Marshall J. Edwards: Discoverer of maternal hyperthermia as a human teratogen

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 73, Issue 11, 2005, Pages 857-864

  Graham Jr , John M ^a,b  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Apoptosis; Cell death; Craniofacial malformations; Eye defects; Fever; Hyperthermia; Microcephaly; Neural tube defects; Skeletal defects; Teratogen

Indexed keywords

AUSTRALIA; BLOOD VESSEL INJURY; CAREER; CATARACT; CELL DEATH; CENTRAL NERVOUS SYSTEM MALFORMATION; COLOBOMA; CONGENITAL HEART DISEASE; CONGENITAL MALFORMATION; CRANIOFACIAL DEVELOPMENT; EMBRYOTOXICITY; FEMALE; FERTILITY; FETUS; FETUS DEVELOPMENT; FINGER MALFORMATION; GUINEA PIG; HUMAN; HYPERTHERMIA; HYPODONTIA; KIDNEY MALFORMATION; KYPHOSCOLIOSIS; MATERNAL DISEASE; MEMBRANE DAMAGE; PLACENTA DISORDER; PREGNANCY; PRIORITY JOURNAL; REVIEW; TERATOGENICITY;

ABNORMALITIES, MULTIPLE; ANIMALS; FEMALE; FEVER; GUINEA PIGS; HISTORY, 20TH CENTURY; HUMANS; MATERNAL-FETAL EXCHANGE; PORTRAITS; PREGNANCY; PREGNANCY COMPLICATIONS; TERATOGENS;

ANIMALIA; CAVIA PORCELLUS;

EID: 28444476190     PISSN: 15420752     EISSN: None     Source Type: Journal    
DOI: 10.1002/bdra.20185     Document Type: Review

References (98)

