Is Sex Hormone a Risk Factor of Nociceptive Hypersensitivity in the Context of Cerebrovascular Diseases?
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Published
Oct 5, 2018
Abstract
Cerebral vessel events have long been considered a leading cause in postmenopausal women with physiological changes in expressing and secreting of sex hormones. Hormone replacement therapy emerged as a supplementary therapeutic strategy under the risk of cerebrovascular accidents and bone loss. Epidemiological and genetic data showed that an interrelationship among hormone and cerebrovascular disorders exist. A battery of animal experiments and clinical observations received different results both positive and negative. Recent studies still cannot give a once-for-all answer to whichever hormone, estrogen or progesterone overweighs the other in benefits. Here we review and analyze the two hormones’ effects on cerebrovascular diseases and that of associated epidemiological and genetic evidences.
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Keywords
Cerebrovascular Disease, Sex Hormone, Estrogen, Progesterone, Inflammation
Supporting Agencies
This work is supported by the National Natural Scientific Foundation of China (81560200).
References
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7. Grewal RP. Stroke in Fabry’s disease. J Neurol 1994; 241: 153-156.
8. Parlakis SG, Phillips PC, Dimauro S, De Vivo DS, Rowland LP. Mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes: a distinctive clinical syndrome. Ann Neurol 1984;16:481-488.
9. Ohene-Frempong K, Weinen SJ, Sleeper LA, Miller ST, Embury S, Moohr JW, Wethers DL, Pegelow CH, Gill FM. Cerebrovascular accidents in sickle cell disease: rates and risk factors. Blood 1998; 91: 288-294.
10. Wade DT, De Jong BA. Recent advances in rehabilitation. Br Med J 2000; 320:1385-1388.
11. Granger CV, Hamilton BB, Sherwin FS. Guide for the use of the uniform data set for medical rehabilitation. Uniform data set for medical rehabilitation project office. Buffalo, NY: Buffalo General Hospital, 1986.
12. Collin C, Wade DT, Davis S, Horne V. The Barthel ADL Inndex: a reliability study. Int Disabil Stud 1988; 10:61-63.
13. Twitchell T. Restoration of motor function following hemiplegia in man. Brain 1951; 74:443-480.
14. Adams HP. Handbook of cerebrovascular diseases. Rehabilitation after stroke. 2nd Ed, Marcel Dekker, New York, 2005; pp231-241.
15. Chen J, Chopp M, and Li Y. Neuroprotective effects of progesterone after transient middle cerebral artery occlusion in rat. J Neurol Sci 1999; 171:24-30.
16. Kumon Y, Kim SC, Tompkins P, Stevens A, Sakaki S, Loftus CM. Neuroprotective effect of postischemic administration of progesterone in spontaneously hypertensive rats with focal cerebral ischemia. J Neurosurg 2000; 92:848-852.
17. Cerrantes M, Gonzalez-Vidal MD, Ruelas R, Escobar A, Morali G. Neuroprotective effects of progesterone on damage elicited by acute global cerebral ischemia in neurons of the caudate nucleus. Arch Med Res 2002; 33:6-14.
18. Genzalez-Vidal MD, Cervera-Gaviria M, Ruelas R, Escobar A, Morali G, Cervantes M. Progesterone: protective effects on the cat hippocampal neuronal damage due to acute global cerebral ischemia. Arch Med Res 1998; 29:117-124.
19. Gibson CL, Murphy SP. Progesterone enhances functional recovery after middle cerebral artery occlusion in male mice. J Cereb Blood Flow Metab 2004; 24:805-813.
20. Murphy SJ, Littleton-Kearney MT, Hurn PD. Progesterone administration during reperfusion, but not preischemia alone, reduces injury in ovariectomized rats. J Cereb Blood Flow Metab 2002; 22:1181-1188.
21. Murphy SJ, Traystman RJ, Hurn PD. Progesterone exacerbates striatal stroke injury in progesterone-deficient female animals. Stroke 2000; 31:1173-1178.
22. Burkman RT. Hormone replacement therapy. Current controversies. Minerva Ginecol 2003; 55:107-116.
23. Sitruk-Ware R. New progestagens for contraceptive use. Hum Reprod Update 2006; 12:169-178.
24. Stein DG, Hoffman SW. Estrogen and progesterone as neuroprotective agents in the treatment of acute brain injuries. Pediatr Rehabil 2003; 6:13-22.
