Heat stress on reproductive function and fertility in mammals

Reproductive Medicine and Biology

Volumn 11, Issue 1, 2012, Pages 37-47

  Takahashi, Masashi ^a  

^a NATIONAL AGRICULTURAL RESEARCH CENTER FOR KYUSHU OKINAWA REGION   (Japan)

Author keywords

Heat stress; Livestock animal; Mammal; Oxidative stress; Reproductive function

Indexed keywords

BODY TEMPERATURE; DOMESTIC ANIMAL; EMBRYO DEVELOPMENT; FERTILITY; FERTILIZATION; HEAT STRESS; HIGH TEMPERATURE; MAMMAL; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FUNCTION; PREGNANCY RATE; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SEX DIFFERENCE;

EID: 84861097032     PISSN: 14455781     EISSN: 14470578     Source Type: Journal    
DOI: 10.1007/s12522-011-0105-6     Document Type: Review

References (154)

1. Prosser CL, Heath JE. Temperature. In: Prosser CL, editor. Comparative animal physiology, environmental and metabolic animal physiology. 4th ed. New York: Wiley; 1991. p. 109-66.
2. Berman A, Folman Y, Kaim M, Mamen M, Herz Z, Wolfenson D, Arieli A, Graber Y. Upper critical temperatures and forced ventilation effects for high-yielding dairy cows in a subtropical climate. J Dairy Sci. 1985;68:1488-95.
3. Sartori R, Sartor-Bergfelt R, Mertens SA, Guenther JN, Parrish JJ, Wiltbank MC. Fertilization and early embryonic development in heifers and lactating cows in summer and lactating and dry cows in winter. J Dairy Sci. 2002;85:2803-12. (Pubitemid 38571406)
4. Bohmanova J, Misztal I, Cole JB. Temperature-humidity indices as indicators of milk production losses due to heat stress. J Dairy Sci. 2007;90:1947-56. (Pubitemid 350045417)
5. Ravagnolo O, Misztal I, Hoogenboom G. Genetic component of heat stress in dairy cattle, development of heat index function. J Dairy Sci. 2000;83:2120-5.
6. Renaudeau D, Noblet J. Effects of exposure to high ambient temperature and dietary protein level on sow milk production and performance of piglets. J Anim Sci. 2001;79:1540-8. (Pubitemid 33620431)
7. Huynh TT, Aarnink AJ, Verstegen MW, Gerrits WJ, Heetkamp MJ, Kemp B, Canh TT. Effects of increasing temperatures on physiological changes in pigs at different relative humidities. J Anim Sci. 2005;83:1385-96.
8. Garcia-Ispierto I, Lopez-Gatius F, Santolaria P, Yaniz JL, Nogareda C, Lopez-Bejar M, De Rensis F. Relationship between heat stress during the peri-implantation period and early fetal loss in dairy cattle. Theriogenology. 2006;65:799-807. (Pubitemid 43197476)
9. Wettemann RP, Bazer FW. Influence of environmental temperature on prolificacy of pigs. J Reprod Fertil Suppl. 1985;33:199-208.
10. Banks S, King SA, Irvine DS, Saunders PT. Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction. 2005;129:505-14. (Pubitemid 40542177)
11. Ivell R. Lifestyle impact and the biology of the human scrotum. Reprod Biol Endocrinol. 2007;5:15.
12. Waites GMH. Temperature regulation and the testis. In: Johnson, editors. The testis. 1970. p. 241-79.
13. Wildeus S, Entwistle KW. Spermiogram and sperm reserves in hybrid Bos indicus 9 Bos taurus bulls after scrotal insulation. J Reprod Fertil. 1983;69:711-6. (Pubitemid 13021980)
14. Barth AD, Bowman PA. The sequential appearance of sperm abnormalities after scrotal insulation or dexamethasone treatment in bulls. Can Vet J. 1994;35:93-102. (Pubitemid 24089142)
15. Yaeram J, Setchell BP, Maddocks S. Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev. 2006;18:647-53. (Pubitemid 44048187)
16. Lue Y, Hikim AP, Wang C, Im M, Leung A, Swerdloff RS. Testicular heat exposure enhances the suppression of spermatogenesis by testosterone in rats: the "two-hit" approach to male contraceptive development. Endocrinology. 2000;141:1414-24. (Pubitemid 32269109)
17. Wettemann RP, Wells ME, Omtvedt IT, Pope CE, Turman EJ. Influence of elevated ambient temperature on reproductive performance of boars. J Anim Sci. 1976;42:664-9.
