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Sex hormone effects on autonomic mechanisms of thermoregulation in humans

Published:November 30, 2015DOI:https://doi.org/10.1016/j.autneu.2015.11.004

      Abstract

      Autonomic mechanisms are fundamental to human physiological thermoregulation, and female reproductive hormones have substantial influences on several aspects of these mechanisms. Of these, the best recognized are the thermoregulatory responses that occur at menopause (hot flushes) and the changes in body temperature within the menstrual cycle which may help couples predict ovulation. Our goal in this brief review is to summarize current knowledge regarding the influences of reproductive hormones on autonomic mechanisms in human thermoregulation. In general, estrogens tend to promote lower body temperatures via augmentation of heat dissipation responses, whereas progesterone tends to promote higher body temperatures. Recent evidence suggests specific influences of estrogens on central autonomic nuclei involved in control of skin blood flow and sweating. Estrogens also augment vasodilation by direct effects on peripheral blood vessels. Influences of progesterone are less well understood, but include both centrally regulated changes in thermoregulatory set-point as well as and peripheral effects, including augmented vasoconstriction in the skin. We conclude with a brief discussion of thermoregulatory adjustments associated with changing hormone levels during menopause, pregnancy and polycystic ovary syndrome.

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      References

        • Avellini B.A.
        • Shapiro Y.
        • Pandolf K.B.
        • Pimental N.A.
        • Goldman R.F.
        Physiological responses of men and women to prolonged dry heat exposure.
        Aviat. Space Environ. Med. 1980; 51: 1081-1085
        • Boulant J.A.
        Neuronal basis of Hammel's model for set-point thermoregulation.
        J. Appl. Physiol. 2006; 100: 1347-1354
        • Brooks E.M.
        • Morgan A.L.
        • Pierzga J.M.
        • Wladkowski S.L.
        • O'Gorman J.T.
        • Derr J.A.
        • Kenney W.L.
        Chronic hormone replacement therapy alters thermoregulatory and vasomotor function in postmenopausal women.
        J. Appl. Physiol. 1997; 83: 477-484
        • Charkoudian N.
        Skin blood flow in adult human thermoregulation: how it works, when it does not, and why.
        Mayo Clin. Proc. 2003; 78: 603-612
        • Charkoudian N.
        Mechanisms and modifiers of reflex induced cutaneous vasodilation and vasoconstriction in humans.
        J. Appl. Physiol. 2010; 109: 1221-1228
        • Charkoudian N.
        • Johnson J.M.
        Modification of active cutaneous vasodilation by oral contraceptive hormones.
        J. Appl. Physiol. 1997; 83: 2012-2018
        • Charkoudian N.
        • Johnson J.M.
        Altered reflex control of cutaneous circulation by female sex steroids is independent of prostaglandins.
        Am. J. Phys. 1999; 276: H1634-H1640
        • Charkoudian N.
        • Johnson J.M.
        Reflex control of cutaneous vasoconstrictor system is reset by exogenous female reproductive hormones.
        J. Appl. Physiol. 1999; 87: 381-385
        • Charkoudian N.
        • Johnson J.M.
        Female reproductive hormones and thermoregulatory control of skin blood flow.
        Exerc. Sport Sci. Rev. 2000; 28: 108-112
        • Charkoudian N.
        • Stachenfeld N.S.
        Reproductive hormone influences on thermoregulation in women.
        Compr. Physiol. 2014; 4: 793-804
        • Cheuvront S.N.
        • Haymes E.M.
        Ad libitum fluid intakes and thermoregulatory responses of female distance runners in three environments.
        J. Sports Sci. 2001; 19: 845-854
        • Clapp 3rd., J.F.
        The changing thermal response to endurance exercise during pregnancy.
        Am. J. Obstet. Gynecol. 1991; 165: 1684-1689
        • Diamanti-Kandarakis E.
        • Dunaif A.
        Insulin resistance and the polycystic ovary syndrome revisited: an update on mechanisms and implications.
        Endocr. Rev. 2012; 33: 981-1030
        • Flanagan A.M.
