Does exposure to pyriproxyfen cause microcephaly? a systematic review of toxic effects in two animal models
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Published
Jan 28, 2023
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Abstract
Objective: This study aimed to evaluate studies on the toxicity of pyriproxyfen in animal models of zebrafish and murine and its relationship with microcephaly. Methods: The keywords pyriproxyfen and toxicity were used for the search on Pubmed, Scorpus, ScieLo and ScienceDirect platforms. Articles that used the keywords in the title or abstract were selected. Inclusion criteria were: articles in English or Portuguese that described an experimental study in vivo or in vitro with zebrafish (Danio rerio) and mice. The information extracted were the year of publication, country, animal model and toxicity outcomes. Results: 13 articles were selected. Exposure to application concentration above the recommendation is toxic. No evidence of microcephaly was observed. We observed an increase in the number of publications after the epidemic, the country with the highest number of publications was Brazil and the zebrafish was the most used model. Final considerations: Based on the studies, pyriproxyfen is not related as a cause of microcephaly, however, it causes toxic effects. Given the wide use of this larvicide in arbovirus control programs, we recommend its use with caution.
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PadilhaR. M. O., SilvaJ. F. da, MagnaboscoA. R. dos S., GomesS. da S., CadenaM. R. S., & CadenaP. G. (2023). Does exposure to pyriproxyfen cause microcephaly? a systematic review of toxic effects in two animal models. Electronic Journal Collection Health, 23(1), e11068. https://doi.org/10.25248/reas.e11068.2023
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References
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18. MAHARAJAN K, et al. Toxicity assessment of pyriproxyfen in vertebrate model zebrafish embryos (Danio rerio): a multi-biomarker study. Aquatic. Toxicology, 2018; 196: 132–145.
19. MAHARAJAN K, et al. "Pyriproxyfen induced impairment of reproductive endocrine homeostasis and gonadal histopathology in zebrafish (Danio rerio) by altered expression of hypothalamus-pituitary-gonadal (HPG) axis genes." Science of The Total Environment, 2020; 139496.
20. MAOZ D, et al. Community effectiveness of pyriproxyfen as a dengue vector control method: a systematic review. PLoS Neglected Tropical Diseases, 2017; 11(7): 1–20.
21. MOURA JAA e SOUZA-SANTOS LP. Environmental risk assessment (ERA) of pyriproxyfen in non-target aquatic organisms. Aquatic Toxicology, 2020; 222: 1-9.
22. WORLD HEALTH ORGANIZATION (WHO). Pyriproxyfen in Drinking-water: Use for Vector Control in Drinking-water Sources and Containers. 2008. Disponível em: https://cdn.who.int/media/docs/default-source/wash-documents/wash-chemicals/pyriproxyfen-background.pdf?sfvrsn=ef4b9372_4. Acessado em: 30 de Junho de 2021.
23. PARENS R, et al. Possible link between pyriproxyfen and microcephaly. PLOS Currents, 2017; 1.
24. PADILLA S, et al. Zebrafish developmental screening of the ToxCast Phase I chemical library. Reproductive Toxicology, 2012; 33: 174-187.
25. REGALDIE AG, et al. Zebrafish Models of Autosomal Recessive Ataxias. Cells, 2021; 10(4): 836.
26. RICHARDSON JR, et al. Neurotoxicity of pesticides. Acta neuropathologica, 2019; 138(3): 343-362.
27. ROPER C e TANGUAY RL. Zebrafish as a model for developmental biology and toxicology. 2ª Edition. Oregon: Oregon State University, Handbook of developmental neurotoxicology; 2018.
28. HUSTEDT JC, et al. Use of pyriproxyfen in control of Aedes mosquitoes: A systematic review. Plos Neglected Tropical Diseases, 2020; 14(6): e0008205.
29. SARTORI AS, et al. Avaliação da toxicidade pré-natal: estudo de teratogenicidade do inseticida piriproxifeno em ratos Wistar. Arq Brasileiro de Medicina Veterinária e Zootecnia, 2020; 72(3): 719-728.
30. SHAHID A e SAHER M. Repeated exposure of pyriproxyfen to pregnant female mice causes developmental abnormalities in prenatal pups. Environmental Science and Pollution Research, 2020; 27(21): 26998-27009.
31. SCHMIDT HR, et al. Quaternary and tertiary aldoxime antidotes for organophosphate exposure in a zebrafish model system. Toxicology and Applied Pharmacology, 2015; 284(2): 197-203.
