12. Tarbiat B, Jansson DS, Tydén E, Höglund J. Evaluation of benzimidazole resistance status in Ascaridia galli. Parasitology. 2017;144(10): 1338–1345. doi: 10.1017/S0031182017000531 28514980
13. Tydén E, Engström A, Morrison DA, Höglund J. Sequencing of the β-tubulin genes in the ascarid nematodes Parascaris equorum and Ascaridia galli. Mol Biochem Parasitol. 2013;190(1): 38–43. doi: 10.1016/j.molbiopara.2013.05.003 23685342
14. Tydén E, Dahlberg J, Karlberg O, Höglund J. Deep amplicon sequencing of preselected isolates of Parascaris equorum in β-tubulin codons associated with benzimidazole resistance in other nematodes. Parasit Vectors. 2014;7:410. doi: 10.1186/1756-3305-7-410 25175357
15. Barreto ML, Genser B, Strina A, Teixeira MG, Assis AM, Rego RF, et al. Impact of a citywide sanitation program in Northeast Brazil on intestinal parasites infection in young children. Environ Health Perspect. 2010;118(11): 1637–1642. doi: 10.1289/ehp.1002058 20705544
16. Zani LC, Favre TC, Pieri OS, Barbosa CS. Impact of antihelminthic treatment on infection by Ascaris lumbricoides, Trichuris trichiura and hookworms in Covas, a rural community of Pernambuco, Brazil. Rev Inst Med Trop Sao Paulo. 2004;46(2): 63–71. doi: 10.1590/s0036-46652004000200002 15141272
17. Furtado LF, Rabelo EM. Molecular analysis of the F167Y SNP in the beta-tubulin gene by screening genotypes of two Ancylostoma caninum populations. Vet Parasitol. 2015;210(1–2): 114–117. doi: 10.1016/j.vetpar.2015.03.018 25865406
18. Furtado LF, Bello AC, dos Santos HA, Carvalho MR, Rabelo EM. First identification of the F200Y SNP in the beta-tubulin gene linked to benzimidazole resistance in Ancylostoma caninum. Vet Parasitol. 2014;206(3–4): 313–316. doi: 10.1016/j.vetpar.2014.10.021 25468029
19. Furtado LF, Rabelo ÉM. Development of a new amplification-refractory mutation system for detection of a single nucleotide polymorphism linked to drug resistance in Ancylostoma caninum. Genet Mol Res. 2015;14(2): 5103–5111. doi: 10.4238/2015.May.12.13 26125702
20. Furtado LF, Alves WP, Moreira TB, Costa LM Junior, Miranda RRC, Rabelo EML. Standardization and application of the tetraprimer ARMS-PCR technique for screening of the E198A SNP in the beta-tubulin gene of hookworm populations in Brazil. Vet Parasitol. 2016;224: 65–67. doi: 10.1016/j.vetpar.2016.05.013 27270392
21. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci. 1977;74: 5463–5467. doi: 10.1073/pnas.74.12.5463 271968
22. Humphries D, Nguyen S, Boakye D, Wilson M, Cappello M. The promise and pitfalls of mass drug administration to control intestinal helminth infections. Curr Opin Infect Dis. 2012;25(5): 584–589. doi: 10.1097/QCO.0b013e328357e4cf 22903231
23. Furtado LF, de Paiva Bello ACP, Rabelo ÉML. Benzimidazole resistance in helminths: From problem to diagnosis. Acta Trop. 2016;162: 95–102. doi: 10.1016/j.actatropica.2016.06.021 27338184
24. Müller I, Beyleveld L, Gerber M, Pühse U, du Randt R, Utzinger J, et al. Low efficacy of albendazole against Trichuris trichiura infection in school children from Port Elizabeth, South Africa. Trans R Soc Trop Med Hyg. 2016;110(11): 676–678.