        • Brown J.L.
        • Santiago C.A.
        • Aad P.Y.
        • Spicer L.J.
        • Spicer M.T.
        High-fat diets promote insulin resistance through cytokine gene expression in growing female rats.
        J. Nutr. Biochem. 2008; 19: 505-513
        • Freedman R.R.
        Physiology of hot flashes.
        Am. J. Hum. Biol. 2001; 13: 453-464
        • Gagnon D.
        • Kenny G.P.
        Sex modulates whole-body sudomotor thermosensitivity during exercise.
        J. Physiol. 2011; 589: 6205-6217
        • Gagnon D.
        • Kenny G.P.
        Does sex have an independent effect on thermoeffector responses during exercise in the heat?.
        J. Physiol. 2012; 590: 5963-5973
        • Gagnon D.
        • Kenny G.P.
        Sex differences in thermoeffector responses during exercise at fixed requirements for heat loss.
        J. Appl. Physiol. (1985). 2012; 113: 746-757
        • Gagnon D.
        • Crandall C.G.
        • Kenny G.P.
        Sex differences in postsynaptic sweating and cutaneous vasodilation.
        J. Appl. Physiol. (1985). 2013; 114: 394-401
        • Gorman A.J.
        • Proppe D.W.
        Mechanisms producing tachycardia in conscious baboons during environmental heat stress.
        J. Appl. Physiol. 1984; 56: 441-446
        • Harrison C.L.
        • Lombard C.B.
        • Moran L.J.
        • Teede H.J.
        Exercise therapy in polycystic ovary syndrome: a systematic review.
        Hum. Reprod. Update. 2011; 17: 171-183
        • Hartgill T.W.
        • Bergersen T.K.
        • Pirhonen J.
        Core body temperature and the thermoneutral zone: a longitudinal study of normal human pregnancy.
        Acta Physiol. (Oxf.). 2011; 201: 467-474
        • Hessemer V.
        • Bruck K.
        Influence of menstrual cycle on shivering, skin blood flow, and sweating responses measured at night.
        J. Appl. Physiol. (1985). 1985; 59: 1902-1910
        • Hubing K.A.
        • Wingo J.E.
        • Brothers R.M.
        • Del Coso J.
        • Low D.A.
        • Crandall C.G.
        Nitric oxide synthase inhibition attenuates cutaneous vasodilation during postmenopausal hot flash episodes.
        Menopause. 2010; 17: 978-982
        • Hutchison S.K.
        • Stepto N.K.
        • Harrison C.L.
        • Moran L.J.
        • Strauss B.J.
        • Teede H.J.
        Effects of exercise on insulin resistance and body composition in overweight and obese women with and without polycystic ovary syndrome.
        J. Clin. Endocrinol. Metab. 2011; 96: E48-E56
        • Johnson J.M.
        • Proppe D.W.
        Cardiovascular adjustments to heat stress.
        in: Handbook of Physiology Environmental Physiology. Oxford University Press, New York1996: 215-244
        • Johnson F.
        • Mavrogianni A.
        • Ucci M.
        • Vidal-Puig A.
        • Wardle J.
        Could increased time spent in a thermal comfort zone contribute to population increases in obesity?.
        Obes. Rev. 2011; 12: 543-551
        • Kelly M.J.
        • Ronnekleiv O.K.
        Minireview: neural signaling of estradiol in the hypothalamus.
        Mol. Endocrinol. 2015; 29: 645-657
        • Kim K.H.
        • Moriarty K.
        • Bender J.R.
        Vascular cell signaling by membrane estrogen receptors.
        Steroids. 2008; 73: 864-869
        • Kolka M.A.
        • Stephenson L.A.
        Effect of luteal phase elevation in core temperature on forearm blood flow during exercise.
        J. Appl. Physiol. (1985). 1997; 82: 1079-1083
        • Low D.A.
        • Davis S.L.
        • Keller D.M.
        • Shibasaki M.
        • Crandall C.G.
        Cutaneous and hemodynamic responses during hot flashes in symptomatic postmenopausal women.
        Menopause. 2008; 15: 290-295
        • Low D.A.
        • Hubing K.A.
        • Del Coso J.
        • Crandall C.G.
        Mechanisms of cutaneous vasodilation during the postmenopausal hot flash.
        Menopause. 2011; 18: 359-365
        • Lowell B.B.
        • Spiegelman B.M.
        Towards a molecular understanding of adaptive thermogenesis.
        Nature. 2000; 404: 652-660
        • Luoto R.
        • Moilanen J.
        • Heinonen R.
        • Mikkola T.
