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International Journal of Hyperthermia Volume 19, 2003 - Issue 3: Adverse temperature levels in the human-proceedings of the WHO conference
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Research Article

Effects of heat on embryos and foetuses

M. J. Edwards The University of Sydney, NSW 2006, Australia
,
R. D. Saunders National Radiation Protection Board, Chilton, Didcot, Oxfordshire OX11 0RQ, UK
&
K. Shiota Congenital Anomaly Research Center, Department of Anatomy & Developmental Biology, Kyoto University Graduate School of Medicine. Kyoto 606-8501, Japan
Pages 295-324 | Published online: 09 Jul 2009

  • UNSCEAR. Biological effects of pre-natal irradiation. Annex C. In: United Nations Scientific Committee on the Effects of Atomic Radiation, Genetic and Somatic Effects of Ionising Radiation. UNSCEAR Report to the General Assembly with Scientific Annexes, New York: United Nations, 1986; 263-366.
  • Germain MA, Webster WS, Edwards MJ. Hypothermia as a teratogen: parameters determining hyperthermia-induced defects in the rat. Teratology 1985; 31: 265-72.
  • Edwards MJ, Shiota K, Smith MSR, Walsh DA. Hyperthermia and birth defects. Reprod Toxicol 1995; 9: 411-25.
  • Wanner RA, Edwards MJ. Comparison of the effects of radiation and hyperthermia on prenatal retardation of brain growth of guinea-pigs. Brit J Radial 1983; 56: 33-9.
  • Edwards MJ, Mulley R, Ring S, Wanner RA. Mitotic cell death and delay of mitotic activity in guinea-pig embryos following brief maternal hyperthermia. J Embryol Exp Morphol 1974; 32: 593-602.
  • Wanner RA, Edwards MJ, Wright RG. The effect of hyperthermia on the neuroepithelium of the 21-day guinea-pig foetus: histologie and ultrastructural study. J Path 1976; 118:235-44.
  • Upfold J, Smith MSR, Edwards MJ. Quantitative study of the effects of maternal hyperthermia on cell death and proliferation in the guinea pig brain on day 21 of pregnancy. Teratology 1989; 39: 173-9.
  • Walsh D, Li K, Wass J, Dolnikov A, Zeng F, Edwards M Heat-shock gene expression and cell cycle changes during mammalian embryonic development. Devel Genet 1993; 14: 12736.
  • Edwards MJ, Walsh DA, Li Z. Hyperthermia, teratogenesis and the heat shock response in mammalian embryos in culture. Int J Dev Biol 1997; 41: 345-58.
  • Li ZL, Shiota K. Stage-specific homeotic vertebral transformations in mouse fetuses induced by maternal hyperthermia during somitogenesis. Devel Dynamics 1999; 216: 336-48.
  • Breen JG, Claggett TW, Kimmel GL, Kimmel CA. Heat shock during rat embryo development in vitro results in decreased mitosis and abundant cell death. Reprod Toxicol 1999; 13: 31-9.
  • Hicks SP, D'Amato CP. Effects of ionizing radiation on mammalian development. In: Woollam DHM, ed., Advances in Teratology, London: Logos Press, 1966; 196-243.
  • Smith MSR, Upfold JB, Edwards MJ, Shiota K, Cawdell-Smith J. The induction of neural tube defects by maternal hyperthermia; a comparison of the guinea-pig and human. Neuropathol Appl Neurobiol 1992; 18: 71-80.
  • Edwards MJ. The experimental production of arthrogryposis multiplex congenita in guinea pigs by maternal hyperthermia during gestation. / Path 1971; 104: 221-9.
  • Lepock JR. Involvement of membranes in cellular responses to hyperthermia. Radiat Res 1982; 92: 433-8.
  • Coss RA, Dewey WC, Hamburg JR. Effects of hyperthermia on dividing Chinese hamster ovary cells and microtubules in vitro. Cancer Res 1982; 42: 1059-71.
  • van Bergenen Henegouwen PM, Jordi WJ, van Dongen Ramaekers CS, Amesz H, Linneman WAM. Studies on a possible relationship between alterations in the cytoskeleton and induction of heat shock protein synthesis in mammalian cells. Int J Hyperthermia 1985; 1: 59-83.
  • Lipson A. Hirschsprung disease in the offspring of mothers exposed to hyperthermia during pregnancy. Am J Med Genet 1988; 29: 117-24.
