Sex and pain perception and analgesia;Sexo e Percepção da Dor e Analgesia

Revista Brasileira de Anestesiologia

Volumn 61, Issue 6, 2011, Pages 814-828

  Palmeira, Cláudia Carneiro de Araújo ^a   Ashmawi, Hazem Adel ^a   Posso, Irimar de Paula ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Gonadal Steroid Hormones; Pain; Sex Factors

Indexed keywords

ACETYLCHOLINE; ANDROGEN; BETA ENDORPHIN; DOPAMINE; ESTRADIOL; ESTRIOL; ESTROGEN; ESTRONE; MITOGEN ACTIVATED PROTEIN KINASE; MORPHINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NOCICEPTIN; PROGESTERONE; PROTEIN C FOS; SEROTONIN; STEROID HORMONE; TESTOSTERONE;

ANALGESIA; ANDROGEN BLOOD LEVEL; CENTRAL NERVOUS SYSTEM; ESTRIOL BLOOD LEVEL; ESTROGEN BLOOD LEVEL; ESTRONE BLOOD LEVEL; FEMALE; HUMAN; MALE; NOCICEPTION; PATHOPHYSIOLOGY; PROGESTERONE BLOOD LEVEL; PROTEIN EXPRESSION; REVIEW; SEX DIFFERENCE; TESTOSTERONE BLOOD LEVEL;

ANALGESIA; ANIMALS; FEMALE; GONADAL STEROID HORMONES; HUMANS; MALE; PAIN THRESHOLD; SEX CHARACTERISTICS; SEX FACTORS;

EID: 84855922713     PISSN: 00347094     EISSN: 1806907X     Source Type: Journal    
DOI: 10.1016/S0034-7094(11)70091-5     Document Type: Review

References (105)