        • Raitanen J.
        • Tomas E.
        • Ojala K.
        • Mansikkamaki K.
        • Nygard C.H.
        Effect of aerobic training on hot flushes and quality of life—a randomized controlled trial.
        Ann. Med. 2012; 44: 616-626
        • McAllen R.M.
        • Farrell M.
        • Johnson J.M.
        • Trevaks D.
        • Cole L.
        • McKinley M.J.
        • Jackson G.
        • Denton D.A.
        • Egan G.F.
        Human medullary responses to cooling and rewarming the skin: a functional MRI study.
        Proc. Natl. Acad. Sci. U. S. A. 2006; 103: 809-813
        • McKinley M.J.
        • Yao S.T.
        • Uschakov A.
        • McAllen R.M.
        • Rundgren M.
        • Martelli D.
        The median preoptic nucleus: front and centre for the regulation of body fluid, sodium, temperature, sleep and cardiovascular homeostasis.
        Acta Physiol. (Oxf.). 2015; 214: 8-32
        • Mittelman-Smith M.A.
        • Williams H.
        • Krajewski-Hall S.J.
        • McMullen N.T.
        • Rance N.E.
        Role for kisspeptin/neurokinin B/dynorphin (KNDy) neurons in cutaneous vasodilatation and the estrogen modulation of body temperature.
        Proc. Natl. Acad. Sci. U. S. A. 2012; 109: 19846-19851
        • Moran L.J.
        • Brinkworth G.
        • Noakes M.
        • Norman R.J.
        Effects of lifestyle modification in polycystic ovarian syndrome.
        Reprod. BioMed. Online. 2006; 12: 569-578
        • Morrison S.F.
        • Madden C.J.
        Central nervous system regulation of brown adipose tissue.
        Compr. Physiol. 2014; 4: 1677-1713
        • Nakamura K.
        Central circuitries for body temperature regulation and fever.
        Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011; 301: R1207-R1228
        • Orshal J.M.
        • Khalil R.A.
        Gender, sex hormones, and vascular tone.
        Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004; 286: R233-R249
        • Rance N.E.
        • Dacks P.A.
        • Mittelman-Smith M.A.
        • Romanovsky A.A.
        • Krajewski-Hall S.J.
        Modulation of body temperature and LH secretion by hypothalamic KNDy (kisspeptin, neurokinin B and dynorphin) neurons: a novel hypothesis on the mechanism of hot flushes.
        Front. Neuroendocrinol. 2013; 34: 211-227
        • Rowell L.B.
        Cardiovascular adjustments to thermal stress.
        in: Handbook of Physiology The Cardiovascular System: Peripheral Circulation and Organ Blood Flow. American Physiological Society, Bethesda1983: 967-1023
        • Shapiro Y.
        • Pandolf K.B.
        • Avellini B.A.
        • Pimental N.A.
        • Goldman R.F.
        Physiological responses of men and women to humid and dry heat.
        J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 1980; 49: 1-8
        • Silva N.L.
        • Boulant J.A.
        Effects of testosterone, estradiol, and temperature on neurons in preoptic tissue slices.
        Am. J. Phys. 1986; 250: R625-R632
        • Stachenfeld N.S.
        • Silva C.
        • Keefe D.L.
        Estrogen modifies the temperature effects of progesterone.
        J. Appl. Physiol. (1985). 2000; 88: 1643-1649
        • Stachenfeld N.S.
        • Yeckel C.W.
        • Taylor H.S.
        Greater exercise sweating in obese women with polycystic ovary syndrome compared with obese controls.
        Med. Sci. Sports Exerc. 2010; 42: 1660-1668
        • Stephenson L.A.
        • Kolka M.A.
        Menstrual cycle phase and time of day alter reference signal controlling arm blood flow and sweating.
        Am. J. Phys. 1985; 249: R186-R191
        • Stephenson L.A.
        • Kolka M.A.
        Esophageal temperature threshold for sweating decreases before ovulation in premenopausal women.
        J. Appl. Physiol. 1999; 86: 22-28
        • Tsilchorozidou T.
        • Overton C.
        • Conway G.S.
        The pathophysiology of polycystic ovary syndrome.
        Clin. Endocrinol. 2004; 60: 1-17
        • Wenner M.M.
        • Taylor H.S.
        • Stachenfeld N.S.
        Progesterone enhances adrenergic control of skin blood flow in women with high but not low orthostatic tolerance.
        J. Physiol. 2011; 589: 975-986