18. Murase T, Imaeda N, Yamada H, Miyazawa K. Seasonal changes in semen characteristics, composition of seminal plasma and frequency of acrosome reaction induced by calcium and calcium ionophore A23187 in Large White boars. J Reprod Dev. 2007;53:853-65. (Pubitemid 47397287)
19. Mieusset R, Quintana Casares PI, Sanchez-Partida LG, Sowerbutts SF, Zupp JL, Setchell BP. The effects of moderate heating of the testes and epididymides of rams by scrotal insulation on body temperature, respiratory rate, spermatozoa output and motility, and on fertility and embryonic survival in ewes inseminated with frozen semen. Ann N Y Acad Sci. 1991;637:445-58.
20. Skinner JD, Louw GN. Heat stress and spermatogenesis in Bos indicus and Bos taurus cattle. J Appl Physiol. 1966;21:1784-90.
21. Love CC, Kenney RM. Scrotal heat stress induces altered sperm chromatin structure associated with a decrease in protamine disulfide bonding in the stallion. Biol Reprod. 1999;60:615-20. (Pubitemid 29102391)
22. Meyerhoeffer DC, Wettemann RP, Coleman SW, Wells ME. Reproductive criteria of beef bulls during and after exposure to increased ambient temperature. J Anim Sci. 1985;60:352-7.
23. Kastelic JP, Cook RB, Coulter GH. Contribution of the scrotum and testes to scrotal and testicular thermoregulation in bulls and rams. J Reprod Fertil. 1996;108:81-5.
24. Kastelic JP, Cook RB, Coulter GH. Effects of ambient temperature and scrotal fleece cover on scrotal and testicular temperatures in rams. Can J Vet Res. 1999;63:157-60. (Pubitemid 129675177)
25. Kunavongkrit A, Suriyasomboon A, Lundeheim N, Heard TW, Einarsson S. Management and sperm production of boars under differing environmental conditions. Theriogenology. 2005;63:657-67. (Pubitemid 40033980)
26. Jannes P, Spiessens C, Van der Auwera I, D'Hooghe T, Verhoeven G, Vanderschueren D. Male subfertility induced by acute scrotal heating affects embryo quality in normal female mice. Hum Reprod. 1998;13:372-5.
27. Paul C, Murray AA, Spears N, Saunders PT. A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction. 2008;136:73-84. (Pubitemid 351984721)
28. Setchell BP, Ekpe G, Zupp JL, Surani MA. Transient retardation in embryo growth in normal female mice made pregnant by males whose testes had been heated. Hum Reprod. 1998;13:342-7.
29. Sailer BL, Sarkar LJ, Bjordahl JA, Jost LK, Evenson DP. Effects of heat stress on mouse testicular cells and sperm chromatin structure. J Androl. 1997;18:294-301. (Pubitemid 27265964)
30. Perez-Crespo M, Pintado B, Gutierrez-Adan A. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol Reprod Dev. 2008;75:40-7. (Pubitemid 350223989)
31. Ax RL, Gilbert GR, Shook GE. Sperm in poor quality semen from bulls during heat stress have a lower affinity for binding hydrogen-3 heparin. J Dairy Sci. 1987;70:195-200.
32. Shiraishi K, Takihara H, Matsuyama H. Elevated scrotal temperature, but not varicocele grade, reflects testicular oxidative stress-mediated apoptosis. World J Urol. 2010;28:359-64.
33. Yamamoto CM, Sinha Hikim AP, Huynh PN, Shapiro B, Lue Y, Salameh WA, Wang C, Swerdloff RS. Redistribution of Bax is an early step in an apoptotic pathway leading to germ cell death in rats, triggered by mild testicular hyperthermia. Biol Reprod. 2000;63:1683-90.
34. Li Y, Zhou Q, Hively R, Yang L, Small C, Griswold MD. Differential gene expression in the testes of different murine strains under normal and hyperthermic conditions. J Androl. 2009;30:325-37.
35. Iuchi Y, Kaneko T, Matsuki S, Sasagawa I, Fujii J. Concerted changes in the YB2/RYB-a protein and protamine 2 messenger RNA in the mouse testis under heat stress. Biol Reprod. 2003;68:129-35. (Pubitemid 36076327)
36. Nichi M, Bols PE, Zuge RM, Barnabe VH, Goovaerts IG, Barnabe RC, Cortada CN. Seasonal variation in semen quality in Bos indicus and Bos taurus bulls raised under tropical conditions. Theriogenology. 2006;66:822-8. (Pubitemid 44192548)
37. Kowalowka M, Wysocki P, Fraser L, Strzezek J. Extracellular superoxide dismutase of boar seminal plasma. Reprod Domest Anim. 2008;43:490-6.