25. Roof RL, Hall ED. Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. J Neurotrauma 2000; 17:367-388.
26. Perez E, Liu R, Yang SH, Cai ZY, Covey DF, Simpkins JW. Neuroprotective effects of an estratriene analog are estrogen receptor independent in vitro and in vivo. Brain Res 2005; 1038:216-222.
27. Cimarosti H, Siqueira IR, Zamin LL, Nassif M, Balk R, Frozza R, Dalmaz C, Netto CA, Salbego C. Neuroprotection and protein damage prevention by estradiol replacement in rat hippocampal slices exposed to oxygen-glucose deprivation. Neurochem Res 2005; 30:583-589.
28. Sumino H, Ichikawa S, Kasama S, Kumakura H, Takayama Y, Sakamaki T, Kurabayashi M. Effect of Transdermal Hormone Replacement Therapy on Carotid Artery Wall Thickness and Levels of Vascular Inflammatory Markers in Postmenopausal Women. Hypertens Res 2005; 28: 579-584.
29. Gordon KB, Macrae IM, Carswell HVO. Effects of 17beta-oestradiol on cerebral ischaemic damage and lipid peroxidation. Brain Res 2005; 1036:155-162.
30. Yong Y, Xie HJ, Zhang YF, Yang QD, Liao DF,Yang HL, Yan PK, Liu ZJ. 17beta-estradiol potentiates ischemia–reperfusion injury in diabetic ovariectomized female rats. Brain Res 2005; 1054:192-199.
31. Goodrow GJ, Vitullo L, Cipolla MJ. Effect of estrogen therapy on cerebral arteries during stroke in female rats. Menopause 2005; 12:99-109.
32. Stein DG. Brain damage, sex hormones and recovery: a new role for progesterone and estrogen? Trends Neurosci 2001; 24:386-391.
33. Moralí G, Letechipía-Vallejo G, López-Loeza E, Montes P, Hernández-Morales L, Cervantes M. Post-ischemic administration of progesterone in rats exerts neuroprotective effects on the hippocampus. Neurosci Lett 2005; 382:286-290.
34. Gibson CL, Constantin D, Prior MJW, Bath PMW, Murphy SP. Progesterone suppresses the inflammatory response and nitric oxide synthase-2 expression following cerebral ischemia. Exp Neurol 2005; 193:522-530.
35. Thomas T, Rhodin J, Clark L, Garces A. Progestins initiate adverse events of menopausal estrogen therapy. Climacteric 2003; 6:293-301.
36. Pelligrino DA, Galea E. Estrogen and cerebrovascular physiology and pathophysiology. Jpn J Pharmacol 2001; 86:137-158.
37. Thomas T, Rhodin JA, Sutton ET, Bryant MW, Price JM. Estrogen protects peripheral and cerebral blood vessels from toxicity of Alzheimer peptide amyloid-beta and inflammatory reaction. J Submicrosc Cytol Pathol 1999; 31:571-579.
38. Stork S, von Schacky C, Angerer P. The effect of 17beta-estradiol an endothelial and inflammatory markers in postmenopausal women: a randomized controlled trial. Atherosclerosis 2002; 165:301-307.
39. Losem-Heinrichs E, Görg B, Redecker C , Schleicher A , Witte OW, Zilles K, Bidmon HJ. 1alpha,25-Dihydroxy-vitamin D3 in combination with 17beta-estradiol lowers the cortical expression of heat shock protein-27 following experimentally induced focal cortical ischemia in rats. Arch Biochem Biophys 2005; 439: 70-79.
40. Xing D, Miller A, Novak L, Rocha R, Chen YF, Oparil S. Estradiol and progestins differentially modulate leukocyte infiltration after vascular injury. Circulation 2004; 109:234-241.
41. Liu R, Wen Y, Perez E, Wang X, Day AL, Simpkins JW, Yang SH. 17beta-Estradiol attenuates blood–brain barrier disruption induced by cerebral ischemia–reperfusion injury in female rats. Brain Res 2005; 1060:55-61.
42. Sunday L, Tran MM, Krause DN, Duckles SP. Estrogen and progesterones differentially modulate vascular proinflammatory factors. Am J Physiol Endocrinol Metab, 2006; 291: E261-E267.