1. Hurley R.W., Adams M.C.B. Sex, gender and pain: an overview of a complex field. Anesth Analg 2008, 107:309-317.
2. Greenspan J.D., Craft R.M., LeResche L., et al. Studying sex and gender differences in pain and analgesia: A consensus report. Pain 2007, 132:26-45.
3. Unruh A.M. Gender variations in clinical pain experience. Pain 1996, 65:123-167.
4. Riley J.L., Robinson M.E., Wise E.A., et al. Sex differences in the perception of noxious experimental stimuli: a meta-analysis. Pain 1998, 74:181-187.
5. Aloisi A.M., Ceccarelli I., Herdegen T. Gonadectomy and persistent pain differently affect hippocampal c-Fos expression in male and female rats. Neurosci Lett 2006, 281:29-32.
6. Turk D.C., Meichenbaum D.H., Berman W.H. Application of biofeedback for the regulation of pain: a critical review. Psychol Bull 1979, 86:1322-1338.
7. McEwen B.S. Permanence of brain sex differences and structural plasticity of the adult brain. Proc Natl Acad Sci USA 1999, 96:7128-7130.
8. Aloisi A.M., Ceccarelli I., Herdegen T. Gonadectomy and persistent pain differently affect hippocampal c-Fos expression in male and female rats. Neurosci Lett 2000, 281:29-32.
9. Tousignant-Laflamme Y., Marchand S. Excitatory and inhibitory pain mechanisms during the menstrual cycle in healthy women. Pain 2009, 146:47-55.
10. Fillingim R.B., Gear R.W. Sex differences in opioid analgesia: clinical and experimental findings. Eur J Pain 2004, 8:413-425.
11. Gaumond I., Arsenault P., Marchand S. Specificity of female and male sex hormones on excitatory and inhibitory phases of formalin-induced nociceptive responses. Brain Res 2005, 1052:105-111.
12. Thompson A.D., Angelotti T., Nag S., et al. Sex-specific modulation of spinal nociception by alpha-adrenoceptors: differential regulation by estrogen and testosterone. Neuroscience 2008, 153:1268-1277.
13. Hagiwara H., Kimura F., Mitsushima D., et al. Formalin-induced nociceptive behavior and c-Fos experssion in middle-aged female rats. Physiol Behav 2010, 100:101-104.
14. Berkley K.J Sex differences in pain. Behav Brain Sci 1997, 20:371-380.
15. Fillingim R.B., Gear R.W. Sex differences in opioid analgesia: clinical and experimental findings. Eur J Pain 2004, 8:413-425.
16. Wolf F., Ross K., Anderson J., et al. Aspects of fibromyalgia in the general population: sex, pain threshold, and fibromyalgia symptoms. J Rheumatol 1995, 22:151-156.
17. Keogh E., McCraken L.M., Eccleston C. Do men and women differ in their response to interdisciplinary chronic pain management?. Pain 2005, 114:37-46.
18. Triadafilopoulos G., Finlayson M., Grellet C. Bowel dysfunction in postmenopausal women. Women Health 1998, 27:55-66.
19. Cervero F., Laird J.M. Role of ion channels in mechanisms controlling gastrointestinal pain pathways. Curr Opin Pharmacol 2003, 3:608-612.
20. Howard F.M. Chronic pelvic pain - Obstet Gynecol 2003, 101:594-611.
21. Vicent K. Chronic pelvic pain in women - Postgrad Med J 2009, 85:24-29.
22. Bingefors K., Isacson D. Epidemiology, co-morbidity, and impact on health-related quality of life of self-reported headache and musculoskeletal pain: a gender perspective. Eur J Pain 2004, 8:435-450.
23. Isacson D., Bingefors K. Epidemiology of analgesic use: a gender perspective. Eur J Anaesthesiol Suppl 2002, 26:5-15.
24. Brody S., Carlstrom K., Lagrelius A., et al. Serum sex hormone binding globulin (SHBG), testosterone/SHBG index, endometrial pathology and bone mineral density in postmenopausal women. Acta Obstet Gynecol Scand 1987, 66:357-360.
25. Katzenellenbogen B.S., Katzenellenbogen J.A. Estrogen receptor transcription and transactivation, estrogen receptor alpha and estrogen receptor β: regulation by selective estrogen receptor modulators and importance in breast cancer. Breast Cancer Res 2000, 2:335-344.
26. Vasudevan N., Kia H.K., Inoue S., et al. Isoform specificity for oestrogen receptor and thyroid hormone receptor genes and their interactions on the NR2D gene promoter. J Neuroendocrinol 2002, 14:836-842.
27. Bai Y., Giguere V. Isoform-selective interactions between estrogen receptors and steroid receptor coactivators promoted by estradiol and ErbB-2 signaling in living cells. Mol Endocrinol 2003, 17:589-599.
28. Arnold A.P., Breedlove S.M. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 1985, 19:469-498.