38. Casao A, Cebrian I, Asumpcao ME, Perez-Pe R, Abecia JA, Forcada F, Cebrian-Perez JA, Muino-Blanco T. Seasonal variations of melatonin in ram seminal plasma are correlated to those of testosterone and antioxidant enzymes. Reprod Biol Endocrinol. 8:59.
39. Marti E, Mara L, Marti JI, Muino-Blanco T, Cebrian-Perez JA. Seasonal variations in antioxidant enzyme activity in ram seminal plasma. Theriogenology. 2007;67:1446-54. (Pubitemid 46660987)
40. Rhynes WE, Ewing LL. Testicular endocrine function in Hereford bulls exposed to high ambient temperature. Endocrinology. 1973;92:509-15.
41. Minton JE, Wettemann RP, Meyerhoeffer DC, Hintz RL, Turman EJ. Serum luteinizing hormone and testosterone in bulls during exposure to elevated ambient temperature. J Anim Sci. 1981;53:1551-8.
42. Younas M, Fuquay JW, Smith AE, Moore AB. Estrous and endocrine responses of lactating Holsteins to forced ventilation during summer. J Dairy Sci. 1993;76:430-6.
43. Gwazdauskas FC, Thatcher WW, Kiddy CA, Paape MJ, Wilcox CJ. Hormonal patterns during heat stress following PGF (2) alpha-tham salt induced luteal regression in heifers. Theriogenology. 1981;16:271-85.
44. Trout JP, McDowell LR, Hansen PJ. Characteristics of the estrous cycle and antioxidant status of lactating Holstein cows exposed to heat stress. J Dairy Sci. 1998;81:1244-50. (Pubitemid 128448496)
45. Pennington JA, Albright JL, Diekman MA, Callahan CJ. Sexual activity of Holstein cows: seasonal effects. J Dairy Sci. 1985;68:3023-30.
46. Wise ME, Armstrong DV, Huber JT, Hunter R, Wiersma F. Hormonal alterations in the lactating dairy cow in response to thermal stress. J Dairy Sci. 1988;71:2480-5.
47. Gilad E, Meidan R, Berman A, Graber Y, Wolfenson D. Effect of heat stress on tonic and GnRH-induced gonadotrophin secretion in relation to concentration of oestradiol in plasma of cyclic cows. J Reprod Fertil. 1993;99:315-21. (Pubitemid 24051974)
48. Howell JL, Fuquay JW, Smith AE. Corpus luteum growth and function in lactating Holstein cows during spring and summer. J Dairy Sci. 1994;77:735-9.
49. Burke JM, Spiers DE, Kojima FN, Perry GA, Salfen BE, Wood SL, Patterson DJ, Smith MF, Lucy MC, Jackson WG, Piper EL. Interaction of endophyte-infected fescue and heat stress on ovarian function in the beef heifer. Biol Reprod. 2001;65:260-8. (Pubitemid 32574808)
50. Ozawa M, Tabayashi D, Latief TA, Shimizu T, Oshima I, Kanai Y. Alterations in follicular dynamics and steroidogenic abilities induced by heat stress during follicular recruitment in goats. Reproduction. 2005;129:621-30. (Pubitemid 40691646)
51. Hill TG, Alliston CW. Effects of thermal stress on plasma concentrations of luteinizing hormone, progesterone, prolactin and testosterone in the cycling ewe. Theriogenology. 1981;15:201-9.
52. Carpenter AJ, Nunneley SA. Endogenous hormones subtly alter women's response to heat stress. J Appl Physiol. 1988;65:2313-7. (Pubitemid 19012344)
53. Shimizu T, Ohshima I, Ozawa M, Takahashi S, Tajima A, Shiota M, Miyazaki H, Kanai Y. Heat stress diminishes gonadotropin receptor expression and enhances susceptibility to apoptosis of rat granulosa cells. Reproduction. 2005;129:463-72. (Pubitemid 40542172)
54. Bridges PJ, Brusie MA, Fortune JE. Elevated temperature (heat stress) in vitro reduces androstenedione and estradiol and increases progesterone secretion by follicular cells from bovine dominant follicles. Domest Anim Endocrinol. 2005;29:508-22. (Pubitemid 41253963)
55. Guzeloglu A, Ambrose JD, Kassa T, Diaz T, Thatcher MJ, Thatcher WW. Long-term follicular dynamics and biochemical characteristics of dominant follicles in dairy cows subjected to acute heat stress. Anim Reprod Sci. 2001;66:15-34. (Pubitemid 32382899)
56. De Rensis F, Scaramuzzi RJ. Heat stress and seasonal effects on reproduction in the dairy cow-a review. Theriogenology. 2003;60:1139-51. (Pubitemid 37096440)
57. Wolfenson D, Thatcher WW, Badinga L, Savio JD, Meidan R, Lew BJ, Braw-Tal R, Berman A. Effect of heat stress on follicular development during the estrous cycle in lactating dairy cattle. Biol Reprod. 1995;52:1106-13.