43. Pan Y, Acharya AB, Patrick PH, Oliver D, Morley JE, Zhang H. Effect of testosterone on functional recovery in a castrate male rat stroke model. Brain Res 2005; 1043:195-204.
44. Brass LM. Hormone replacement therapy and stroke clinical trials review. Stroke 2004; Suppl I: 2644-2647.
45. Bath PMW, Gray LJ. Association between hormone replacement therapy and subsequent stroke: a meta-analysis. Br Med J 2005; 330:342-345.
46. Couzin J. The great estrogen conundrum. Science 302:1136-1138, 2003.
47. Wickelgren I. Brain researchers try to salvage estrogen treatment. Science 2003; 302:1138-1138.
48. Bartley EJ, Fillingim RB. Sex differences in pain: a brief review of clinical and experimental findings. Br J Anaesth 2013; 111:52-58.
49. Dao TT, LeResche L. Gender differences in pain. J Orofac Pain 2000; 14:169-195.
50. Maurer AJ, Lissounov A, Knezevic I, Candido KD, Knezevic NN. Pain and sex hormones: a review of current understanding. Pain Manag 2016; 6:285-296.
51. Macfarlane TV, Blinkhorn A, Worthington HV, Davies RM, Macfarlane GJ. Sex hormonal factors and chronic widespread pain: a population study among women. Rheumatology (Oxford), 2002; 41:454-457.
52. Licini F, Nojelli A, Segù M, Collesano V. Role of psychosocial factors in the etiology of temporomandibular disorders: relevance of a biaxial diagnosis. Minerva Stomatol 2009; 58:557-566.
53. Haast RA, Gustafson DR, Kiliaan AJ. Sex differences in stroke. J Cereb Blood Flow Metab 2012; 32:2100-2107.
54. Marcus DA. Sex hormones and chronic headache in women. Expert Opin Pharmacother 2001; 2:1839-1848.
55. Bruce S. McEwen1 and Teresa A. Milner. Understanding the Broad Influence of Sex Hormones and Sex Differences in the Brain. J Neurosci Res 2017; 95:24-39.
2. Anonymous. Special report from the National Institute of Neurological Disorders and Stroke. Classification of cerebrovascular diseases III. Stroke 1990; 21:637-676.
3. Adams HP. Handbook of cerebrovascular diseases. Epidemiology and risk factors for stroke. 2nd Ed, Marcel Dekker, New York, 2005; pp 1-20.
4. Krishner HS. Medical prevention of stroke. South Med J 2003; 96: 354-358.
5. Adams HP. Handbook of cerebrovascular diseases. Genetic causes of stroke. 2nd Ed, Marcel Dekker, New York, 2005; pp743-761.
6. Joutel A, Corpechot C, Ducros A, Vahedi K, Chabriat H, Mouton P, Alamowitch S, Domenga V, Cecillion M, Marechal E, Maciazek J, Vayssiere C, Cruaud C, Cabanis EA, Ruchoux MM, Weissenbath J, Bach JF, Bousser MG, Tournier-Lasserve E. Notch 3 mutation in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 1996; 383: 707-710.
7. Grewal RP. Stroke in Fabry’s disease. J Neurol 1994; 241: 153-156.
8. Parlakis SG, Phillips PC, Dimauro S, De Vivo DS, Rowland LP. Mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes: a distinctive clinical syndrome. Ann Neurol 1984;16:481-488.
9. Ohene-Frempong K, Weinen SJ, Sleeper LA, Miller ST, Embury S, Moohr JW, Wethers DL, Pegelow CH, Gill FM. Cerebrovascular accidents in sickle cell disease: rates and risk factors. Blood 1998; 91: 288-294.
10. Wade DT, De Jong BA. Recent advances in rehabilitation. Br Med J 2000; 320:1385-1388.
11. Granger CV, Hamilton BB, Sherwin FS. Guide for the use of the uniform data set for medical rehabilitation. Uniform data set for medical rehabilitation project office. Buffalo, NY: Buffalo General Hospital, 1986.
12. Collin C, Wade DT, Davis S, Horne V. The Barthel ADL Inndex: a reliability study. Int Disabil Stud 1988; 10:61-63.
13. Twitchell T. Restoration of motor function following hemiplegia in man. Brain 1951; 74:443-480.
14. Adams HP. Handbook of cerebrovascular diseases. Rehabilitation after stroke. 2nd Ed, Marcel Dekker, New York, 2005; pp231-241.