32. SPIRHANZLOVA P, et al. The pyriproxyfen metabolite 4’OH-pyriproxyfen disrupts thyroid hormone signaling and enhances Musashi-1 levels in neuro progenitor. bioRxiv, 2018; 352088.
33. TRUONG L, et al. Assessment of the developmental and neurotoxicity of the mosquito control larvicide, pyriproxyfen, using embryonic zebrafish. Environmental Pollution, 2016; 1-5.
34. VAN DER LINDEN H, et al. Epilepsy and EEG Abnormalities in Congenital Zika Syndrome. Journal of Clinical Neurophysiology, 2022; 39(4): 248-252.
35. VANI JM, et al. Pyriproxyfen does not cause microcephaly or malformations in a preclinical mammalian model. Environmental Science and Pollution Research, 2020; 28(4): 4585-4593.
36. WEEKS ENI, et al. Novel effective mosquito larvicide DL-methionine: Lack of toxicity to non-target aquatic organisms. Ecotoxicology and Environmental Safety, 2021; 213: 102013.
2. ARAÚJO TVB, et al. Association between microcephaly, Zika virus infection, and other risk factors in Brazil: final report of a case-control study. The Lancet infectious diseases, 2018; 18(3): 328-336.
3. AZEVEDO RD, et al. Effects of pyriproxyfen on zebrafish brain mitochondria and acetylcholinesterase. Chemosphere, 2020; 263: 128029.
4. BRASIL. Boletim Epidemiológico: Síndrome congênita associada à infecção pelo vírus Zika, situação epidemiológica, ações desenvolvidas e desafios de 2015 a 2019, 2019. Disponível em:http://www. https://www.gov.br/saude/pt-br/centrais-de-conteudo/publicacoes. Acessado em: 26 de junho de 2021.
5. BRASIL. Orientações técnica para utilização do larvicida pyriproxyfen (0,5 G) no controle de Aedes aegypti, 2014. Disponível em: https://www.saude.gov.br/images/pdf/.../Instrucoes-para-uso-de-pyriproxifen-maio-2014.pdf. Acessado em: 20 de março de 2021.
6. BREETA RE, et al. Non-toxic and non teratogenic extract of Thuja orientalis L. inhibited angiogenesis in zebrafish and suppressed the growth of human lung cancer cell line. Biomedicine & Pharmacotherapy, 2018; 106: 699–706.
7. CAMPOS KB, et al. Assessment of the susceptibility status of Aedes aegypti (Diptera: Culicidae) populations to pyriproxyfen and malathion in nation-wide monitoring of insecticide resistance performed in Brazil from 2017 to 2018. Parasites Vectors, 2020; 13: 531.
8. CHŁOPECKA M, et al. The effect of pyriproxyfen on the motoric activity of rat intestine-In vitro study. Environmental Pollution, 2018; 241: 1146-1152.
9. DEVILLERS J. Fate and ecotoxicological effects of pyriproxyfen in aquatic ecosystems. Environmental Science and Pollution Research, 2020; 27(14): 16052-16068.
10. DZIECIOLOWSKA S, et al. The larvicide pyriproxyfen blamed during the Zika virus outbreak does not cause microcephaly in zebrafish embryos. Scientific Reports Nature, 2017; 7: 40067.
11. CRISTOFOLI F, et al. Variantes de novo em LMNB1 causam microcefalia sindrômica pronunciada e ruptura da integridade do envelope nuclear. The American Journal of Human Genetics, 2020; 107(4): 753-762.
12. GONÇALVES ÍFS, et al. Toxicity testing of pesticides in zebrafish—a systematic review on chemicals and associated toxicological endpoints. Environmental Science and Pollution Research, 2020; 27(10): 10185-10204.
13. GUSSO D, et al. Pyriproxyfen Exposure Impairs Cognitive Parameters and Alters Cortisol Levels in Zebrafish. Frontiers in Behavioral Neuroscience, 2020; 14: 103.
14. BECERRA-SOLANO LE, et al. Microcephaly, an etiopathogenic vision. Pedi Neo, 2021; 62(4): 354-360.
15. HORIE Y, et al. Assessment of the lethal and sublethal effects of 20 environmental chemicals in zebrafish embryos and larvae by using OECD TG 212. Journal of Applied Toxicology, 2017; 37(10): 245-1253.