58. Roth Z, Meidan R, Braw-Tal R, Wolfenson D. Immediate and delayed effects of heat stress on follicular development and its association with plasma FSH and inhibin concentration in cows. J Reprod Fertil. 2000;120:83-90.
59. Hansen PJ, Drost M, Rivera RM, Paula-Lopes FF, al-Katanani YM, Krininger CE 3rd, Chase CC Jr. Adverse impact of heat stress on embryo production: causes and strategies for mitigation. Theriogenology. 2001;55:91-103. (Pubitemid 32060566)
60. Roth Z, Meidan R, Shaham-Albalancy A, Braw-Tal R, Wolfenson D. Delayed effect of heat stress on steroid production in medium-sized and preovulatory bovine follicles. Reproduction. 2001;121:745-51. (Pubitemid 32472060)
61. Shehab-El-Deen MA, Leroy JL, Fadel MS, Saleh SY, Maes D, Van Soom A. Biochemical changes in the follicular fluid of the dominant follicle of high producing dairy cows exposed to heat stress early post-partum. Anim Reprod Sci. 2010;117:189-200.
62. de Castro EPLA, Andrzejewski J, Julian D, Spicer LJ, Hansen PJ. Oxygen and steroid concentrations in preovulatory follicles of lactating dairy cows exposed to acute heat stress. Theriogenology. 2008;69:805-13.
63. Grøndahl C, Greve T, Schmidt M, Hunter RHF. Bovine preovulatory follicles are cooler than ovarian stroma and deep rectal temperature. Theriogenology. 1996;45 abstract:289.
64. Hunter RH, Bogh IB, Einer-Jensen N, Muller S, Greve T. Preovulatory graafian follicles are cooler than neighbouring stroma in pig ovaries. Hum Reprod. 2000;15:273-83. (Pubitemid 30076705)
65. Grinsted J, Blendstrup K, Andreasen AG, Byskov MP. Temperature measurements of rabbit antral follicles. J Reprod Fertil. 1980;60:149-55. (Pubitemid 11228312)
66. Grinsted J, Kjer JJ, Blendstrup K, Pedersen JF. Is low temperature of the follicular fluid prior to ovulation necessary for normal oocyte development? Fertil Steril. 1985;43:34-9. (Pubitemid 15198272)
67. Wettemann RP, Bazer FW, Thatcher WW, Caton D, Roberts RM. Conceptus development, uterine response, blood gases and endocrine function of gilts exposed to increased ambient temperature during early pregnancy. Theriogenology. 1988;30:57-74.
68. Lublin A, Wolfenson D. Lactation and pregnancy effects on blood flow to mammary and reproductive systems in heatstressed rabbits. Comp Biochem Physiol A Physiol. 1996;115:277-85. (Pubitemid 27006606)
69. Putney DJ, Drost M, Thatcher WW. Embryonic development in superovulated dairy cattle exposed to elevated ambient temperatures between days 1 to 7 post insemination. Theriogenology. 1988;30:195-209.
70. Ealy AD, Drost M, Hansen PJ. Developmental changes in embryonic resistance to adverse effects of maternal heat stress in cows. J Dairy Sci. 1993;76:2899-905.
71. Ozawa M, Hirabayashi M, Kanai Y. Developmental competence and oxidative state of mouse zygotes heat-stressed maternally or in vitro. Reproduction. 2002;124:683-9. (Pubitemid 35402343)
72. Aroyo A, Yavin S, Arav A, Roth Z. Maternal hyperthermia disrupts developmental competence of follicle-enclosed oocytes: in vivo and ex vivo studies in mice. Theriogenology. 2007;67:1013-21. (Pubitemid 46273593)
73. Baumgartner AP, Chrisman CL. Analysis of post-implantation mouse embryos after maternal heat stress during meiotic maturation. J Reprod Fertil. 1988;84:469-74. (Pubitemid 18268063)
74. Roth Z, Aroyo A, Yavin S, Arav A. The antioxidant epigallocatechin gallate (EGCG) moderates the deleterious effects of maternal hyperthermia on follicle-enclosed oocytes in mice. Theriogenology. 2008;70:887-97.
75. Ozawa M, Matsuzuka T, Hirabayashi M, Kanai Y. Redox status of the oviduct and CDC2 activity in 2-cell stage embryos in heat-stressed mice. Biol Reprod. 2004;71:291-6. (Pubitemid 38915336)
76. Biggers BG, Geisert RD, Wetteman RP, Buchanan DS. Effect of heat stress on early embryonic development in the beef cow. J Anim Sci. 1987;64:1512-8.