1. Angles JM, Walsh DA, Li K, et al. 1990. Effects of pulsed ultrasound and temperature on the development of rat embryos in culture. Teratology 42:285-293.
2. Arora KL, Cohen BJ, Beaudoin AR. 1979. Fetal and placental responses to artificially induced hyperthermia in rats. Teratology 19:251-260.
3. Bell AW. 1987. Consequences of severe heat stress for fetal development. In: Hales JRS, Richards DAB, editors. Heat stress: physical exertion and environment. Amsterdam: Exerpta Medica, Elsevier Science, pp. 313-333.
4. Beveridge WIB. 1957. The art of scientific investigation. New York; Norton.
5. Beveridge WIB. 1980. Seeds of discovery. New York: Norton.
6. Bouwes-Bavinck JN, Weaver DD. 1986. Subclavian artery supply disruption sequence: hypothesis of a vascular etiology for Poland, Klippel Feil, and Moebius anomalies. Am J Med Genet 23:903-918.
7. Cawdell-Smith J, Upfold J, Edwards M, Smith M. 1992. Neural tube and other developmental anomalies in the guinea pig following maternal hyperthermia during early neural rube development. Teratogen Carcinogen Mutagen 12:1-9.
8. Chambers CD, Johnson KA, Felix RJ, et al. 1997. Hyperthermia in pregnancy: a prospective cohort study. Teratology 55:45.
9. Chance PI, Smith DW. 1978. Hyperthermia and meningomyelocele and anencephaly. Lancet 1:769.
10. Cockroft DL, New DAT. 1975. Effects of hyperthermia on rat embryos in culture. Nature 258:604-606.
11. Cockroft DL, New DAT. 1978. Abnormalities induced in cultured rat embryos by hyperthermia. Teratology 17:277-284.
12. Coffey VP, Jessop WJE. 1959. Maternal influenza and congenital deformities: a prospective study. Lancet 1:935-938.
13. Coffey VP, Jessop WJE. 1963. Maternal influenza and congenital deformities: a follow-up study. Lancet 1:748-751.
14. Edwards MJ. 1966. Prenatal loss of foetuses and abortion in guinea-pigs. Nature 210:223-224.
15. Edwards MJ. 1967. Congenital defects in guinea pigs following induced hyperthermia during gestation. Arch Pathol 84:42-48.
16. Edwards MJ. 1968. Congenital malformations in the rat following induced hyperthermia during gestation. Teratology 1:173-177.
17. Edwards MJ. 1969a. Congenital defects in guinea pigs: fetal resorptions, abortions and malformations following induced hyperthermia during early gestation. Teratology 2:313-328.
18. Edwards MJ. 1969b. Congenital defects in guinea pigs: retardation of brain growth of guinea pigs following hyperthermia during gestation. Teratology 2:329-336.
19. Edwards MJ. 1969c. Hyperthermia and congenital defects in guinea-pigs. Aust Vet J 45:189-193.
20. Edwards MJ. 1971a. The experimental production of arthogryposis multiplex congenita in guinea-pigs by maternal hyperthermia during gestation. J Pathol 104:221-229.
21. Edwards MJ. 1971b. The experimental production of clubfoot in guinea pigs by maternal hyperthermia during gestation. J Pathol 103:49-53.
22. Edwards MJ. 1972. Influenza, hyperthermia, and congenital malformation. Lancet 1:320-321.
23. Edwards MJ, Mulley RC, Ring S, Wanner RA. 1974. Mitotic cell death and delay of mitotic activity in guinea pig embryos following brief maternal hyperthermia. J Embryol Exp Morphol 32:593-602.
24. Edwards MJ, Wanner RA, Mulley RC. 1976. Growth and development of the brain in normal and heat-retarded guinea pigs. Neuropathol Appl Neurobiol 2:439-450.
25. Edwards MJ. 1981. Clinical disorders of fetal brain development: defects due to hyperthermia. In: Hetzel BS, Smith RM, editors. Fetal brain disorders-recent approaches to the problem of mental deficiency. Elsevier/North Holland Biomedical Press, pp. 335-364.
26. Edwards MJ, Beatson J. 1984. Effects of lead and hyperthermia on prenatal brain growth of guinea pigs. Teratology 30:413-421.
27. Edwards MJ, Gray CH, Beatson J, 1984. Retardation of brain growth of guinea pigs by hyperthermia: effect of varying intervals between successive exposures. Teratology 29:305-312.
28. Edwards MJ. 1986. Hyperthermia as a teratogen: a review of experimental studies and their clinical significance. Teratogen Carcinogen Mutagen 6:563-582.
29. Edwards M, Moeschler J, Fahy M, et al. 1990. History of gestational hyperthermia in two patients with amyoplasia. Pediatr Res 27:68A.
30. Edwards MJ, Shiota K, Smith MSR, Walsh DA. 1995. Hyperthermia and birth defects. Reprod Toxicol 9:411-425.
31. Edwards MJ, Walsh DA, Li Z. 1997. Hyperthermia, teratogenesis and the heat shock response in mammalian embryos in cultures. Int J Dev Biol 41:345-358.
32. Edwards MJ, Saunders RD, Shiota K. 2003a. Effects of heat on embryos and fetuses. Int J Hypertherm 19:295-324.
