Sex differences in pain and analgesia: the role of gonadal hormones
Abstract
There is now strong evidence for sex differences in pain and analgesia. These differences imply that gonadal steroid hormones such as estradiol and testosterone modulate sensitivity to pain and analgesia. The goal of this review is to present an overview of gonadal steroid modulation of pain and analgesia in animals and humans, and to describe mechanisms by which males' and females' biology may differentially predispose them to pain and to analgesic effects of drugs and stress. Evidence is presented to demonstrate that sex differences in pain and analgesia may be both quantitative and qualitative in nature. Current research suggests that sex‐specific management of clinical pain will be a reality in the not‐so‐distant future.
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Evidence suggests that estradiol modulates central neuronal activity in pain states.
“evidence suggests estradiol modulates central neuronal activity in pain states”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Craft et al., 2004
Cites
The Physiology of Reproduction
Legendre, M., & Jalabert, B. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-2-176_1 · Cited by 7,879 · see citing works
A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia
Hargreaves, K., Dubner, R. A., Brown, F. J., Flores, C., & Joris, J. L. (1988) · Pain · doi:10.1016/0304-3959(88)90026-7 · Cited by 5,155 · see citing works
Genetic Dissection of Complex Traits
Lander, E. S., & Schork, N. J. (1994) · Science · doi:10.1126/science.8091226 · Cited by 3,425 · see citing works
The Physiology of Reproduction
Blandau, R. J. (1988) · JAMA · doi:10.1001/jama.1988.03410200127050 · Cited by 3,000 · see citing works
Endogenous Pain Control Systems: Brainstem Spinal Pathways and Endorphin Circuitry
Basbaum, A. I., & Fields, H. L. (1984) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.07.030184.001521 · Cited by 2,687 · see citing works
PHOENIX, C. H., GOY, R. W., GERALL, A. A., & YOUNG, W. C. (1959) · Endocrinology · doi:10.1210/endo-65-3-369 · Cited by 1,934 · see citing works
Gender variations in clinical pain experience
Unruh, A. M. (1996) · Pain · doi:10.1016/0304-3959(95)00214-6 · Cited by 1,550 · see citing works
Young, W. C., & Allen, E. (1961) · Williams & Wilkins eBooks · doi:10.5962/bhl.title.7323 · Cited by 1,171 · see citing works
Berkley, K. J. (1997) · Behavioral and Brain Sciences · doi:10.1017/s0140525x97221485 · Cited by 1,125 · see citing works
Valverde, P., Healy, E., Jackson, I., Rees, J. L., & Thody, A. J. (1995) · Nature Genetics · doi:10.1038/ng1195-328 · Cited by 999 · see citing works
The physiology of male sexual behavior
Meisel, R. (1994) · Medical Entomology and Zoology · Cited by 988 · see citing works
Organizational and activational effects of sex steroids on brain and behavior: A reanalysis
Arnold, A. P. (1985) · Hormones and Behavior · doi:10.1016/0018-506x(85)90042-x · Cited by 805 · see citing works
Young, W. C., Corner, G. W., & Albert, A. (1933) · Archives of Internal Medicine · doi:10.1001/archinte.1933.00150240174015 · Cited by 671 · see citing works
A meta-analytic review of pain perception across the menstrual cycle
Riley, J. L., Robinson, M. E., Wise, E. A., & Price, D. D. (1999) · Pain · doi:10.1016/s0304-3959(98)00258-9 · Cited by 581 · see citing works
Sex-related hormonal influences on pain and analgesic responses
Fillingim, R. B., & Ness, T. J. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00017-8 · Cited by 554 · see citing works
Intrinsic Mechanisms of Pain Inhibition: Activation by Stress
Terman, G. W., Shavit, Y., Lewis, J. W., Cannon, J. T., & Liebeskind, J. C. (1984) · Science · doi:10.1126/science.6505691 · Cited by 530 · see citing works
The melanocortin-1 receptor gene mediates female-specific mechanisms of analgesia in mice and humans
Mogil, J. S., Wilson, S. G., Chesler, E. J., Rankin, A. L., Nemmani, K. V. S., Lariviere, W. R., Groce, M. K., Wallace, M. R., Kaplan, L., Staud, R. M., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0730053100 · Cited by 528 · see citing works
Self-citationEndocrine consequences of long-term intrathecal administration of opioids