77. Wang JZ, Sui HS, Miao DQ, Liu N, Zhou P, Ge L, Tan JH. Effects of heat stress during in vitro maturation on cytoplasmic versus nuclear components of mouse oocytes. Reproduction. 2009;137:181-9.
78. LaRosa C, Downs SM. Meiotic induction by heat stress in mouse oocytes: involvement of AMP-activated protein kinase and MAPK family members. Biol Reprod. 2007;76:476-86.
79. Payton RR, Romar R, Coy P, Saxton AM, Lawrence JL, Edwards JL. Susceptibility of bovine germinal vesicle-stage oocytes from antral follicles to direct effects of heat stress in vitro. Biol Reprod. 2004;71:1303-8. (Pubitemid 39249816)
80. Andreu-Vazquez C, Lopez-Gatius F, Garcia-Ispierto I, Maya-Soriano MJ, Hunter RH, Lopez-Bejar M. Does heat stress provoke the loss of a continuous layer of cortical granules beneath the plasma membrane during oocyte maturation? Zygote. 18:293-9.
81. Sugiyama S, McGowan M, Phillips N, Kafi M, Young M. Effects of increased ambient temperature during IVM and/or IVF on the in vitro development of bovine zygotes. Reprod Domest Anim. 2007;42:271-4. (Pubitemid 46763495)
82. Zhandi M, Towhidi A, Nasr-Esfahani MH, Eftekhari-Yazdi P, Zare-Shahneh A. Unexpected detrimental effect of Insulin like growth factor-1 on bovine oocyte developmental competence under heat stress. J Assist Reprod Genet. 2009;26:605-11.
83. Ju JC, Tseng JK. Nuclear and cytoskeletal alterations of in vitro matured porcine oocytes under hyperthermia. Mol Reprod Dev. 2004;68:125-33.
84. Roth Z, Hansen PJ. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction. 2005;129:235-44. (Pubitemid 40331016)
85. Roth Z, Hansen PJ. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod. 2004;71:1898-906. (Pubitemid 39586934)
86. Soto P, Smith LC. BH4 peptide derived from Bcl-xL and Baxinhibitor peptide suppresses apoptotic mitochondrial changes in heat stressed bovine oocytes. Mol Reprod Dev. 2009;76:637-46.
87. Tseng JK, Tang PC, Ju JC. In vitro thermal stress induces apoptosis and reduces development of porcine parthenotes. Theriogenology. 2006;66:1073-82. (Pubitemid 44232931)
88. Schrock GE, Saxton AM, Schrick FN, Edwards JL. Early in vitro fertilization improves development of bovine ova heat stressed during in vitro maturation. J Dairy Sci. 2007;90:4297-303. (Pubitemid 350045207)
89. Kim M, Geum D, Khang I, Park YM, Kang BM, Lee KA, Kim K. Expression pattern of HSP25 in mouse preimplantation embryo: heat shock responses during oocyte maturation. Mol Reprod Dev. 2002;61:3-13. (Pubitemid 135715260)
90. Edwards JL, Bogart AN, Rispoli LA, Saxton AM, Schrick FN. Developmental competence of bovine embryos from heatstressed ova. J Dairy Sci. 2009;92:563-70.
91. Arechiga CF, Hansen PJ. Response of preimplantation murine embryos to heat shock as modified by developmental stage and glutathione status. In Vitro Cell Dev Biol Anim. 1998;34:655-9. (Pubitemid 29069603)
92. Ealy AD, Howell JL, Monterroso VH, Arechiga CF, Hansen PJ. Developmental changes in sensitivity of bovine embryos to heat Reprod Med Biol (2012) 11:37-47 45 shock and use of antioxidants as thermoprotectants. J Anim Sci. 1995;73:1401-7.
93. Sakatani M, Kobayashi S, Takahashi M. Effects of heat shock on in vitro development and intracellular oxidative state of bovine preimplantation embryos. Mol Reprod Dev. 2004;67:77-82. (Pubitemid 37467338)
94. Edwards JL, Hansen PJ. Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol Reprod Dev. 1997;46:138-45. (Pubitemid 27074997)
95. Krininger CE 3rd, Stephens SH, Hansen PJ. Developmental changes in inhibitory effects of arsenic and heat shock on growth of pre-implantation bovine embryos. Mol Reprod Dev. 2002;63:335-40.