  • Hinoue A, Fushiki S, Nishimura Y, Shiota K. In utero exposure to brief hyperthermia interferes with the production and migration of neocortical neurons and induces apoptotic cell death in the fetal mouse brain. Dev Brain Res 2001; 132: 59-67.
  • Kinder BF. Prenatal irradiation: a major concern for the developing brain. Int J Radiat Biol 1998; 73: 423-34.
  • Otake M, Schull WJ. Review: radiation-related brain damage and growth retardation among the prenatally exposed bomb survivors. Int J Radial Biol 1998; 74: 159-71.
  • Nilsen NO. Vascular abnormalities due to hyperthermia in chick embryos. Teratology 1985; 30: 237-51.
  • Arora KL, Cohen BJ, Beaudoin AR. Fetal and placenta! responses to artificially induced hyperthermia in rats. Teratology 1979; 19: 251-60.
  • Hendrickx AG, Stone GW, Henrickson RV, Matayoshi K. Teratogenic effects of hyperthermia in the bonnet monkey (macaca radiata). Teratology 1979; 19: 177-82.
  • Morishima HO, Glaser B, Biermann WH, James LS. Increased uterine activity and fetal deterioration during maternal hyperthermia. Am J Obstet Gynecol 1975; 121: 531-8.
  • Kline J, Stein Z, Susser M, Warburton D. Fever during pregnancy and spontaneous abortion. Am J Epidemiol 1985; 121: 832-42.
  • Schröder HJ, Power GG. Engine and radiator: fetal and placenta! interactions for heat dissipation. Exp Physiol 1997; 82: 403-14.
  • Power GG. Biology of temperature: the mammalian fetus. J Devel Physiol 1989; 12: 295304.
  • Erkkola RU, Pirhonen JP, Kivijarvi AK. Flow velocity waveforms in uterine and umbi- lical arteries during submaximal bicycle exercise in normal pregnancy. Obstet Gynaecol 1992; 79: 611-5.
  • Pirhonen JP, Vähä-Eskeli KK, Seppänen A, Vuorinen J, Erkkola RU. Does thermal stress decrease uterine blood flow in hypertensive pregnancies. Am J Perinatology 1994; 11: 3136.
  • Labum HP, Mitchell D, Goelst K. Fetal and maternal body temperatures measured by radiotelemetry in near-term sheep during thermal stress. J Appl Physiol 1992; 72:894-900.
  • Bell AW. Consequences of severe heat stress for fetal development. In: Hales JRS, Richards DAB, Heat Stress, Physical Exertion and Environment, New York: Excerpta Medica, 1987; 313-33.
  • McMurray RG, Katz VL. Thermoregulation in pregnancy: implications for exercise. Sports Med 1990; 10: 146-58.
  • Walsh D, Zhe L, Zeng F, Van W, Edwards M. Heat shock genes and cell cycle regulation in early mammalian development. Environ Med 1994; 38: 1-6.
  • Heikkila JJ, Miller JG, Schultz GA, Kloc M, Browder LW. Heat shock gene expression during early animal development. In: Atkinson BG, Waiden DB, eds, Changes in Eukaryote Gene Expression in Response to Environmental Stress, Orlando: Academic Press, 1985; 135-8.
  • Morange M, Diu A, Bensaude O, Babinet C. Altered expression of heat shock proteins in embryonal carcinoma cells and mouse early embryonic cells. MoI Cell Biol 1984; 4: 730-5.
  • Walsh DA, Klein NW, Hightower LE, Edwards MJ. Heat shock and thermotolerance during early rat embryo development. Teratology 1987; 36: 181-91.
  • Walsh DA, Li K, Speirs J, Crowther CE, Edwards MJ. Regulation of the inducible heat shock 71 genes in early neural development of cultured rat embryos. Teratology 1989; 40: 321-34.
  • Mirkes PE. Effects of acute exposure to elevated temperatures on rat embryo growth and development in vitro. Teratology 1985; 32: 259-66.
  • Mirkes PE. Hyperthermia-induced heat shock response and thermotolerance in postim- plantation rat embryos. Devel Biol 1987; 119: 115-22.
  • Mirkes PE, Cornel L. A comparison of sodium arsenite and hyperthermia-induced stress responses and abnormal development in cultured postimplantation rat embryos. Teratology 1992; 46: 251-9.
  • Mirkes PE, Doggett B 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 1992; 46: 301-9.
