Neuropathology Evaluation in Juvenile Toxicity Studies in Rodents: Comparison of Developmental Neurotoxicity Studies for Chemicals With Juvenile Animal Studies for Pediatric Pharmaceuticals

1. Rodier, PM . Developmental neurotoxicology. Toxical Pathol. 1990;18(1 Pt. 2):89–95.
Google Scholar | SAGE Journals | ISI2. Rice, D, Barone, SJ. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000;108(suppl 3):511–533.
Google Scholar | Crossref | Medline | ISI3. Bal-Price, AK, Coecke, S, Costa, L, et al. Advancing the science of developmental neurotoxicity (DNT): testing for better safety evaluation. ALTEX. 2012;29(2):202–215.
Google Scholar | Crossref | Medline4. Sidhu, RS, Del Bigio, MR, Tuor, UI, Seshia, SS. Low-dose vigabatrin (γ-vinyl GABA)-induced damage in the immature rat brain. Exp Neurol. 1997;144(2):400–405.
Google Scholar | Crossref | Medline5. van der Laan, JW, van Malderen, K, de Jager, N, et al. Evaluation of juvenile animal studies for pediatric CNS-targeted compounds: a regulatory perspective. Int J Toxicol. 2019;38(6):456–475.
Google Scholar | SAGE Journals | ISI6. EPA (U.S. Environmental Protection Agency) . Health effects test guidelines: OPPTS 870.6300: developmental neurotoxicity study. Published 1998. Accessed September 5, 2021. https://www.epa.gov/test-guidelines-pesticides-and-toxic-substances/series-870-health-effects-test-guidelines [Listed under “GroupE−NeurotoxicityTestGuidelines”].
Google Scholar7. OECD (Organisation for Economic Co-operation and Development) . Test No. 426: Developmental neurotoxicity study. Published 2007. Accessed September 5, 2021. http://www.oecd-ilibrary.org/environment/test-no-426-developmental-neurotoxicity-study_9789264067394-en
Google Scholar8. FDA (US Food and Drug Administration) . Redbook 2000. Published 2000. Accessed September 5, 2021. [https://www.fda.gov/regulatory-information/search-fda-guidance-documents/guidance-industry-and-other-stakeholders-redbook-2000#TOC
Google Scholar9. ICH (International Council for Harmonisation of Technical Requirements for Pharmaceuticals for Human Use) . S11: nonclinical safety testing in support of development of paediatric medicines. Published 2020. Accessed September 5, 2021. https://database.ich.org/sites/default/files/S11_Step4_FinalGuideline_2020_0310.pdf
Google Scholar10. FDA (US Food and Drug Administration) . S11: nonclinical safety testing in support of development of pediatric medicines. Published 2021. Accessed September 5, 2021. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/s11-nonclinical-safety-testing-support-development-pediatric-pharmaceuticals
Google Scholar11. Parker, GA, Picut, CA. Developmental assessments of the nervous system. In: Hoberman, AM, Lewis, EM, eds. Pediatric Non-clinical Drug Testing: Principles, Requirements, and Practices. 2nd ed. John Wiley & Sons; 2022:(in press).
Google Scholar12. Clancy, B, Finlay, BL, Darlington, RB, Anand, KJ. Extrapolating brain development from experimental species to humans. Neurotoxicology. 2007;28(5):931–937.
Google Scholar | Crossref | Medline13. Clancy, B, Charvet, CJ, Darlington, RB, Finlay, BL, Workman, A. Translating time (across developing mammalian brains). Published 2013. Accessed September 5, 2021. http://translatingtime.net/
Google Scholar14. Rodier, PM . Vulnerable periods and processes during central nervous system development. Environ Health Perspec. 1994;102(suppl 2):121–124.
Google Scholar | Crossref | Medline | ISI15. Rodier, PM . Chronology of neuron development: animal studies and their clinical implications. Dev Med Child Neurol. 1980;22(4):525–545.
Google Scholar | Crossref | Medline16. Semple, BD, Blomgren, K, Gimlin, K, Ferriero, DM, Noble-Haeusslein, LJ. Brain development in rodents and humans: identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol. 2013;106-107:1–16.
Google Scholar | Crossref | Medline | ISI17. Wiggins, RC . Myelination: a critical stage in development. Neurotoxicology. 1982;7(2):103–120.
Google Scholar18. Kaufmann, W . Pathology methods in nonclinical neurotoxicity studies: the developing central nervous system. In: Bolon, B, Butt, MT, eds. Fundamental Neuropathology for Pathologists and Toxicologists: Principles and Techniques. John Wiley & Sons; 2011:339–363.