Abs, R., Verhelst, J., Maeyaert, J., Van Buyten, J.-P., Opsomer, F., Adriaensen, H., Verlooy, J., Van Havenbergh, T., Smet, M., & Van Acker, K. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.6.6615 · Cited by 491 · see citing works
Kappa–opioids produce significantly greater analgesia in women than in men
Gear, R. W., Miaskowski, C. A., Gordon, N. C., Paul, S. M., Heller, P. H., & Levine, J. D. (1996) · Nature Medicine · doi:10.1038/nm1196-1248 · Cited by 457 · see citing works
Lewandowski, S. A., Kalita, K. B., & Kaczmarek, L. (2002) · FEBS Letters · doi:10.1016/s0014-5793(02)03015-6 · Cited by 378 · see citing works
Neuroendocrinology of Reproduction
(1981) · Springer eBooks · doi:10.1007/978-1-4684-3875-8 · Cited by 347 · see citing works
Sex differences in thermal nociception and morphine antinociception in rodents depend on genotype
Mogil, J. S., Chesler, E. J., Wilson, S. G., Juraska, J. M., & Sternberg, W. F. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00015-4 · Cited by 346 · see citing works
Self-citationEndorphin-Mediated Increases in Pain Threshold During Pregnancy
Gintzler, A. R. (1980) · Science · doi:10.1126/science.7414330 · Cited by 341 · see citing works
Proceedings of the 7th World Congress on Pain
Korevaar, W. C. (1995) · Clinical Journal of Pain · doi:10.1097/00002508-199509000-00017 · Cited by 320 · see citing works
Sex Differences in Opioid Analgesia: “From Mouse to Man”
Craft, R. M. (2003) · Clinical Journal of Pain · doi:10.1097/00002508-200305000-00005 · Cited by 319 · see citing works
Self-citationAge‐dependent genetic effects on a secondary sexual trait in male Alpine ibex,Capra ibex
von Hardenberg, A., Bassano, B., Festa‐Bianchet, M., Luikart, G., Lanfranchi, P., & Coltman, D. W. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2006.03221.x · Cited by 315 · see citing works
Katzenellenbogen, B., & Katzenellenbogen, J. (2000) · Breast Cancer Research · doi:10.1186/bcr78 · Cited by 313 · see citing works
Gear, R. W., Miaskowski, C. A., Gordon, N. C., Paul, S. M., Heller, P. H., & Levine, J. D. (1999) · Pain · doi:10.1016/s0304-3959(99)00119-0 · Cited by 275 · see citing works
Mogil, J. S., Sternberg, W. F., Kest, B., Marek, P., & Liebeskind, J. C. (1993) · Pain · doi:10.1016/0304-3959(93)90050-y · Cited by 260 · see citing works
Self-citationNeural Mechanisms of Female Reproductive Behavior
Pfaff, D. W., & Modianos, D. T. (1985) · Springer eBooks · doi:10.1007/978-1-4684-4832-0_10 · Cited by 255 · see citing works
Fillingim, R. B. (2017) · Principles of Gender-Specific Medicine · doi:10.1016/b978-0-12-803506-1.00038-3 · Cited by 255 · see citing works
Kepler, K. L., Kest, B., Kiefel, J. M., Cooper, M. L., & Bodnar, R. J. (1989) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(89)90363-8 · Cited by 234 · see citing works
Gender difference in analgesic response to the kappa-opioid pentazocine
Gear, R. W., Gordon, N. C., Heller, P. H., Paul, S. M., Miaskowski, C. A., & Levine, J. D. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(96)12402-2 · Cited by 232 · see citing works
Eckersell, C. B., Popper, P., & Micevych, P. E. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-10-03967.1998 · Cited by 221 · see citing works
Stoffel, E. C., Ulibarri, C., & Craft, R. M. (2003) · Pain · doi:10.1016/s0304-3959(02)00457-8 · Cited by 201 · see citing works
Self-citationCharacteristics of sex behaviour in male rats following castration
Davidson, J. M. (1966) · Animal Behaviour · doi:10.1016/s0003-3472(66)80082-9 · Cited by 194 · see citing works
Effects of Ovarian Steroids on Vaginal Smears in the Rat
Monies, G. S., & Luque, E. H. (1988) · Cells Tissues Organs · doi:10.1159/000146639 · Cited by 185 · see citing works
Gender effects and central opioid analgesia
Kepler, K. L., Standifer, K. M., Paúl, D., Kest, B., Pasternak, G. W., & Bodnar, R. J. (1991) · Pain · doi:10.1016/0304-3959(91)90168-w · Cited by 184 · see citing works
Pfeiffer, A. F. H., & Herz, A. (1984) · Hormone and Metabolic Research · doi:10.1055/s-2007-1014801 · Cited by 161 · see citing works
Progesterone Blockade of Estrogen Activation of μ-Opioid Receptors Regulates Reproductive Behavior
Sinchak, K., & Micevych, P. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05723.2001 · Cited by 157 · see citing works
Cloning and Functional Characterization of a Family of Receptors for the Melanotropic Peptides