  • Mirkes PE, Cornel LM, Park HW, Cunningham LM. Induction of thermotolerance in early postimplantation rat embryos is associated with increased resistance to hyperthermia-induced apoptosis. Teratology 1997; 56: 210-9.
  • UNSCEAR. Radiation effects on the developing human brain. Annex H. In: United Nations Scientific Committee on the Effects of Atomic Radiation, Sources and Effects of Ionising Radiation. UNSCEAR Report to the General Assembly with Scientific Annexes, New York: United Nations, 1993; 805-67.
  • Konermann G. Postnatal brain maturation damage induced by prenatal irradiation: modes of manifestation and dose-response relations. In: Baverstock KF, Stather JW, eds, Low Dose Radiation: Biological Bases of Risk Assessment, London: Taylor & Francis, 1989; 364-76.
  • Sienkiewicz ZJ, Haylock RG, Saunders RD. Differential learning impairments produced by prenatal exposure to ionising radiation in mice. Int J Radiat Biol 1999: 75: 121-7.
  • Sienkiewicz ZJ, Saunders RD, Rutland BK. Prenatal irradiation and spatial memory in mice: investigation of critical period. Int J Radiat Biol 1992; 62: 211-9.
  • Sienkiewicz ZJ, Haylock RGE, Saunders RD. Prenatal irradiation and spatial memory in mice: investigation of dose-response relationship. Int J Radiat Biol 1994; 65: 611-8.
  • Finnell RH, Moon SP, Abbott LC, Golden JA, Chernoff GF. Strain differences in heat- induced neural tube defects in mice. Teratology 1986; 33: 247-52.
  • Webster WS, Edwards MJ. Hyperthermia and the induction of neural tube defects in mice. Teratology 1984; 29: 417-25.
  • Kimmel CA, Cuff JM, Kimmel GL, Heredia DJ, Tudor N, Silverman PM, Chen J. Skeletal development following heat exposure in the rat. Teratology 1993; 47: 229-42.
  • Vacha SJ, Bennett CD, Mackler SA, Koebbe MJ, Finnell RH. Identification of a growth arrest specific (gas 5) gene by differential display as a candidate gene for determining susceptibility to hyperthermia-induced exencephaly in mice. Dev Genet 1997; 21: 212-22.
  • Miller MW, Nyborg WL, Dewey WC, Edwards MJ, Abramowicz JS, Brayman AA. Hyperthermic teratogenicity, thermal dose and diagnostic ultrasound during pregnancy: implications of new standards on tissue heating. Int J Hyperthermia, 2002; 18: 361-84.
  • Dewhirst MW, Vigilanti BL, Lora-Michiels M, Hanson M, Hoopes PJ. Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia. Int J Hyperthermia, 2003; 19: 267-294.
  • Lary JM, Conover DL, Foley ED, Hansen PL. Teratogenic effects of 27.12MHz radio- frequency radiation in rats. Teratology 1982; 26: 299-309.
  • Lary JM, Conover DL, Johnson PG, Burg JR. Teratogenicity of 27.12MHz radiation in rats is related to duration of hyperthermic exposure. Bioelectromagnetics 1983; 4: 24955.
  • Lary JM, Conover DL, Johnson PG, Hornung RW. Dose-response relationship between body temperature and birth defects in radiofrequency-irradiated rats. Bioelectromagnetics 1986; 7: 141-9.
  • Brown-Woodman PDC, Hadley JA, Waterhouse J, Webster WS. Teratogenic effects of exposure to radiofrequency radiation (27.12MHz) from a shortwave diathermy unit. Industrial Health 1988; 26: 1-10.
  • Skreb N, Frank Z. Developmental abnormalities in the rat induced by heat shock. J Embryol Exp Morphol 1963; 11: 445-57.
  • Cockroft DL, New DAT. Effect of hyperthermia on rat embryos in culture. Nature 1975; 258: 604-6.
  • Cockroft DL, New DAT. Abnormalities induced in cultured rat embryos by hyperthermia. Teratology 1978; 17: 277-84.
  • Edwards MJ. Congenital defects in guinea pigs: fetal resorptions, abortions and malformations following induced hyperthermia during early gestation. Teratology 1969; 2: 31328.
  • Edwards MJ. Congenital defects in guinea pigs: prenatal retardation of brain growth following hyperthermia during gestation. Teratology 1969; 2: 329-36.
  • Jonson KM, LyIe JG, Edwards MJ, Penny RHC. Effect of prenatal heat stress on brain growth and serial discrimination reversal learning in the guinea pig. Brain Res Bull 1976; 1: 135-50.