16. KOHNKEN R, et al. A. Overview of the use of murine models in leukemia and lymphoma research. Frontiers in oncology, 2017; 7(22).
17. LI M, et al. Cardiovascular toxicity and anxiety-like behavior induced by deltamethrin in zebrafish (Danio rerio) larvae. Chemosphere, 2019; 219: 155-164.
18. MAHARAJAN K, et al. Toxicity assessment of pyriproxyfen in vertebrate model zebrafish embryos (Danio rerio): a multi-biomarker study. Aquatic. Toxicology, 2018; 196: 132–145.
19. MAHARAJAN K, et al. "Pyriproxyfen induced impairment of reproductive endocrine homeostasis and gonadal histopathology in zebrafish (Danio rerio) by altered expression of hypothalamus-pituitary-gonadal (HPG) axis genes." Science of The Total Environment, 2020; 139496.
20. MAOZ D, et al. Community effectiveness of pyriproxyfen as a dengue vector control method: a systematic review. PLoS Neglected Tropical Diseases, 2017; 11(7): 1–20.
21. MOURA JAA e SOUZA-SANTOS LP. Environmental risk assessment (ERA) of pyriproxyfen in non-target aquatic organisms. Aquatic Toxicology, 2020; 222: 1-9.
22. WORLD HEALTH ORGANIZATION (WHO). Pyriproxyfen in Drinking-water: Use for Vector Control in Drinking-water Sources and Containers. 2008. Disponível em: https://cdn.who.int/media/docs/default-source/wash-documents/wash-chemicals/pyriproxyfen-background.pdf?sfvrsn=ef4b9372_4. Acessado em: 30 de Junho de 2021.
23. PARENS R, et al. Possible link between pyriproxyfen and microcephaly. PLOS Currents, 2017; 1.
24. PADILLA S, et al. Zebrafish developmental screening of the ToxCast Phase I chemical library. Reproductive Toxicology, 2012; 33: 174-187.
25. REGALDIE AG, et al. Zebrafish Models of Autosomal Recessive Ataxias. Cells, 2021; 10(4): 836.
26. RICHARDSON JR, et al. Neurotoxicity of pesticides. Acta neuropathologica, 2019; 138(3): 343-362.
27. ROPER C e TANGUAY RL. Zebrafish as a model for developmental biology and toxicology. 2ª Edition. Oregon: Oregon State University, Handbook of developmental neurotoxicology; 2018.
28. HUSTEDT JC, et al. Use of pyriproxyfen in control of Aedes mosquitoes: A systematic review. Plos Neglected Tropical Diseases, 2020; 14(6): e0008205.
29. SARTORI AS, et al. Avaliação da toxicidade pré-natal: estudo de teratogenicidade do inseticida piriproxifeno em ratos Wistar. Arq Brasileiro de Medicina Veterinária e Zootecnia, 2020; 72(3): 719-728.
30. SHAHID A e SAHER M. Repeated exposure of pyriproxyfen to pregnant female mice causes developmental abnormalities in prenatal pups. Environmental Science and Pollution Research, 2020; 27(21): 26998-27009.
31. SCHMIDT HR, et al. Quaternary and tertiary aldoxime antidotes for organophosphate exposure in a zebrafish model system. Toxicology and Applied Pharmacology, 2015; 284(2): 197-203.
32. SPIRHANZLOVA P, et al. The pyriproxyfen metabolite 4’OH-pyriproxyfen disrupts thyroid hormone signaling and enhances Musashi-1 levels in neuro progenitor. bioRxiv, 2018; 352088.
33. TRUONG L, et al. Assessment of the developmental and neurotoxicity of the mosquito control larvicide, pyriproxyfen, using embryonic zebrafish. Environmental Pollution, 2016; 1-5.
34. VAN DER LINDEN H, et al. Epilepsy and EEG Abnormalities in Congenital Zika Syndrome. Journal of Clinical Neurophysiology, 2022; 39(4): 248-252.
35. VANI JM, et al. Pyriproxyfen does not cause microcephaly or malformations in a preclinical mammalian model. Environmental Science and Pollution Research, 2020; 28(4): 4585-4593.
36. WEEKS ENI, et al. Novel effective mosquito larvicide DL-methionine: Lack of toxicity to non-target aquatic organisms. Ecotoxicology and Environmental Safety, 2021; 213: 102013.