29. Micevych P., Sinchak K., Mills R.H., et al. The luteinizing hormone surge is preceded by an estrogen-induced increase of hypothalamic progesterone in ovariectomized and adrenalectomized rats. Neuroendocrinology 2003, 78:29-35.
30. Sinchak K., Mills R.H., Tao L., et al. Estrogen induces de novo progesterone synthesis in astrocytes. Dev Neurosci 2003, 25:343-348.
31. Amateu S.K., Alt J.J., Stamps C.L., et al. Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon. Endocrinology 2004, 145:2906-2917.
32. Hojo Y., Hattori T.A., Enami T., et al. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017 alpha and P450 aromatase localized in neurons. Proc Natl Acad Sci USA 2004, 101:865-870.
33. Kretz O., Fester L., Wehrenberg U., et al. Hippocampal synapses depend on hippocampal estrogen synthesis. J Neurosci 2004, 24:5913-5921.
34. Bennett H.L., Gustafsson J.A., Keast J.R. Estrogen receptor expression in lumbosacral dorsal root ganglion cells innervating the female rat urinary bladder. Auton Neurosci 2003, 105:90-100.
35. Evrard H.C. Estrogen synthesis in the spinal dorsal horn: a new central mechanism for the hormonal regulation of pain. Am J Physiol Regul Integr Comp Physiol 2006, 291:R291-R299.
36. Muller-Lissner S.A., Fumagalli I., Bardhan K.D., et al. Tagaserod, a 5HT(4) receptor partial agonist, relieves symptoms in irritable bowel syndrome patients with abdominal pain, bloating and constipation. Aliment Pharmacol Ther 2001, 15:1655-1666.
37. Simpson E.R. Sources of estrogen and their importance. J Steroid Biochem Mol Biol 2003, 86:225-230.
38. Foster T.C. Interaction of rapid signal transduction cascades and gene expression in mediating estrogen effects on memory over the life span. Front Neuroencocrinol 2005, 26:51-64.
39. Robichaud M., Debonnel D. Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J Neuroendocrinol 2005, 17:179-185.
40. Paul S.M., Purdy R.H. Neuroactive Steroids. FASEB J 1992, 6:2311-2322.
41. Rupprecht R., Holsboer F. Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci 1999, 22:410-416.
42. Rupprecht R., di Michele F., Hermann B., et al. Neuroactive steroids: molecular mechanisms of action and implications for neuropsychopharmacology. Brain Res Rev 2001, 37:59-67.
43. Teyler T.J., Vardaris R.M., Lewis D., et al. Gonadal steroids: effects on excitability of hippocampal pyramidal cells. Science 1980, 209:1017-1018.
44. Beyenburg S., Stoffel-Wagner B., Bauer J., et al. Neuroactive steroids and seizure susceptibility. Epilepsy Res 2001, 44:141-153.
45. Shibuya K., Takata N., Hojo Y., et al. Hippocampal cytochrome P450s synthesize brain neurosteroids which are paracrine neuromodulators of synaptic signal transduction. Biochim Biophys Acta 2003, 1619:301-316.
46. Mellon S.H. Neurosteroids: biochemistry, modes of action, and clinical relevance. J Clin Endocrinol Metab 1994, 78:1003-1008.
47. Balthazart J., Ball G.F. Fast regulation of steroid biosynthesis: a further piece in the neurosteroid puzzle. Trends Neurosci 2000, 23:57-58.
48. Lanlua P., Decorti F., Gangula P.R.R., et al. Female steroid hormones modulate receptors for nerve growth factor in rat dorsal root ganglia. Biol Reprod 2001, 64:331-338.
49. Rudick C.N., Woolley C.S. Estradiol induces a phasic c-fos response in the hippocampal CA1 and CA3 regions of adult female rats. Hippocampus 2000, 10:274-283.
50. Toran-Alleran C.D., Singh M., Sétáló G. Novel mechanisms of estrogen action in the brain: new players and an old story. Front Neuroendocrinol 1999, 20:97-121.
51. Foy M.R., Xu J., Xie X., et al. 17 beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J Neurophysiol 1999, 81:925-929.
52. McEwen B.S., Alves S.E. Estrogen actions in the central nervous system. Endocr Rev 1999, 20:279-307.
53. Silberstein S.D. Hormone related headache. Med Clin North Am 2001, 85:1017-1035.
54. Zuloaga D.G., Puts D.A., Jordan C.L., et al. The role of androgen receptors in the masculinization of brain and behavior: what we've learned from the testicular feminization mutation. Horm Behav 2008, 53:613-626.
55. Aloisi A.M., Affaitati G., Ceccarelli I., et al. Estradiol and testosterone differently affect visceral pain-related behavioural responses in male and female rats. Eur J Pain 2010, 14:602-607.
56. Affaitati G., Ceccarelli I., Fiorenzani P., et al. Sex differences in the analgesic effects of ICI 182,780 and flutamide on ureteral calculosis in rats. Horm Behav 2011, 59(1):9-13.