15. Chen J, Chopp M, and Li Y. Neuroprotective effects of progesterone after transient middle cerebral artery occlusion in rat. J Neurol Sci 1999; 171:24-30.
16. Kumon Y, Kim SC, Tompkins P, Stevens A, Sakaki S, Loftus CM. Neuroprotective effect of postischemic administration of progesterone in spontaneously hypertensive rats with focal cerebral ischemia. J Neurosurg 2000; 92:848-852.
17. Cerrantes M, Gonzalez-Vidal MD, Ruelas R, Escobar A, Morali G. Neuroprotective effects of progesterone on damage elicited by acute global cerebral ischemia in neurons of the caudate nucleus. Arch Med Res 2002; 33:6-14.
18. Genzalez-Vidal MD, Cervera-Gaviria M, Ruelas R, Escobar A, Morali G, Cervantes M. Progesterone: protective effects on the cat hippocampal neuronal damage due to acute global cerebral ischemia. Arch Med Res 1998; 29:117-124.
19. Gibson CL, Murphy SP. Progesterone enhances functional recovery after middle cerebral artery occlusion in male mice. J Cereb Blood Flow Metab 2004; 24:805-813.
20. Murphy SJ, Littleton-Kearney MT, Hurn PD. Progesterone administration during reperfusion, but not preischemia alone, reduces injury in ovariectomized rats. J Cereb Blood Flow Metab 2002; 22:1181-1188.
21. Murphy SJ, Traystman RJ, Hurn PD. Progesterone exacerbates striatal stroke injury in progesterone-deficient female animals. Stroke 2000; 31:1173-1178.
22. Burkman RT. Hormone replacement therapy. Current controversies. Minerva Ginecol 2003; 55:107-116.
23. Sitruk-Ware R. New progestagens for contraceptive use. Hum Reprod Update 2006; 12:169-178.
24. Stein DG, Hoffman SW. Estrogen and progesterone as neuroprotective agents in the treatment of acute brain injuries. Pediatr Rehabil 2003; 6:13-22.
25. Roof RL, Hall ED. Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. J Neurotrauma 2000; 17:367-388.
26. Perez E, Liu R, Yang SH, Cai ZY, Covey DF, Simpkins JW. Neuroprotective effects of an estratriene analog are estrogen receptor independent in vitro and in vivo. Brain Res 2005; 1038:216-222.
27. Cimarosti H, Siqueira IR, Zamin LL, Nassif M, Balk R, Frozza R, Dalmaz C, Netto CA, Salbego C. Neuroprotection and protein damage prevention by estradiol replacement in rat hippocampal slices exposed to oxygen-glucose deprivation. Neurochem Res 2005; 30:583-589.
28. Sumino H, Ichikawa S, Kasama S, Kumakura H, Takayama Y, Sakamaki T, Kurabayashi M. Effect of Transdermal Hormone Replacement Therapy on Carotid Artery Wall Thickness and Levels of Vascular Inflammatory Markers in Postmenopausal Women. Hypertens Res 2005; 28: 579-584.
29. Gordon KB, Macrae IM, Carswell HVO. Effects of 17beta-oestradiol on cerebral ischaemic damage and lipid peroxidation. Brain Res 2005; 1036:155-162.
30. Yong Y, Xie HJ, Zhang YF, Yang QD, Liao DF,Yang HL, Yan PK, Liu ZJ. 17beta-estradiol potentiates ischemia–reperfusion injury in diabetic ovariectomized female rats. Brain Res 2005; 1054:192-199.
31. Goodrow GJ, Vitullo L, Cipolla MJ. Effect of estrogen therapy on cerebral arteries during stroke in female rats. Menopause 2005; 12:99-109.
32. Stein DG. Brain damage, sex hormones and recovery: a new role for progesterone and estrogen? Trends Neurosci 2001; 24:386-391.
33. Moralí G, Letechipía-Vallejo G, López-Loeza E, Montes P, Hernández-Morales L, Cervantes M. Post-ischemic administration of progesterone in rats exerts neuroprotective effects on the hippocampus. Neurosci Lett 2005; 382:286-290.
34. Gibson CL, Constantin D, Prior MJW, Bath PMW, Murphy SP. Progesterone suppresses the inflammatory response and nitric oxide synthase-2 expression following cerebral ischemia. Exp Neurol 2005; 193:522-530.