25. Clarke NE, Doi SAR, Wangdi K, Chen Y, Clements ACA, Nery SV. Efficacy of Anthelminthic Drugs and Drug Combinations Against Soil-transmitted Helminths: A Systematic Review and Network Meta-analysis. Clin Infect Dis. 2019;68(1): 96–105. doi: 10.1093/cid/ciy423 29788074
26. Adugna S, Kebede Y, Moges F, Tiruneh M. Efficacy of mebendazole and albendazole for Ascaris lumbricoides and hookworm infections in an area with long time exposure for antihelminthes, Northwest Ethiopia. Ethiop Med J. 2007;45(3): 301–306. 18330331
27. Cabada MM, Lopez M, Arque E, Clinton White A. Prevalence of soil-transmitted helminths after mass albendazole administration in an indigenous community of the Manu jungle in Peru. Pathog Glob Health. 2014;108(4): 200–205. doi: 10.1179/2047773214Y.0000000142 24934795
28. Krücken J, Fraundorfer K, Mugisha JC, Ramünke S, Sifft KC, Geus D, et al. Reduced efficacy of albendazole against Ascaris lumbricoides in Rwandan schoolchildren. Int J Parasitol Drugs Drug Resist. 2017;7(3): 262–271. doi: 10.1016/j.ijpddr.2017.06.001 28697451
29. Dixit AK, Das G, Dixit P, Singh AP, Kumbhakar NK, Sankar M, et al. An assessment of benzimidazole resistance against caprine nematodes in Central India. Trop Anim Health Prod; 2017;49(7): 1471–1478. doi: 10.1007/s11250-017-1349-x 28717849
30. Mohanraj K, Subhadra S, Kalyanasundaram A, Ilangopathy M, Raman M. Genotyping of benzimidazole resistant and susceptible isolates of Haemonchus contortus from sheep by allele specific PCR. J Parasit Dis. 2017;41(1): 282–288. doi: 10.1007/s12639-016-0793-2 28316426
31. Furtado LF, Magalhães JGS, Rabelo ÉML. Standardization and application of a modified RFLP-PCR methodology for analysis of polymorphisms linked to treatment resistance in Ancylostoma braziliense. Parasit Vectors. 2018; 11(1): 540. doi: 10.1186/s13071-018-3125-9 30301454
32. Schwenkenbecher JM, Kaplan RM. Real-time PCR assays for monitoring benzimidazole resistance-associated mutations in Ancylostoma caninum. Exp Parasitol. 2009;122: 6–10. doi: 10.1016/j.exppara.2009.01.006 19545525
33. Albonico M, Wright V, Bickle Q. Molecular analysis of the beta-tubulin gene of human hookworms as a basis for possible benzimidazole resistance on Pemba Island. Mol Biochem Parasitol. 2004;134(2): 281–284. doi: 10.1016/j.molbiopara.2003.12.008 15003848
34. Niciura SC, Veríssimo CJ, Gromboni JG, Rocha MI, de Mello SS, Barbosa CM, et al. F200Y polymorphism in the β-tubulin gene in field isolates of Haemonchus contortus and risk factors of sheep flock management practices related to anthelmintic resistance. Vet Parasitol. 2012;190(3–4): 608–612. doi: 10.1016/j.vetpar.2012.07.016 22858226
35. Furtado LF, Aguiar PH, Zuccherato LW, Teixeira TT, Alves WP, Silva VJ, et al. Albendazole resistance induced in Ancylostoma ceylanicum is not due to single-nucleotide polymorphisms (SNPs) at codons 167, 198, or 200 of the beta-tubulin gene, indicating another resistance mechanism. Parasitol Res. 2019;118(3): 837–849. doi: 10.1007/s00436-019-06218-9 30697644
36. Ota M, Fukushima H, Kulski JK, Inoko H. Single nucleotide polymorphism detection by polymerase chain reaction-restriction fragment length polymorphism. Nat Protoc. 2007;2: 2857–2864. doi: 10.1038/nprot.2007.407 18007620
37. Baltrušis P, Halvarsson P, Höglund J. Exploring benzimidazole resistance in Haemonchus contortus by next generation sequencing and droplet digital PCR. Int J Parasitol Drugs Drug Resist. 2018;8(3):411–419. doi: 10.1016/j.ijpddr.2018.09.003 30266023
Článek vyšel v časopise
PLOS One
2019 Číslo 10
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