33. Edwards MJ, Smith MSR, Freeman B. 2003b. Measurement of the linear dynamics of the descent of the bovine testis. J Anat 203:133-142.
34. Erickson JD. 1991. Risk factors for birth defects: data from the Atlanta birth defects case-control study. Teratology 43:41-51.
35. Ferm VH, Perm RR. 1979. Teratogenic interaction of hyperthermia and vitamin A. Biol Neonate 36:168-172.
36. Ferm VH, Kilham L. 1977. Synergistic teratogenic effects of arsenic and hyperthermia in hamsters. Environ Res 14:483-486.
37. Finnell RH, Moon SP, Abbott LC, et al. 1986. Strain differenced in heat-induced neural tube defects in mice. Teratology 33:247-252.
38. Firth HV, Boyd P, Chamberlain PF, MacKenzie IZ. 1994. Analysis of limb reduction defects in babies exposed to chorionic villus sampling. Lancet 342:1069-1071.
39. Fisher NL, Smith DW. 1981. Occipital encephalocele and early gestational hyperthermia. Pediatrics 68:480-483.
40. Fraser FC, Skelton J. 1978. Possible teratogenicity of maternal fever. Lancet 2:634.
41. Fujita I, Koyanagi T, Kukita J, et al. 1991. Moebius syndrome with central hypoventilation and brainstem calcification: a case report. Eur J Pediatr 150:582-583.
42. Germain MA, Webster WS, Edwards MJ. 1985. Hyperthermia as a teratogen: parameters determining hyperthermia-induced head defects in the rat. Teratology 31:265-272.
43. Gonzalez CH, Vargas RR, Perez AB, et al. 1993. Limb deficiency with or without Moebius sequence in seven Brazilian children associated with misoprostal use in the first trimester of pregnancy. Am J Med Genet 47:59-64.
44. Govaert P, Van Faesebrouck P, DePraeter C, et al. 1989. Moebius sequence and prenatal brainstem ischemia. Pediatrics 84:570-573.
45. Graf WD, Shepard TH. 1997. Uterine contraction in the development of Moebius syndrome. J Child Neurol 12:225-227.
46. Graham JM Jr, Perm VH. 1985. Heat and alcohol induced neural tube defects: interactions with folate in a golden hamster model. Pediatr Res 19:247-251.
47. Graham JM Jr, Matthew J, Edwards AH, et al. 1988. Gestational hyperthermia as a cause for Moebius syndrome. Teratology 37:461A.
48. Graham JM, Edwards MJ. 1989. Teratogenic effects of maternal hyperthermia. Ann Res Inst Environ Med Nagoya 40:365-374.
49. Graham JM Jr, Edwards MJ, Edwards MJ. 1998. Teratogen update: gestational effects of maternal hyperthermia due to febrile illnesses and resultant patterns of defects in humans. Teratology 58:209-221.
50. Halperin LR, Wilroy RS. 1978. Maternal hyperthermia and neural tube defects. Lancet 2:212.
51. Harbord MG, Finn JP, Halls-Craggs MA, et al. 1989. Moebius syndrome with unilateral cerebellar hypoplasia. J Med Genet 26:579-582.
52. Harding AJ, Edwards MJ. 1993. Micrencephaly in rats caused by maternal hyperthermia on days 13 and 14 of pregnancy. Cong Anom 33:203-209.
53. Hendrickx AG, Stone GW, Hendrickson RV, Matayoshi K. 1979. Teratogenic effects of hyperthermia in the bonnet monkey (Macaca radiata). Teratology 19:177-182.
54. Hightower LE. 1991. Heat shock, stress proteins, chaperons and proteotoxicity. Cell 66:1-20.
55. Hilbelink DR, Chen LT, Bryant M. 1986. Endotoxin-induced hyperthermia in pregnant golden hamsters. Teratogen Carcinogen Mutagen 6:209-217.
56. Hunter AGW. 1984. Neural tube defects in eastern Ontario and western Quebec: demography and family data. Am J Med Genet 19:45-63.
57. Ivarsson SA, Henriksson P. 1984. Septic shock and hyperthermia as possible teratogenic factors. Acta Paediatri Scand 73:875-876.
58. Johnson HA, Pavelec M. 1972. Thermal injury due to normal body temperature. Am J Pathol 66:557-564.
59. Kline J, Stein Z, Susser M, Warburton D. 1985. Fever during pregnancy and spontaneous abortion. Am J Epidemiol 121:832-842.
60. Kumar D. 1990. Moebius syndrome. J Med Genet 27:122-126.
61. Layde PM, Edmonds LD, Erickson JD. 1980. Maternal fever and neural tube defects. Teratology 21:105-108.
62. Lindquist S. 1986. The heat shock response. Ann Rev Biochem 55:1151-1191.
63. Lipson A. 1988. Hirschsprung disease in the offspring of mothers exposed to hyperthermia during pregnancy. Am J Med Genet 29:117-124.
64. Lipson AH, Webster WS, Woodman-Brown PDC, Osborn RA. 1989. Moebius syndrome: animal model human correlations and evidence for a brainstem vascular etiology. Teratology 40:339-350.
65. Little BB, Ghali FE, Snell LM, et al. 1991. Is hyperthermia teratogenic in humans? Am J Perinatal 8:185-189.
66. McDonald AD. 1958. Maternal health and congenital defect. N Engl J Med 258:767-773.
67. McDonald AD. 1961. Maternal health in early pregnancy and congenital defect. Final report on a prospective inquiry. Br J Prev Soc Med 15: 154-166.
68. Miller P, Smith DW, Shepard T. 1978. Maternal hyperthermia as a possible cause of anencephaly. Lancet 1:519.