96. Schultz RM. Regulation of zygotic gene activation in the mouse. Bioessays. 1993;15:531-8.
97. Telford NA, Watson AJ, Schultz GA. Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev. 1990;26:90-100. (Pubitemid 20154996)
98. De Sousa PA, Caveney A, Westhusin ME, Watson AJ. Temporal patterns of embryonic gene expression and their dependence on oogenetic factors. Theriogenology. 1998;49:115-28. (Pubitemid 28135787)
99. Edwards MJ. Apoptosis, the heat shock response, hyperthermia, birth defects, disease and cancer. Where are the common links? Cell Stress Chaperones. 1998;3:213-20. (Pubitemid 29051820)
100. Paula-Lopes FF, Hansen PJ. Apoptosis is an adaptive response in bovine preimplantation embryos that facilitates survival after heat shock. Biochem Biophys Res Commun. 2002;295:37-42. (Pubitemid 34743771)
101. Paula-Lopes FF, Hansen PJ. Heat shock-induced apoptosis in preimplantation bovine embryos is a developmentally regulated phenomenon. Biol Reprod. 2002;66:1169-77. (Pubitemid 34263136)
102. Isom SC, Prather RS, Rucker EB 3rd. Heat stress-induced apoptosis in porcine in vitro fertilized and parthenogenetic preimplantation-stage embryos. Mol Reprod Dev. 2007;74:574-81. (Pubitemid 46493746)
103. Jin YX, Lee JY, Choi SH, Kim T, Cui XS, Kim NH. Heat shock induces apoptosis related gene expression and apoptosis in porcine parthenotes developing in vitro. Anim Reprod Sci. 2007;100:118-27. (Pubitemid 46671484)
104. Makarevich AV, Olexikova L, Chrenek P, Kubovicova E, Freharova K, Pivko J. The effect of hyperthermia in vitro on vitality of rabbit preimplantation embryos. Physiol Res. 2007;56:789-96.
105. Drost M, Ambrose JD, Thatcher MJ, Cantrell CK, Wolfsdorf KE, Hasler JF, Thatcher WW. Conception rates after artificial insemination or embryo transfer in lactating dairy cows during summer in Florida. Theriogenology. 1999;52:1161-7.
106. Putney DJ, Drost M, Thatcher WW. Influence of summer heat stress on pregnancy rates of lactating dairy cattle following embryo transfer or artificial insemination. Theriogenology. 1989;31:765-78.
107. Stocco CO, Deis RP. Participation of intraluteal progesterone and prostaglandin F2 alpha in LH-induced luteolysis in pregnant rat. J Endocrinol. 1998;156:253-9. (Pubitemid 28105813)
108. Wolfenson D, Sonego H, Bloch A, Shaham-Albalancy A, Kaim M, Folman Y, Meidan R. Seasonal differences in progesterone production by luteinized bovine thecal and granulosa cells. Domest Anim Endocrinol. 2002;22:81-90. (Pubitemid 34552927)
109. Schrick FN, Inskeep EK, Butcher RL. Pregnancy rates for embryos transferred from early postpartum beef cows into recipients with normal estrous cycles. Biol Reprod. 1993;49:617-21. (Pubitemid 23259688)
110. Maurer RR, Beier HM. Uterine proteins and development in vitro of rabbit preimplantation embryos. J Reprod Fertil. 1976;48:33-41.
111. Breuel KF, Fukuda A, Schrick FN. Effect of prostaglandin F2 on development of 8-cell rat embryos in vitro. Biol Reprod. 1993;48(Suppl. 1):173.
112. Scenna FN, Edwards JL, Rohrbach NR, Hockett ME, Saxton AM, Schrick FN. Detrimental effects of prostaglandin F2alpha on preimplantation bovine embryos. Prostaglandins Other Lipid Mediat. 2004;73:215-26. (Pubitemid 38757799)
113. Soto P, Natzke RP, Hansen PJ. Identification of possible mediators of embryonic mortality caused by mastitis: actions of lipopolysaccharide, prostaglandin F2alpha, and the nitric oxide generator, sodium nitroprusside dihydrate, on oocyte maturation and embryonic development in cattle. Am J Reprod Immunol. 2003;50:263-72. (Pubitemid 37045306)
114. Scott JE, Persaud TV. Prostaglandin F2alpha conceptus-endometrial interaction during early gestation in the mouse. Prostaglandins Med. 1981;7:133-47. (Pubitemid 11040729)
115. Putney DJ, Malayer JR, Gross TS, Thatcher WW, Hansen PJ, Drost M. Heat stress-induced alterations in the synthesis and secretion of proteins and prostaglandins by cultured bovine conceptuses and uterine endometrium. Biol Reprod. 1988;39:717-28.
116. Nakamura H, Matsuzaki I, Hatta K, Ogino K. Physiological involvement of placental endothelin-1 and prostaglandin F2alpha in uteroplacental circulatory disturbance in pregnant rats exposed to heat stress. Can J Physiol Pharmacol. 2004;82:225-30. (Pubitemid 38859592)
117. Hensleigh PA, Johnson DC. Heat stress effects during pregnancy. I. Retardation of fetal rat growth. Fertil Steril. 1971;22:522-7.