  • Chernoff GF, Golden JA. Hyperthermia-induced exencephaly in mice: effect of multiple exposures. Teratology 1988; 37: 37-42.
  • Shiota K. Induction of neural tube defects and skeletal malformations in mice following brief hyperthermia in utero. Biol Neonate 1988; 53: 86-97.
  • Shiota K, Kayamura T. Effects of prenatal heat stress on postnatal growth, behavior and learning capacity in mice. Biol Neonate 1989; 56: 6-14.
  • Fukui Y, Hoshino K, Inouye M, Kameyama Y. Effects of hyperthermia induced by microwave irradiation on brain development in mice. J Radit Res 1992; 33: 1-10.
  • New DAT. Whole embryo culture and the study of mammalian embryos during organo- genesis. Biol Rev 1978; 53: 81-122.
  • Kimmel GL, Cuff JM, Kimmel CA, Heredia DJ, Tudor N, Silverman PM. Embryonic development in vitro following short-duration exposure to heat. Teratology 1993; 47: 243-51.
  • Webster WS, Germain MA, Edwards MJ. The induction of microphthalmia, encephalo- cele, and other head defects following hyperthermia during the gastrulation process in the rat. Teratology 1985; 31: 73-82.
  • Cawdell-Smith J, Upfold J, Edwards M, Smith M. Neural tube and other developmental anomalies in the guinea pig following maternal hyperthermia during early neural tube development. Teratogen Carcinogen Mutagen 1992; 12: 1-9.
  • Upfold J, Smith MSR, Edwards MJ. Maternal hyperthermia and its effects on embryonic and fetal brain development. In: Hales JRS, Richards DAB, eds, Heat Stress, Physical Exertion and Environment. New York: Excerpta Medica, 1987; 303-11.
  • Edwards MJ, Wanner RA, Mulley RC. Growth and development of the brain in normal and heat-retarded guinea pigs. Neuropathol Appl Neurobiol 1976; 2: 439-50.
  • Edwards MJ. Clinical disorders of fetal brain development. Defects due to hyperthermia. In: Hetzel BS, Smith RM, eds, Fetal Brain Disorders-Recent Approaches to the Problem of Mental Deficiency. New York: Elsevier, 1981; 335-64.
  • LyIe JG, Edwards MJ, Jonson KM. Critical periods and the effects of prenatal heat stress on the learning and brain growth of mature guinea pigs. Biobehav Rev 1977; 1: 1-13.
  • Dutt RH. Critical periods for early embryonic mortality in ewes exposed to high ambient temperature. J Anim Sci 1963; 22: 713-9.
  • Hartley WJ, Alexander G, Edwards MJ. Brain cavitation and micrencephaly in lambs exposed to prenatal hyperthermia. Teratology 1974; 9: 299-303.
  • Tompkins EC, Heidenreich CJ, Stob M. Effect of post breeding thermal stress on embryo- nic mortality in swine. J Anim Sci 1967; 26: 377-80.
  • Poswillo D, Nunnerley H, Sopher D, Keith J. Hyperthermia as a teratogenic agent. Ann R Coll Surg Engl 1974; 55: 171-4.
  • Lomax P. Implications of drugs for heat and exercise tolerance. In: Hales JRS, Richards DAB, eds, Heat Stress, Physical Exertion and Environment. New York: Excerpta Medica, International Congress Series 773, 1987; 399-418.
  • Niswander KR, Gordon M. Collaborative Perinatal study of The National Institute of Neurological Diseases and Stroke. The Women and their Pregnancies, US Dept Education, Health and Welfare. Philadelphia: WB Saunders, 1972; 252-6.
  • Hilbelink DR, Chen LT, Bryant M. Endotoxin induced fever in pregnant golden ham- sters. Teratogen Carcinogen Mutagen 1986; 6: 209-17.
  • Perm VH, Kilham L. Synergistic teratogenic effects of arsenic and hyperthermia in hamsters. Environ Res 1977; 14: 483-6.
  • Perm VH, Perm RR. Teratogenic interactions of hyperthermia and vitamin A. Biol Neonate 1979; 36: 168-72.
  • Edwards MJ, Beatson J. Effects of lead and hyperthermia on prenatal brain growth of guinea pigs. Teratology 1984; 30: 413-21.
