Critical evaluation of current developmental toxicity testing strategies: A case of babies and their bathwater

Birth Defects Research Part B - Developmental and Reproductive Toxicology

Volumn 92, Issue 5, 2011, Pages 395-403

  Carney, Edward W ^a   Ellis, Amy L ^b   Tyl, Rochelle W ^c   Foster, Paul M D ^d   Scialli, Anthony R ^e   Thompson, Kary ^f   Kim, James ^g  

^a DOW CHEMICAL COMPANY   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c RTI INTERNATIONAL   (United States)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^e TETRA TECH INC   (United States)

^f BRISTOL MYERS SQUIBB   (United States)

^g ILSI HEALTH AND ENVIRONMENTAL SCIENCES INSTITUTE   (United States)

Author keywords

Alternatives to animal testing; Maternal toxicity; Pharmacokinetics; Safety testing

Indexed keywords

ETHYLENE GLYCOL; GLYCOLIC ACID; THALIDOMIDE;

ANIMAL TESTING ALTERNATIVE; COST; ENVIRONMENTAL EXPOSURE; HUMAN; MAMMAL; NONHUMAN; PRIORITY JOURNAL; REPRODUCTIVE TOXICITY; REVIEW; TOXICITY TESTING; TOXICOKINETICS;

ANIMALS; FEMALE; FETAL DEVELOPMENT; HUMANS; MICE; MODELS, ANIMAL; PREGNANCY; RABBITS; RATS; RISK ASSESSMENT; SAFETY; TOXICITY TESTS;

ANIMALIA;

EID: 80054695345     PISSN: 15429733     EISSN: 15429741     Source Type: Journal    
DOI: 10.1002/bdrb.20318     Document Type: Review

References (55)