Google Scholar | Crossref19. Downes, N, Mullins, P. The development of myelin in the brain of the juvenile rat. Toxicol Pathol. 2014;42(5):913–922.
Google Scholar | SAGE Journals | ISI20. Belay, ED, Bresee, JS, Holman, RC, Khan, AS, Shahriari, A, Schonberger, LB. Reye’s syndrome in the United States from 1981 through 1997. N Engl J Med. 1999;340(18):1377–1382.
Google Scholar | Crossref | Medline21. NC3Rs (National Centre for the Replacement, Refinement, & Reduction of Animals in Research) . The macaque website. Accessed September 5, 2021. https://www.nc3rs.org.uk/macaques/macaques/life-history-and-diet/
Google Scholar22. Hill, MA . Embryology: dog development. Published 2020. Accessed September 5, 2021. https://embryology.med.unsw.edu.au/embryology/index.php/Dog_Development
Google Scholar23. Hill, MA . Embryology: pig development. Published 2020. Accessed September 5, 2021. https://embryology.med.unsw.edu.au/embryology/index.php/Pig_Development
Google Scholar24. Kim, NN, Parker, RM, Weinbauer, GF, Remick, AK, Steinbach, T. Points to consider in designing and conducting juvenile toxicology studies. Int J Toxicol. 2017;36(4):325–339.
Google Scholar | SAGE Journals | ISI25. DeSesso, JM . Comparative features of vertebrate embryology. In: Hood, RD , ed. Developmental and Reproductive Toxicology: A Practical Approach. 2nd ed. CRC Press; 2006:147–197.
Google Scholar26. Sengupta, P . The laboratory rat: relating its age with human’s. Int J Prev Med. 2013;4(6):624–630.
Google Scholar | Medline27. Workman, AD, Charvet, CJ, Clancy, B, Darlington, RB, Finlay, BL. Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci. 2013;33(17):7368–7383.
Google Scholar | Crossref | Medline28. Simmons, HA . Age-associated pathology in rhesus macaques (Macaca mulatta). Vet Pathol. 2016;53(2):399–416.
Google Scholar | SAGE Journals | ISI29. FDA (U.S. Food and Drug Administration) . Guidance for industry: E11 clinical investigation of medicinal products in the pediatric population. Published 2000. Accessed September 5, 2021. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/e11-clinical-investigation-medicinal-products-pediatric-population
Google Scholar30. Fawcett, LB, Brent, RL. Pathogenesis of abnormal development. In: Hood, RD , ed. Developmental and Reproductive Toxicology: A Practical Approach. 2nd ed. CRC Press (Taylor & Francis); 2006:61–92.
Google Scholar31. Fisher, JE, Ravindran, A, Elayan, I. CDER experience with juvenile animal studies for CNS drugs. Int J Toxicol. 2019;38(2):88–95.
Google Scholar | SAGE Journals | ISI32. O’Leary-Moore, SK, Parnell, SE, Lipinski, RJ, Sulik, KK. Magnetic resonance-based imaging in animal models of fetal alcohol spectrum disorder. Neuropsychol Rev. 2011;21(2):167–185.
Google Scholar | Crossref | Medline33. Costa, LG, Guizzetti, M, Burry, M, Oberdoerster, J. Developmental neurotoxicity: do similar phenotypes indicate a common mode of action? A comparison of fetal alcohol syndrome, toluene embryopathy and maternal phenylketonuria. Toxicol Lett. 2002;127(1-3):197–205.
Google Scholar | Crossref | Medline34. Mellon, RD, Simone, AF, Rappaport, BA. Use of anesthetic agents in neonates and young children. Anesth Analg. 2007;104(3):509–520.
Google Scholar | Crossref | Medline35. Nau, H, Hauck, RS, Ehlers, K. Valproic acid-induced neural tube defects in mouse and human: aspects of chirality, alternative drug development, pharmacokinetics and possible mechanisms. Pharmacol Toxicol. 1991;69(5):310–321.
Google Scholar | Crossref | Medline36. Vorhees, CV . Developmental neurotoxicity induced by therapeutic and illicit drugs. Environ Health Perspect. 1994;102(suppl 2):145–153.
Google Scholar | Crossref | Medline37. Rasmussen, AD, Richmond, E, Wegener, KM, Downes, N, Mullins, P. Vigabatrin-induced CNS changes in juvenile rats: induction, progression and recovery of myelin-related changes. Neurotoxicology. 2015;46:137–144.