  • Shiota K, Shionoya Y, Ide M, Uenobe F, Kurahara C, Fukui Y. Teratogenic interaction of ethanol and hyperthermia in mice. Proc Soc Exp Biol Med 1988; 187: 142-8.
  • Angles JM, Walsh DA, Li K, Barnett SB, Edwards MJ. Effects of pulsed ultrasound and temperature on the development of rat embryos in culture. Teratology 1990; 42: 285-93.
  • Tiboni GM, Iammarrone E, Piccirillo G, Liberal! M, Bellati U. Aspirin pretreatment potentiates hyperthermia-induced teratogenesis in the mouse. Am J Obstet Gynecol 1998; 178: 270-9.
  • Shin JH, Shiota K. Folic acid supplementation of pregnant mice suppresses heat induced neural tube defects in the offspring. J Nutr 1999; 129: 2070-3.
  • Graham JM, Edwards Matthew J, Edwards MJ. Teratogen update: gestational effects of maternal hyperthermia due to febrile illnesses and resultant patterns of defects in humans. Teratology 1998; 58: 209-21.
  • McDonald AD. Maternal health and congenital defect. N Engl J Med 1958; 258: 767-73.
  • McDonald AD. Maternal health in early pregnancy and congenital defect. Final report on a prospective inquiry. Br J Prev Soc Med 1961; 15: 154-66.
  • Milunsky A, Ulcickas M, Rothman KJ, Willett W, Jick SS, Jick H. Maternal heat exposure and neural tube defects. JAMA 1992; 268: 882-5.
  • Clarren SK, Smith DW, Harvey MAS, Ward RH, Myrianthopoulas NC. Hyperthermia; a prospective evaluation of a possible teratogenic agent in man. J Pediatr 1979; 95: 81-3.
  • Sever JL. Infection in pregnancy. Teratology 1982; 25: 227-37.
  • Shiota K. Teratothanasia: prenatal loss of abnormal conceptuses and the prevalence of various malformations during human gestation. Birth Defects. Original Article Series 1993; 29: 189-99.
  • Coffey VP, Jessop WJE. Maternal influenza and congenital deformities; a prospective study. Lancet 1959; 1: 935-8.
  • Coffey VP, Jessop WJE. Maternal influenza and congenital deformities; a follow-up study. Lancet 1961; 1: 748-51.
  • Chambers CD, Johnson KA, Dick LM, Felix RJ, Jones KL. Maternal fever and birth outcome: a prospective study. Teratology 1998; 58: 251-7.
  • Shiota K. Neural tube defects and maternal hyperthermia in early pregnancy: epidemiol- ogy in a human embryo population. Am J Med Genet 1982; 12: 281-8.
  • Chance PF, Smith DW. Hyperthermia and meningomyelocele and anencephaly. Lancet 1978; 1: 769-70.
  • Miller P, Smith DW, Shepard TH. Maternal hyperthermia as a possible cause of anen- cephaly. Lancet 1978; 1: 519-21.
  • Layde PM, Edmonds LD, Erickson JD. Maternal fever and neural tube defects. Teratology 1980; 21: 105-8.
  • Fisher NL, Smith DW. Occipital encephalocele and early gestational hyperthermia. Pediatrics 1981; 68: 480-3.
  • Hunter AGW. Neural tube defects in Eastern Ontario and Western Quebec: demography and family data. Am J Med Genet 1984; 19: 45-63.
  • Fraser FC, Skelton J. Possible teratogenicity of maternal fever. Lancet 1978; 2: 634.
  • Fleet H, Graham JM, Smith DW. Central nervous system and facial defects associated with maternal hyperthermia at 4 to 14 weeks gestation. Pediatrics 1981; 67: 785-9.
  • Graham JM, Edwards MJ. Teratogenic effects of maternal hyperthermia. Ann Res Inst Environ Med 1989; 40: 365-74.
  • Erickson JD. Risk factors for birth defects: data from the Atlanta birth defects case- control study. Teratology 1991; 43: 41-51.
  • Tikkanen J, Heinonen OP. Maternal hyperthermia during pregnancy and cardiovascular malformations in the offspring. Eur J Epidemiol 1991; 7: 628-35.
  • Spraggett K, Fraser FC. Teratogenicity of maternal fever in women. A retrospective study. Teratology 1982; 25: 78.
  • Elliott DS, Burfening PJ, Ulberg LC. Subsequent development during incubation of mouse ova stressed by high ambient temperatures. J Exp Zool 1968; 169: 481-6.

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