118. Padmanabhan R, Al-Menhali NM, Ahmed I, Kataya HH, Ayoub MA. Histological, histochemical and electron microscopic changes of the placenta induced by maternal exposure to hyperthermia in the rat. Int J Hyperth. 2005;21:29-44. (Pubitemid 40124621)
119. Bell AW, McBride BW, Slepetis R, Early RJ, Currie WB. Chronic heat stress and prenatal development in sheep: I. Conceptus growth and maternal plasma hormones and metabolites. J Anim Sci. 1989;67:3289-99.
120. Vatnick I, Ignotz G, McBride BW, Bell AW. Effect of heat stress on ovine placental growth in early pregnancy. J Dev Physiol. 1991;16:163-6.
121. Early RJ, McBride BW, Vatnick I, Bell AW. Chronic heat stress and prenatal development in sheep: II. Placental cellularity and metabolism. J Anim Sci. 1991;69:3610-6.
122. Gericke GS, Hofmeyr GJ, Laburn H, Isaacs H. Does heat damage fetuses? Med Hypotheses. 1989;29:275-8. (Pubitemid 19206877)
123. Collier RJ, Doelger SG, Head HH, Thatcher WW, Wilcox CJ. Effects of heat stress during pregnancy on maternal hormone concentrations, calf birth weight and postpartum milk yield of Holstein cows. J Anim Sci. 1982;54:309-19.
124. Hansen PJ. Effects of heat stress on mammalian reproduction. Philos Trans R Soc Lond B Biol Sci. 2009;364:3341-50.
125. Ghasemi N, Babaei H, Azizallahi S, Kheradmand A. Effect of long-term administration of zinc after scrotal heating on mice spermatozoa and subsequent offspring quality. Andrologia. 2009;41:222-8.
126. Balog T, Sobocanec S, Sverko V, Krolo I, Rocic B, Marotti M, Marotti T. The influence of season on oxidant-antioxidant status in trained and sedentary subjects. Life Sci. 2006;78:1441-7. (Pubitemid 43233811)
127. Bernabucci U, Ronchi B, Lacetera N, Nardone A. Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. J Dairy Sci. 2002;85:2173-9. (Pubitemid 38572135)
128. Wang L, Xue B, Wang K, Li S, Li Z. Effect of heat stress on endotoxin flux across mesenteric-drained and portal-drained viscera of dairy goat. J Anim Physiol Anim Nutr (Berl). 2010. doi:10.1111/j.1439-0396.
129. Matsuzuka T, Ozawa M, Nakamura A, Ushitani A, Hirabayashi M, Kanai Y. Effects of heat stress on the redox status in the oviduct and early embryonic development in mice. J Reprod Dev. 2005;51:281-7. (Pubitemid 41359854)
130. Ando M, Katagiri K, Yamamoto S, Asanuma S, Usuda M, Kawahara I, Wakamatsu K. Effect of hyperthermia on glutathione peroxidase and lipid peroxidative damage in river. J Therm Biol. 1994;19:177-85.
131. Lapointe J, Bilodeau JF. Antioxidant defenses are modulated in the cow oviduct during the estrous cycle. Biol Reprod. 2003;68:1157-64. (Pubitemid 36361992)
132. Sakamoto N, Ozawa M, Yokotani-Tomita K, Morimoto A, Matsuzuka T, Ijiri D, Hirabayashi M, Ushitani A, Kanai Y. DLalphatocopherol acetate mitigates maternal hyperthermiainduced pre-implantation embryonic death accompanied by a reduction of physiological oxidative stress in mice. Reproduction. 2008;135:489-96. (Pubitemid 351578155)
133. Matsuzuka T, Sakamoto N, Ozawa M, Ushitani A, Hirabayashi M, Kanai Y. Alleviation of maternal hyperthermia-induced early embryonic death by administration of melatonin to mice. J Pineal Res. 2005;39:217-23. (Pubitemid 41337800)
134. Arechiga CF, Staples CR, McDowell PJ, Hansen LR. Effects of timed insemination and supplemental beta-carotene on reproduction and milk yield of dairy cows under heat stress. J Dairy Sci. 1998;81:390-402. (Pubitemid 128444836)
135. Arechiga CF, Vazquez-Flores S, Ortiz O, Hernandez-Ceron J, Porras A, McDowell LR, Hansen PJ. Effect of injection of betacarotene or vitamin E and selenium on fertility of lactating dairy cows. Theriogenology. 1998;50:65-76. (Pubitemid 28354669)
136. Sakatani M, Suda I, Oki T, Kobayashi S, Kobayashi S, Takahashi M. Effects of purple sweet potato anthocyanins on development and intracellular redox status of bovine preimplantation embryos exposed to heat shock. J Reprod Dev. 2007;53:605-14. (Pubitemid 47052586)
137. Namekawa T, Ikeda S, Sugimoto M, Kume S. Effects of astaxanthincontaining oil on development and stress-related gene expression of bovine embryos exposed to heat stress. Reprod Domest Anim. 2010;45:387-91.
