A multifaceted approach to combatting the emergence of drug-resistant helminths

Conflict of interest statement

The authors declare that there is no conflict of interest.

Funding

This study received no extramural funding.

Data availability statement

The data supporting the findings of this study are available from the corresponding author upon request.

References

[1] Tenorio JCB, Heikal MF, Kafle A, Saichua P, Suttiprapa S. Benzimidazole resistance-associated mutations in the β-tubulin gene of hookworms: A systematic review. Parasitol Res 2024; 123(12): 405.

[2] Jimenez Castro PD, Venkatesan A, Redman E, Chen R, Malatesta A, Huff H, et al. Multiple drug resistance in hookworms infecting greyhound dogs in the USA. Int J Parasitol Drugs Drug Resist 2021; 17: 107-117.

[3] Venkatesan A, Castro PDJ, Morosetti A, Horvath H, Chen R, Redman E, et al. Molecular evidence of widespread benzimidazole drug resistance in Ancylostoma caninum from domestic dogs throughout the USA and discovery of a novel β-tubulin benzimidazole resistance mutation . PLoS Pathog 2023; 19(3): e1011146.

[4] Doyle SR, Laing R, Bartley D, Morrison A, Holroyd N, Maitland K, et al. Genomic landscape of drug response reveals mediators of anthelmintic resistance. Cell Rep 2022; 41(3): 111522.

[5] Zongze Z, Xin Y, Awais AA, Weiqiang L, Chunqun W, Di W, et al. Development of a tetra-primer ARMS-PCR for detecting the E198A SNP in the isotype-1 β-tubulin gene of Haemonchus contortus populations in China . Vet Parasitol 2018; 252: 127-130.

[6] Kapo N, Omeragić J, Goletić Š, Šabić E, Softić A, Smajlović A, et al. First report of benzimidazole resistance in field population of Haemonchus contortus from sheep, goats and cattle in Bosnia and Herzegovina . Pathogens 2024; 13(1): 77.

[7] Schnyder M, Torgerson PR, Schönmann M, Kohler L, Hertzberg H. Multiple anthelmintic resistance in Haemonchus contortus isolated from South African boer goats in Switzerland . Vet Parasitol 2005; 128(3): 285-290.

[8] Ng’etich AI, Amoah ID, Bux F, Kumari S. Anthelmintic resistance in soil-transmitted helminths: One-Health considerations. Parasitol Res 2023; 123(1): 62.

[9] Keller L, Welsche S, Patel C, Sayasone S, Ali SM, Ame SM, et al. Long-term outcomes of ivermectin-albendazole versus albendazole alone against soil-transmitted helminths: Results from randomized controlled trials in Lao PDR and Pemba Island, Tanzania. PLoS Negl Trop Dis 2021; 15(6): e0009561.

[10] Golenser J, Birman I, Gold D. Considering ivermectin for treatment of schistosomiasis. Parasitol Res 2024; 123(4): 180.

[11] Fordjour FA, Kwarteng A. The filarial and the antibiotics: Single or combination therapy using antibiotics for filariasis. [Online] Available from: https://www.frontiersin.org/articles/10.3389/fcimb.2022.1044412. [Accessed on 23 June 2024].

[12] Kellerová P, Navrátilová M, Nguyen LT, Dimunová D, Raisová Stuchlíková L, Štěrbová K, et al. UDP-Glycosyltransferases and albendazole metabolism in the jvenile stages of Haemonchus contortus . [Online] Available from: https://www.frontiersin.org/journals/physiology/articles/10.3389/fphys.2020.594116/full. [Accessed on 20 June 2024].

[13] Dimunová D, Navrátilová M, Kellerová P, Ambrož M, Skálová L, Matoušková P. The induction and inhibition of UDP-glycosyltransferases in Haemonchus contortus and their role in the metabolism of albendazole . Int J Parasitol Drugs Drug Resist 2022; 19: 56-64.

[14] Leutenegger CM, Lozoya CE, Tereski J, Savard C, Ogeer J, Lallier R. Emergence of Ancylostoma caninum parasites with the benzimidazole resistance F167Y polymorphism in the US dog population . Int J Parasitol Drugs Drug Resist 2023; 21: 131-140.

[15] Rashwan N, Bourguinat C, Keller K, Gunawardena NK, de Silva N, Prichard R. Isothermal Diagnostic assays for monitoring single nucleotide polymorphisms in Necator americanus associated with benzimidazole drug resistance . PLoS Negl Trop Dis 2016; 10(12): e0005113.

[16] Zhao H, Dong H, Zhao Q, Zhu S, Jia L, Zhang S, et al. Integrated application of transcriptomics and metabolomics provides insight into the mechanism of Eimeria tenella resistance to maduramycin . Int J Parasitol Drugs Drug Resist 2024; 24: 100526.

[17] Tuersong W, Liu X, Wang Y, Wu S, Qin P, Zhu S, et al. Comparative metabolome analyses of ivermectin-resistant and susceptible strains of Haemonchus contortus . Animals 2023; 13(3): 456.

[18] Hotez PJ, Diemert D, Bacon KM, Beaumier C, Bethony JM, Bottazzi ME, et al. The human hookworm vaccine. Vaccine 2013; 31(Suppl 2): B227-232.

[19] Puchner KP, Bottazzi ME, Periago V, Grobusch M, Maizels R, McCarthy J, et al. Vaccine value profile for Hookworm. [Online] Available from: https://www.sciencedirect.com/science/article/pii/S0264410X23005406. [Accessed on 23 June 2024].

[20] Diemert DJ, Zumer M, Campbell D, Grahek S, Li G, Peng J, et al. Safety and immunogenicity of the Na-APR-1 hookworm vaccine in infection-naïve adults. Vaccine 2022; 40(42): 6084-6092.

[21] Kafle A, Tenorio JCB, Mahato RK, Dhakal S, Heikal MF, Suttiprapa S. Construction and validation of a novel multi-epitope in silico vaccine design against the paramyosin protein of Opisthorchis viverrini using immunoinformatics analyses . Acta Tropica 2024; 260: 107389.

[22] Tenorio JCB, Heikal MF, Kafle A, Macalalad MAB, Orosco FL, Saichua P, et al. Unraveling the mechanisms of benzimidazole resistance in hookworms: A molecular docking and dynamics study. [Online] Available from: https://www.researchsquare.com/article/rs-4933910/v1. [Accessed on 11 October 2024].

[23] Inobaya M. Compliance to mass drug administration and the sustainable control of Schistosomiasis in the Philippines. [Online] Available from: https://research-repository.griffith.edu.au/handle/10072/371220. [Accessed on 19 August 2023].

[24] Philippine Department of Health. Administrative order 2006-0028: Strategic and operational framework for Establishing Integrated Helminth Control Program. [Online] Available from: https://doh.gov.ph/sites/default/files/health_programs/IHCP%20Operational%20and%20Strategic%20Framework%20-%20AO%202006-0028.pdf. [Accessed on 11 October 2024].

[25] Tangcalagan D, Daga C, Tan A, Reyes R, Macalinao MaL, Mationg ML, et al. The 2013-2015 nationwide prevalence survey of soil-transmitted helminths (STH) and schistosomiasis among school-age children in public schools in the Philippines. Pediatr Infect Dis J 2022; 23(1): 75-96.

[26] Becker SL, Liwanag HJ, Snyder JS, Akogun O, Jr VB, Freeman MC, et al. Toward the 2020 goal of soil-transmitted helminthiasis control and elimination. PLoS Negl Trop Dis 2018; 12(8): e0006606.