35. Thomas T, Rhodin J, Clark L, Garces A. Progestins initiate adverse events of menopausal estrogen therapy. Climacteric 2003; 6:293-301.
36. Pelligrino DA, Galea E. Estrogen and cerebrovascular physiology and pathophysiology. Jpn J Pharmacol 2001; 86:137-158.
37. Thomas T, Rhodin JA, Sutton ET, Bryant MW, Price JM. Estrogen protects peripheral and cerebral blood vessels from toxicity of Alzheimer peptide amyloid-beta and inflammatory reaction. J Submicrosc Cytol Pathol 1999; 31:571-579.
38. Stork S, von Schacky C, Angerer P. The effect of 17beta-estradiol an endothelial and inflammatory markers in postmenopausal women: a randomized controlled trial. Atherosclerosis 2002; 165:301-307.
39. Losem-Heinrichs E, Görg B, Redecker C , Schleicher A , Witte OW, Zilles K, Bidmon HJ. 1alpha,25-Dihydroxy-vitamin D3 in combination with 17beta-estradiol lowers the cortical expression of heat shock protein-27 following experimentally induced focal cortical ischemia in rats. Arch Biochem Biophys 2005; 439: 70-79.
40. Xing D, Miller A, Novak L, Rocha R, Chen YF, Oparil S. Estradiol and progestins differentially modulate leukocyte infiltration after vascular injury. Circulation 2004; 109:234-241.
41. Liu R, Wen Y, Perez E, Wang X, Day AL, Simpkins JW, Yang SH. 17beta-Estradiol attenuates blood–brain barrier disruption induced by cerebral ischemia–reperfusion injury in female rats. Brain Res 2005; 1060:55-61.
42. Sunday L, Tran MM, Krause DN, Duckles SP. Estrogen and progesterones differentially modulate vascular proinflammatory factors. Am J Physiol Endocrinol Metab, 2006; 291: E261-E267.
43. Pan Y, Acharya AB, Patrick PH, Oliver D, Morley JE, Zhang H. Effect of testosterone on functional recovery in a castrate male rat stroke model. Brain Res 2005; 1043:195-204.
44. Brass LM. Hormone replacement therapy and stroke clinical trials review. Stroke 2004; Suppl I: 2644-2647.
45. Bath PMW, Gray LJ. Association between hormone replacement therapy and subsequent stroke: a meta-analysis. Br Med J 2005; 330:342-345.
46. Couzin J. The great estrogen conundrum. Science 302:1136-1138, 2003.
47. Wickelgren I. Brain researchers try to salvage estrogen treatment. Science 2003; 302:1138-1138.
48. Bartley EJ, Fillingim RB. Sex differences in pain: a brief review of clinical and experimental findings. Br J Anaesth 2013; 111:52-58.
49. Dao TT, LeResche L. Gender differences in pain. J Orofac Pain 2000; 14:169-195.
50. Maurer AJ, Lissounov A, Knezevic I, Candido KD, Knezevic NN. Pain and sex hormones: a review of current understanding. Pain Manag 2016; 6:285-296.
51. Macfarlane TV, Blinkhorn A, Worthington HV, Davies RM, Macfarlane GJ. Sex hormonal factors and chronic widespread pain: a population study among women. Rheumatology (Oxford), 2002; 41:454-457.
52. Licini F, Nojelli A, Segù M, Collesano V. Role of psychosocial factors in the etiology of temporomandibular disorders: relevance of a biaxial diagnosis. Minerva Stomatol 2009; 58:557-566.
53. Haast RA, Gustafson DR, Kiliaan AJ. Sex differences in stroke. J Cereb Blood Flow Metab 2012; 32:2100-2107.
54. Marcus DA. Sex hormones and chronic headache in women. Expert Opin Pharmacother 2001; 2:1839-1848.
55. Bruce S. McEwen1 and Teresa A. Milner. Understanding the Broad Influence of Sex Hormones and Sex Differences in the Brain. J Neurosci Res 2017; 95:24-39.
How to Cite
Bao, S. (2018). Is Sex Hormone a Risk Factor of Nociceptive Hypersensitivity in the Context of Cerebrovascular Diseases?. Science Insights, 2018(10), 1–8. https://doi.org/10.15354/si.18.re079
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