Google Scholar | Crossref | Medline | ISI38. Arnon, J, Meirow, D, Lewis-Roness, H, Ornoy, A. Genetic and teratogenic effects of cancer treatments on gametes and embryos. Hum Reprod Update. 2001;7(4):394–403.
Google Scholar | Crossref | Medline39. Blommaert, J, Radwan, A, Sleurs, C, et al. The impact of cancer and chemotherapy during pregnancy on child neurodevelopment: a multimodal neuroimaging analysis. EClinicalMedicine. 2020;28:100598.
Google Scholar | Crossref | Medline40. Noguchi, KK, Johnson, SA, Manzella, FM, et al. Caffeine augments anesthesia neurotoxicity in the fetal macaque brain. Sci Rep. 2018;8(1):5302.
Google Scholar | Crossref | Medline41. Costa, LG, Aschner, M, Vitalone, A, Syversen, T, Soldin, OP. Developmental neuropathology of environmental agents. Annu Rev Pharmacol Toxicol. 2004;44:87–110.
Google Scholar | Crossref | Medline | ISI42. Grandjean, P, Landrigan, PJ. Developmental neurotoxicity of industrial chemicals. Lancet. 2006;368(9553):2167–2178.
Google Scholar | Crossref | Medline | ISI43. Giordano, G, Costa, LG. Developmental neurotoxicity: some old and new issues. ISRN Toxicol. 2012;2012:814795.
Google Scholar | Crossref | Medline44. de Groot, DM, Hartgring, S, van de Horst, L, et al. 2D and 3D assessment of neuropathology in rat brain after prenatal exposure to methylazoxymethanol, a model for developmental neurotoxicty. Reprod Toxicol. 2005;20(3):417–432.
Google Scholar | Crossref | Medline | ISI45. Sadiq, S, Ghazala, Z, Chowdhury, A, Busselberg, D. Metal toxicity at the synapse: presynaptic, postsynaptic, and long-term effects. J Toxicol. 2012;2012:132671.
Google Scholar | Crossref | Medline46. Vorhees, CV, Ahrens, KG, Acuff-Smith, KD, Schilling, MA, Fisher, JE. Methamphetamine exposure during early postnatal development in rats: I. Acoustic startle augmentation and spatial learning deficits. Psychopharmacology. 1994;114(3):392–401.
Google Scholar | Crossref | Medline47. Vorhees, CV, Ahrens, KG, Acuff-Smith, KD, Schilling, MA, Fisher, JE. Methamphetamine exposure during early postnatal development in rats: II. Hypoactivity and altered responses to pharmacological challenge. Psychopharmacology. 1994;114(3):402–408.
Google Scholar | Crossref | Medline48. Garman, RH, Li, AA, Kaufmann, W, Auer, RN, Bolon, B. Recommended methods for brain processing and quantitative analysis in rodent developmental neurotoxicity studies. Toxicol Pathol. 2016;44(1):14–42.
Google Scholar | SAGE Journals | ISI49. Bolon, B, Garman, R, Jensen, K, Krinke, G, Stuart, B. A best practices approach to neuropathologic assessment in developmental neurotoxicity testing—for today. Toxicol Pathol. 2006;34(3):296–313.
Google Scholar | SAGE Journals | ISI50. OECD (Organisation for Economic Co-operation and Development) . Test No. 443: extended one-generation reproductive toxicity study. Published 2018. Accessed September 5, 2021. http://www.oecd-ilibrary.org/environment/test-no-443-extended-one-generation-reproductive-toxicity-study_9789264185371-en
Google Scholar51. Li, AA, Sheets, LP, Raffaele, K, et al. Recommendations for harmonization of data collection and analysis of developmental neurotoxicity endpoints in regulatory guideline studies: proceedings of workshops presented at Society of Toxicology and joint Teratology Society and Neurobehavioral Teratology Society meetings. Neurotoxicol Teratol. 2017;63:24–45.
Google Scholar | Crossref | Medline52. Li, AA, Garman, RH, Sheets, LP. Regulatory testing for developmental neurotoxicology. In: McQueen, CA , ed. Comprehensive Toxicology. Vol 9. 3rd ed. Elsevier Ltd; 2018:183–215.
Google Scholar | Crossref53. Crofton, KM, Makris, SL, Sette, WF, Mendez, E, Raffaele, KC. A qualitative retrospective analysis of positive control data in developmental neurotoxicity studies. Neurotoxicol Teratol. 2004;26(3):345–352.
Google Scholar | Crossref |

Comments (0)

No login
gif