1. Andersen ME, Krewski D. 2009. Toxicity testing in the 21st century: bringing the vision to life. Toxicol Sci 107:324-330.
2. Bailey J, Knight A, Balcombe J. 2005. The future of teratology research is in vitro. Biogenic Amines 19:97-145.
3. Beyer BK, Chernoff N, Danielsson BR, Davis-Bruno K, Harrouk W, Hood RD, Janer G, Wandel Liminga U, Kim JH, Rocca M, Rogers J, Scialli AR. ILSI/HESI Maternal Toxicity Workshop Summary: Maternal Toxicity and Its Impact on Study Design and Data Interpretation. Birth Defects Res. (Part B) Devel Reprod Toxicol 92:36-51.
4. Cappon GD, Fleeman TL, Chapin RE, Hurtt ME. 2005. Effects of feed restriction during organogenesis on embryo-fetal development in rabbit. Birth Defects Res B Dev Reprod Toxicol 74:424-430.
5. Carney EW. 1996. Maternal physiological disruption. In: Daston GaRK, editor. Handbook of Experimental Pharmacology: Drug Toxicity in Embryonic Development. Springer. p 573-594.
6. Carney EW, Kimmel CA. 2007. Interpretation of skeletal variations for human risk assessment: delayed ossification and wavy ribs. Birth Defects Res B Dev Reprod Toxicol 80:473-496.
7. Carney EW, Scialli AR, Watson RE, DeSesso JM. 2004. Mechanisms regulating toxicant disposition to the embryo during early pregnancy: an interspecies comparison. Birth Defects Res C Embryo Today 72:345-360.
8. Carney EW, Tornesi B, Keller C, et al. 2007. Refinement of a morphological scoring system for postimplantation rabbit conceptuses. Birth Defects Res B Dev Reprod Toxicol 80:213-222.
9. Carney EW, Tornesi B, Markham DA, et al. 2008. Species-specificity of ethylene glycol-induced developmental toxicity: toxicokinetic and whole embryo culture studies in the rabbit. Birth Defects Res B Dev Reprod Toxicol 83:573-581.
10. Chahoud I, Ligensa A, Dietzel L, Faqi AS. 1999. Correlation between maternal toxicity and embryo/fetal effects. Reprod Toxicol 13:375-381.
11. Chernoff N, Rogers JM, Kavlock RJ. 1989. An overview of maternal toxicity and prenatal development: considerations for developmental toxicity hazard assessments. Toxicology 59:111-125.
12. Clark RL, Robertson RT, Peter CP, et al. 1986. Association between adverse maternal and embryo-fetal effects in norfloxacin-treated and food-deprived rabbits. Fundam Appl Toxicol 7:272-286.
13. Collins TF, Welsh JJ, Black TN, et al. 1987. Potential reversibility of skeletal effects in rats exposed in utero to caffeine. Food Chem Toxicol 25:647-662.
14. Conolly RB, Beck BD, Goodman JI. 1999. Stimulating research to improve the scientific basis of risk assessment. Toxicol Sci 49:1-4.
15. Daston GP, Seed J. 2007. Skeletal malformations and variations in developmental toxicity studies: interpretation issues for human risk assessment. Birth Defects Res B Dev Reprod Toxicol. 80:421-424.
16. ECSCF. 2001. Guidance on Submissions for Food Additive Evaluations by the Scientific Committee on Food (dated 11 July 2001).
17. Edwards JA. 1968. The external development of the rabbit and rat embryo. Adv Teratol 3:239-263.
18. FDA. 2000. Redbook 2000 Chapter IV.C.9.a.: Guidelines for Reproduction Studies.
19. Georgiades P, Ferguson-Smith AC, Burton GJ. 2002. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23:3-19.
20. Grindon C, Combes R, Cronin MT, et al. 2006. Integrated testing strategies for use in the EU REACH system. Altern Lab Anim 34:407-427.
21. Guerri C, Bazinet A, Riley EP. 2009. Foetal alcohol spectrum disorders and alterations in brain and behaviour. Alcohol Alcohol 44:108-114.
22. Hansen JM, Harris C. 2004. A novel hypothesis for thalidomide-induced limb teratogenesis: redox misregulation of the NF-kappaB pathway. Antioxid Redox Signal 6:1-14.
23. Holsapple MP, Wallace KB. 2008. Dose response considerations in risk assessment-an overview of recent ILSI activities. Toxicol Lett 180:85-92.
24. Hood RD. 1989. A perspective on the significance of maternally mediated developmental toxicity. Regul Toxicol Pharmacol 10:144-148.
25. Hotchkiss AK, Rider CV, Blystone CR, et al. 2008. Fifteen years after "Wingspread"-environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol Sci 105:235-259.
26. ICH. 1997. S6: Preclinical Safety Evaluation of Biotechnology-Derived Pharmaceuticals (ICH Harmonised Tripartite Guideline; dated 16 July 1997).
27. ICH. 2005. S5(R2): detection of toxicity to reproduction for medicinal products & toxicity to male fertility In: ICH Harmonised Tripartite Guideline; Parent Guideline dated 24 June 1993 AdN, incorporated in November 2005, editor.