57. Sanoja R., Cervero F. Estrogen-dependent changes in visceral afferent sensitivity. Auton Neurosci 2010, 153:84-89.
58. Sanoja R., Cervero F. Estrogen-dependent abdominal hyperalgesia induced by ovariectomy in adult mice: a model of functional abdominal pain. Pain 2005, 118:243-252.
59. Sanoja R., Cervero F. Estrogen modulation of ovariectomy-induced hyperalgesia in adult mice. Eur J Pain 2008, 12:573-581.
60. Dong D.X., Mann M.K., Kumar U. Sex-related differences in MNDA-evoked rat masseter muscle afferente discharge result from estrogenmediated modulation of peripheral NMDA receptor activity. Neuroscience 2007, 146:822-832.
61. Tang B., Ji Y., Traub R.J. Estrogen alters spinal NMDA receptor activity via a PKA signaling pathway in a visceral pain model in the rat. Pain 2008, 137:540-549.
62. Dina O.A., Gear E.W., Messing R.O. Severity of alcohol-induced painful peripheral neuropathy in female rats: role of estrogen and protein kinase (A and Ce). Neuroscience 2007, 145:350-356.
63. Ceccarelli I., Fiorezani P., Massafra C., et al. Repeated nociceptive stimulation induces different behavioral and neuronal responses in intact and gonadectomized female rats. Brain Res 2006, 1106:142-149.
64. Mannino C.A., South S.M., Quinones-Jenab V., et al. Estradiol replacement in ovariectomized rats is antihyperalgesic in formalin test. J Pain 2007, 8:334-342.
65. Nag S., Mokha S.S. Testosterone is essential for alpha-2-adrenoceptor-induced antinociception in the trigeminal region of the male rat. Neurosci Lett 2009, 467:48-52.
66. Wu W., Bi Y., Kou X., et al. 17-beta Estradiol enhaced allodynia if inflamatory temporomandibular joint through upregulation of hippocampal TRPV1 in ovariectomized rats. J Neurosci 2010, 26:8710-8719.
67. Stoffel E.C., Ulibarri C.M., Folk J.E. Gonadal hormone modulation of mu, kappa and delta opioid antinociception in male and female rats. J Pain 2005, 6:261-274.
68. Mitrovic I., Mitrovic M.M., Bader S., et al. Contribuition of GIRK-2 mediated postsynaptic signaling to opiate and alpha -2 adrenergic analgesia and analgesic sex differences. Proc Natl Acad Sci USA 2003, 100:271-276.
69. Claiborne J., Nag S., Mokha S.S. Activation of opioid receptor like-1 receptor in the spinal cord produces sex-specific antinociception in the rat: estrogen attenuates antinociception in the female, whereas testosterone is required for the expression of antinociception in the male. J Neurosci 2006, 26:13048-13053.
70. Li L., Fan X., Warner M., et al. Ablation of estrogen receptor alpha or beta eliminates sex differences in mechanical pain threshold in norma and inflamed mice. Pain 2009, 143:37-40.
71. Zubieta J.K., Smith Y.R., Bueller J.A., et al. Mu-opioid receptor-mediated antinociceptive responses differ in men and women. J Neurosci 2002, 22:5100-5107.
72. Zubieta J.K., Dannals R.F., Frost J.J. Gender and age influences on human brain mu-opioid receptor binding measured by PET. Am J Psychiatry 1999, 156:842-848.
73. Wiesenfeld-Hallin Z. Sex differences in pain perception. Gender Med 2005, 2:137-145.
74. Cicero T.J., Nock B., OConnor L., et al. Role of steroids in sex differences in morphine-induced analgesia: activational and organizational effects. J Pharmacol Exp Ther 2002, 300:695-701.
75. Krzanowska E.K., Ogawa S., Pfaf D.W., et al. Reversal of sex differences in morphine analgesia elicited from the ventrolateral periaqueductal gray in rats by neonatal hormone manipulations. Brain Res 2002, 929:1-9.
76. Cook C.D., Barret A.C., Roach A.L., et al. Sex-related differences in the antinociceptive effects of opioids: importance of rat genotype, nociceptive stimulus intensity, and efficacy at the mu opioid receptor. Psychopharmacology 2000, 150:430-442.
77. Gear R.W., Miaskowiski C., Gordon N.C., et al. The kappa opioid nalbuphine produces gender- and dose-dependent analgesia and antianalgesia in patients with postoperative pain. Pain 1999, 83:339-345.
78. Dahan A., Kest B., Waxman A.R., et al. Sex-specific responses to opiates: animal and human studies. Anesth Analg 2008, 107:83-95.
79. Kepler K.L., Standifer K.M., Paul D., et al. Gender effects and central opioid analgesia. Pain 1991, 45:87-94.
80. Wise E.A., Price D.D., Myers C.D., et al. Gender role expectations of pain: relationship to experimental pain perception. Pain 2002, 96:335-342.