138. Sakatani M, Yamanaka K, Kobayashi S, Takahashi M. Heatshockderived reactive oxygen species induce embryonic mortality in in vitro early stage bovine embryos. J Reprod Dev. 2008;54:496-501.
139. Gardiner CS, Reed DJ. Status of glutathione during oxidantinduced oxidative stress in the preimplantation mouse embryo. Biol Reprod. 1994;51:1307-14. (Pubitemid 24354293)
140. Ishibashi M, Akazawa S, Sakamaki H, Matsumoto K, Yamasaki H, Yamaguchi Y, Goto S, Urata Y, Kondo T, Nagataki S. Oxygen-induced embryopathy and the significance of glutathionedependent antioxidant system in the rat embryo during early organogenesis. Free Radic Biol Med. 1997;22:447-54. (Pubitemid 27020118)
141. Wells PG, Kim PM, Laposa RR, Nicol CJ, Parman T, Winn LM. Oxidative damage in chemical teratogenesis. Mutat Res. 1997;396:65-78. (Pubitemid 28012643)
142. Whitaker BD, Knight JW. Mechanisms of oxidative stress in porcine oocytes and the role of anti-oxidants. Reprod Fertil Dev. 2008;20:694-702. (Pubitemid 351962220)
143. Takahashi M, Nagai T, Hamano S, Kuwayama M, Okamura N, Okano A. Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biol Reprod. 1993;49:228-32. (Pubitemid 23210241)
144. Takahashi M, Nagai T, Okamura N, Takahashi H, Okano A. Promoting effect of beta-mercaptoethanol on in vitro development under oxidative stress and cystine uptake of bovine embryos. Biol Reprod. 2002;66:562-7. (Pubitemid 34193908)
145. Arechiga CF, Ealy AD, Hansen PJ. Evidence that glutathione is involved in thermotolerance of preimplantation murine embryos. Biol Reprod. 1995;52:1296-301.
146. Lopez-Gatius F. Is fertility declining in dairy cattle? A retrospective study in northeastern Spain. Theriogenology. 2003;60:89-99. (Pubitemid 36524440)
147. Srikandakumar A, Johnson EH. Effect of heat stress on milk production, rectal temperature, respiratory rate and blood chemistry in Holstein, Jersey and Australian Milking Zebu cows. Trop Anim Health Prod. 2004;36:685-92. (Pubitemid 39283023)
148. Al-Katanani YM, Webb DW, Hansen PJ. Factors affecting seasonal variation in 90-day nonreturn rate to first service in lactating Holstein cows in a hot climate. J Dairy Sci. 1999;82:2611-6. (Pubitemid 129545909)
149. Lacetera N, Bernabucci U, Scalia D, Basirico L, Morera P, Nardone A. Heat stress elicits different responses in peripheral blood mononuclear cells from Brown Swiss and Holstein cows. J Dairy Sci. 2006;89:4606-12. (Pubitemid 46118361)
150. Hernandez-Ceron J, Chase CC Jr, Hansen PJ. Differences in heat tolerance between preimplantation embryos from Brahman, Romosinuano, and Angus breeds. J Dairy Sci. 2004;87:53-8. (Pubitemid 44145432)
151. Paula-Lopes FF, Chase CC Jr, Al-Katanani YM, Krininger CE 3rd, Rivera RM, Tekin S, Majewski AC, Ocon OM, Olson TA, Hansen PJ. Genetic divergence in cellular resistance to heat shock in cattle: differences between breeds developed in temperate versus hot climates in responses of preimplantation embryos, reproductive tract tissues and lymphocytes to increased culture temperatures. Reproduction. 2003;125:285-94. (Pubitemid 36284900)
152. Hansen PJ. Physiological and cellular adaptations of zebu cattle to thermal stress. Anim Reprod Sci. 2004;82-83:349-60. (Pubitemid 39027071)
153. Barros CM, Pegorer MF, Vasconcelos JL, Eberhardt BG, Monteiro FM.
154. Pegorer MF, Vasconcelos JL, Trinca LA, Hansen PJ, Barros CM. Influence of sire and sire breed (Gyr versus Holstein) on establishment of pregnancy and embryonic loss in lactating Holstein cows during summer heat stress. Theriogenology. 2007;67:692-7. (Pubitemid 46161736)