28. Khera KS. 1984. Maternal toxicity-a possible factor in fetal malformations in mice. Teratology 29:411-416.
29. Khera KS. 1985. Maternal toxicity: a possible etiological factor in embryo-fetal deaths and fetal malformations of rodent-rabbit species. Teratology 31:129-153.
30. Leazer TM, Daston GP, Keen CL, Rogers JM. 2003. The embryolethality of lipopolysaccharide in CD-1 and metallothionein I-II null mice: lack of a role for induced zinc deficiency or metallothionein induction. Toxicol Sci 73:442-447.
31. Marr MC, Price CJ, Myers CB, Morrissey RE. 1992. Developmental stages of the CD (Sprague-Dawley) rat skeleton after maternal exposure to ethylene glycol. Teratology 46:169-181.
32. Martin PL, Breslin W, Rocca M, et al. 2009. Considerations in assessing the developmental and reproductive toxicity potential of biopharmaceuticals. Birth Defects Res B Dev Reprod Toxicol 86:176-203.
33. Matsuzawa T, Nakata M, Goto I, Tsushima M. 1981. Dietary deprivation induces fetal loss and abortion in rabbits. Toxicology 22:255-259.
34. Minot CS, Taylor E. 1905. Normal Plates of the Development of the Rabbit (Lepus cuniculus). Jena: Verlag von Gustav Fishcher. 101p.
35. Narotsky MG, Best DS, Guidici DL, Cooper RL. 2001. Strain comparisons of atrazine-induced pregnancy loss in the rat. Reprod Toxicol 15:61-69.
36. Nishimura M, Iizuka M, Iwaki S, Kast A. 1982. Repairability of drug-induced "wavy ribs" in rat offspring. Arzneimittelforschung 32:1518-1522.
37. NAS. 2007. Toxicity Testing in the 21st Century: A Vision and a Strategy. Washington, DC: The National Academies Press.
38. Palmer AK. 1968. Spontaneous malformations of the New Zealand White rabbit: the background to safety evaluation tests. Lab Anim 2:195-206.
39. Petrere JA, Rohn WR, Grantham 2nd LE, Anderson JA. 1993. Food restriction during organogenesis in rabbits: effects on reproduction and the offspring. Fundam Appl Toxicol 21:517-522.
40. Pitt JA, Carney EW. 1999. Development of a morphologically-based scoring system for postimplantation New Zealand White rabbit embryos. Teratology 59:88-101.
41. Pollard I. 2007. Neuropharmacology of drugs and alcohol in mother and fetus. Semin Fetal Neonatal Med 12:106-113.
42. Price CJ, Strong PL, Marr MC, et al. 1996. Developmental toxicity NOAEL and postnatal recovery in rats fed boric acid during gestation. Fundam Appl Toxicol 32:179-193.
43. Rich KJ, Boobis AR. 1997. Expression and inducibility of P450 enzymes during liver ontogeny. Microsc Res Tech 39:424-435.
44. Rogers JM, Chernoff N, Keen CL, Daston GP. 2005. Evaluation and interpretation of maternal toxicity in Segment II studies: issues, some answers, and data needs. Toxicol Appl Pharmacol 207:367-374.
45. Rovida C, Hartung T. 2009. Re-evaluation of animal numbers and costs for in vivo tests to accomplish REACH legislation requirements for chemicals - a report by the transatlantic think tank for toxicology (t(4)). Altex 26:187-208.
46. Saghir SA, Marty MS, Clark AJ, et al. 2009. A dietary dose range-finding and toxicokinetic (TK) study of 2, 4-dichlorophenoxyacetic acid (2, 4-D) in adult CRL:CD(SD) rats and their offspring: I. Toxicokinetics. Toxicologist 114(Supplement 1):Abstract 1161.
47. Schardein JL. 2000. Chemically Induced Birth Defects. New York: Marcel Dekker. p. 40.
48. Scialli AR. 2008. The challenge of reproductive and developmental toxicology under REACH. Regul Toxicol Pharmacol 51:244-250.
49. Smith 3rd JM, Reul Jr GJ, Wukasch DC, Cooley DA. 1979. Retroesophageal subclavian arteries: surgical management of symptomatic children. Cardiovasc Dis 6:331-334.
50. Stewart J. 2009. Developmental toxicity testing of monoclonal antibodies: an enhanced pre- and postnatal study design option. Reprod Toxicol 28:220-225.
51. Taubeneck MW, Daston GP, Rogers JM, Keen CL. 1994. Altered maternal zinc metabolism following exposure to diverse developmental toxicants. Reprod Toxicol 8:25-40.
52. Van der Jagt KMS, Torslov J, de Bruijn J. 2004. Alternative approaches can reduce the use of test animals under REACH 2004. European Commission Report EUR 21405 EN.
53. Waterman AJ. 1943. Studies of normal development of the New Zealand White strain of rabbit. Am J Anat 72:473-515.
54. Wilson GN, Howe M, Stover JM. 1985. Delayed developmental sequences in rodent diabetic embryopathy. Pediatr Res 19:1337-1340.
55. Winkelmann CT, Wise LD. 2009. High-throughput micro-computed tomography imaging as a method to evaluate rat and rabbit fetal skeletal abnormalities for developmental toxicity studies. J Pharmacol Toxicol Methods 59:156-165.