81. Jensen I.B., Bergstrom G., Ljungquist T., Bodin L., Nygren A.L. A randomized controlled component analysis of a behavioural medicine rehabilitation program for chronic spinal pain: are the effects dependent on gender?. Pain 2001, 91:65-78.
82. Krogstad B.S., Jokstad A., Dahl B.L., et al. The reporting of pain, somatic complaints, and anxiety in a group of patients with TMD before and 2 years after treatment: sex differences. J Orofac Pain 1996, 10:263-269.
83. Hansen F.R., Bendix T., Skov P., et al. Intensive, dynamic back-muscle exercises, conventional physiotherapy, or placebo-control treatment of low-back-pain-a randomized, observer-blind trial. Spine 1993, 18:98-106.
84. Klatzkin R.R., Mechlin B., Girdler S.S. Menstrual cycle does not influence gender differences in experimental pain sensitivity. Eur J Pain 2010, 14:77-82.
85. Okifuji A., Turk D.C. Sex hormones and pain in regularly menstruating women with fibromyalgia syndrome. J Pain 2006, 11:851-859.
86. Fillingim R.B., Maxiner W. Gender differences in the responses to noxious stimuli. Pain Forum 1995, 4:221-308.
87. Chesterton L.S., Barlas P., Foster N.E., et al. Gender differences in pressure pain threshold in healthy humans. Pain 2003, 101:259-266.
88. Kowalczyk W.J., Sullivan M.A., Evans S.M., et al. Sex differences and hormonal influences on response to mechanical pressure pain in humans. J Pain 2010, 11:330-342.
89. Nisenblat V., Engel-Yeger B., Ohel G., et al. The association between supra-physiological levels of estradiol and response patterns to experimental pain. Eur J Pain 2010, 14:840-846.
90. LeBars D., Dickenson A.H., Besson J.M. Diffuse noxious inhibitory controls (DNIC) Efffects on dorsal horn convergent neurons in the rat. Pain 1979, 6:283-304.
91. Edwards R.R. Individual differences in endogenous pain modulation as a risk factor for chronic pain. Neurology 2005, 65:437-443.
92. Tousignant-Laflamme Y., Pagé S., Goffaux P., et al. An experimental model to measure excitatory and inhibitory pain mechanisms in humans. Brain Res 2008, 1230:73-79.
93. France C.R., Suchowiecki S. A comparison of diffuse noxious inhibitory controls in men and women. Pain 1999, 81:77-84.
94. Baad-Hansen L., Pousen H.F., Jensen H.M., et al. Lack of sex differences in modulation of experimental intraoral pain by diffuse noxious inhibitory controls (DNIC). Pain 2005, 116:359-365.
95. Serrao M., Rossi P., Sandrini G., et al. Effects of diffuse noxious inhibitory controls on temporal summation of the RIII reflex in humans. Pain 2004, 112:353-360.
96. Ge H.Y., Madeleine P., Arendt-Nielsen L. Sex differences in temporal characteristics of descending inhibitory control: an evaluation using repeated bilateral experimental induction of muscle pain. Pain 2004, 110:72-78.
97. Ge H.Y., Madeleine P., Arendt-Nielsen L. Gender differences in pain modulation evoked by repeated injections of glutamate into the human trapezius muscle. Pain 2005, 113:134-140.
98. Staud R., Robinson M.E., Vierck C.J., et al. Diffuse noxious inhibitory controls (DNIC) attenuate temporal summation of second pain in normal males but not in normal females or fibromyalgia patients. Pain 2003, 101:167-174.
99. Cepeda M.S., Carr D.B. Women experience more pain and require more morphine than men to achieve a similar degree of analgesia. Anesth Analg 2003, 97:1464-1468.
100. Miller P.L., Ernst A.A. Sex differences in analgesia: a randomized trial of mu versus k opioid agonists. South Med J 2004, 97:35-41.
101. Gear R.W., Miaskowisk C., Gordon N.C., et al. Kappa-opioids produce significantly greater analgesia in women than in men. Nat Med 1996, 2:1248-1250.
102. Gear R.W., Gordon N.C., Heller P.H., et al. Gender difference in analgesic response to the kappa-opioid pentazocine. Neurosci Lett 1996, 205:207-209.
103. Mogil J.S., Wilson S.G., Chesler E.J., et al. The melanocortin-1 receptor gene mediates female-specific mechanisms of analgesia in mice and humans. Proc Natl Acad Sci USA 2003, 100:4867-4872.
104. Loyd D.R., Murphy A.Z. The role of the periaqueductal gray in the modulation of pain in males and females: are the anatomy and physiology really that different?. Neural Plast 2009, 2009:462879.
105. Smith Y.R., Stohler C.S., Nichols T.E., et al. Pronociceptive and antinociceptive effects of estradiol through endogenous opioid neurotransmission in women. J Neurosci 2006, 26:5777-57785.