69. Milunsky A, Ulcickas M, Rothman KJ, et al. 1992. Maternal heat exposure and neural tube defects. JAMA 268:882-885.
70. Mirkes PE. 1985. Effects of acute exposure to elevated temperatures on rat embryo growth and development in vitro. Teratology 32:259-266.
71. Mirkes PE. 1987. Hyperthermia-induced heat shock response and thermotolerance in postimplantation rat embryos. Dev Biol 119:115-122.
72. Mirkes PE, Doggett B. 1992. Accumulation of heat shock protein 72 (hsp72) in postimplantation rat embryos after exposure to various periods of hyperthermia (40°43°C) in vitro: evidence that heat shock protein 72 is a biomarker of heat-induced embryotoxicity. Teratology 46:301-309.
73. Mirkes PE, Cornel LM, Park HW, Cunningham ML. 1997. Induction of thermotolerance in early postimplantation rat embryos is associated with increased resistance to hyperthermia-induced apoptosis. Teratology 56:210-219.
74. Mirsky AE, Pauling L. 1936. On the structure of native, denatured, and coagulated proteins. Proc Natl Acad Sci USA 22:439-447.
75. Nilson NO. 1985. Vascular abnormalities due to hyperthermia in chick embryos. Teratology 30:237-251.
76. Fleet H, Graham JM Jr, Smith DW. 1981. Central nervous system and facial defects associated with maternal hyperthermia at four to 14 weeks' gestation. Pediatrics 67:785-789.
77. Saxen L, Holmberg PC, Nurminen M, Kuosma E. 1982. Sauna and congenital defects. Teratology 25:309-313.
78. Schlesinger MJ. 1990. Heat shock proteins. J Biol Chem 265:12111-12114.
79. Shiota K. 1982. Neural tube defects and maternal hyperthermia in early pregnancy: epidemiology in a human embryo population. Am J Med Genet 12:281-288.
80. Shiota K. 1988. Induction of neural tube defects and skeletal malformations in mice following brief hyperthermia in utero. Biol Neonate 53:86-97.
81. Shiota K, Shionoya Y, Ide M, et al. 1988. Teratogenic interaction of ethanol and hyperthermia in mice. Proc Soc Exp Biol Med 187:142-148.
82. Spragget K, Fraser FC. 1982b. Sauna-induced hyperthermia in women. Teratology 25:77A.
83. St. Charles S, DiMario FJ Jr, Grunnet ML. 1993. Möbius sequence: further in vivo support for the subclavian artery supply disruption sequence. Am J Med Genet 47:289-293.
84. Superneau DW, Wertelecki W. 1985. Brief clinical report: similarity of effects-experimental hyperthermia as a teratogen and maternal febrile illness associated with oromandibular and limb defects. Am J Med Genet 21:575-580.
85. Tiboni GM, Iammarrone E, Piccirillo G, et al. 1997. Aspirin pre-treatment potentiates hyperthermia-induced teratogenesis in the mouse. Am J Obstet Gynecol. 178:270-279.
86. Tikkanen J, Heinonen OP. 1991. Maternal hyperthermia during pregnancy and cardiovascular malformations in the offspring. Eur J Epidemiol 7:628-635.
87. Umpierre CC, Dukelow WR. 1977. Environmental heat stress effects in the hamster. Teratology 16:155-158.
88. Upfold JB, Smith MSR, Edwards MJ. 1989. Quantitative study of the effects of maternal hyperthermia on cell death and proliferation in the guinea pig brain on day 21 of pregnancy. Teratology 39:173-179.
89. Walsh DA, Hightower LE, Klein NW, Edwards MJ. 1985. The induction of the heat shock proteins during early mammalian development. Heat shock [abstract]. Cold Spring Harbor Lab Symp 2:92.
90. Walsh DA, Klein NW, Hightower LE, Edwards MJ. 1987. Heat shock and thermotolerance during early rat embryo development. Teratology 36:181-191.
91. Walsh DA, Li K, Speirs J, Crowther CE, Edwards MJ. 1989. Regulation of the inducible heat shock 71 genes in early neural development of cultured rat embryos. Teratology 40:312-334.
92. Walsh DA, Li K, Wass J, et al. 1993. Heat-shock gene expression and cell cycle changes during mammalian embryonic development. Dev Genet 14:127-136.
93. Walsh DA, Zhe L, Zeng F, et al. 1994. Heat shock genes and cell cycle regulation during early mammalian development. Environ Med 38: 1-6.
94. Walsh DA, Edwards MJ, Smith MSR. 1997. Heat shock proteins and their role in early mammalian development. Exp MoI Med 29:129-132.
95. Wanner RA, Edwards MJ, Wright RG. 1975. The effect of hyperthermia on the neuroepithelium of the 21-day guinea pig foetus: histologic and ultrastructural study. J Pathol 118:235-244.
96. Webster WS, Edwards MJ. 1984. Hyperthermia and the induction of neural tube defects in mice. Teratology 29:417-425.
97. Webster WS, Lipson AH, Brown-Woodman PDC. 1987. Uterine trauma and limb defects. Teratology 35:253-260.
98. Webster WS, Lipson AS, Brown-Woodman PDC, Osbom RA. 1988. Moebius unmasked: pathogenesis of the Moebius syndrome in an animal model. Teratology 38:199.