Cone, R. D., Mountjoy, K. G., Robbins, L. S., Nadeau, J. H., Johnson, K. R., Roselli-Rehfuss, L., & Mortrud, M. T. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb19694.x · Cited by 151 · see citing works
Cicero, T. J., Nock, B., O’Connor, L., & Meyer, E. R. (2002) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.300.2.695 · Cited by 150 · see citing works
Receptor Biology of the Melanocortins, a Family of Neuroimmunomodulatory Peptides
Tatro, J. B. (1997) · NeuroImmunoModulation · doi:10.1159/000097281 · Cited by 143 · see citing works
Feder, H. H. (1981) · Springer eBooks · doi:10.1007/978-1-4684-3875-8_10 · Cited by 138 · see citing works
Kaneko, M. A. N., Park, J. H., Cheng, Y., Hardin, P. E., & Hall, J. C. (2000) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(20000605)43:3 · Cited by 138 · see citing works
Expression of melanocortin 1 receptor in periaqueductal gray matter
Xia, Y., Wikberg, J. E. S., & Chhajlani, V. (1995) · Neuroreport · doi:10.1097/00001756-199511000-00022 · Cited by 137 · see citing works
Simerly, R. B., McCall, L. D., & Watson, S. J. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902760309 · Cited by 135 · see citing works
Sex differences in NMDA receptor mediated responses in rats
Ho¨nack, D., & ̈scher, W. L. (1993) · Brain Research · doi:10.1016/0006-8993(93)90287-w · Cited by 131 · see citing works
Gestational and ovarian sex steroid antinociception: synergy between spinal κ and δ opioid systems
Dawson-Basoa, M., & Gintzler, A. R. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00192-9 · Cited by 130 · see citing works
Interactions among aging, gender, and gonadectomy effects upon morphine antinociception in rats
Islam, A. K., Cooper, M. L., & Bodnar, R. J. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90042-e · Cited by 128 · see citing works
Sex Hormone Suppression by Intrathecal Opioids: A Prospective Study
Roberts, L. J., Finch, P. M., Pullan, P. T., Bhagat, C. I., & Price, L. M. (2002) · Clinical Journal of Pain · doi:10.1097/00002508-200205000-00002 · Cited by 128 · see citing works
Liu, N., & Gintzler, A. R. (2000) · Pain · doi:10.1016/s0304-3959(99)00278-x · Cited by 127 · see citing works
The estrous cycle and estrogen modulate stress-induced analgesia.
Ryan, S. M., & Maier, S. F. (1988) · Behavioral Neuroscience · doi:10.1037//0735-7044.102.3.371 · Cited by 124 · see citing works
Sex differences in drug- and non-drug-induced analgesia
Craft, R. M. (2003) · Life Sciences · doi:10.1016/s0024-3205(03)00178-4 · Cited by 118 · see citing works
Self-citationMogil, J. S., Richards, S. P., O’Toole, L. A., Helms, M. L., Mitchell, S. R., Kest, B., & Belknap, J. K. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-20-07995.1997 · Cited by 117 · see citing works
Self-citationEnhancement of morphine analgesia by the GABAB agonist baclofen
Gordon, N. C., Gear, R. W., Heller, P. H., Paul, S. M., Miaskowski, C. A., & Levine, J. D. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00335-g · Cited by 117 · see citing works
Kelly, M. J., Qiu, J., Wagner, E. J., & Rønnekleiv, O. K. (2002) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/s0960-0760(02)00249-2 · Cited by 116 · see citing works
Pfaus, J. G. (1992) · Hormones and Behavior · doi:10.1016/0018-506x(92)90014-m · Cited by 113 · see citing works
Effect of adrenal and sex hormones on opioid analgesia and opioid receptor regulation
Candido, J., Lutfy, K., Billings, B., Sierra, V., Duttaroy, A., Inturrisi, C. E., & Yoburn, B. C. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90015-8 · Cited by 109 · see citing works
The estrous cycle and estrogen modulate stress-induced analgesia.
Ryan, S. M., & Maier, S. F. (1988) · Behavioral Neuroscience · doi:10.1037/0735-7044.102.3.371 · Cited by 109 · see citing works
Estrogen and Progesterone Regulate Opiate Receptor Densities in Multiple Brain Regions*
Weiland, N. G., & Wise, P. M. (1990) · Endocrinology · doi:10.1210/endo-126-2-804 · Cited by 108 · see citing works
Krzanowska, E. K., & Bodnar, R. J. (1999) · Brain Research · doi:10.1016/s0006-8993(98)01364-x · Cited by 108 · see citing works
Vaginal lavage attenuates cocaine-stimulated activity and establishes place preference in rats
Walker, Q. D., Nelson, C. J., Smith, D., & Kuhn, C. M. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00883-3 · Cited by 104 · see citing works
Negus, S. S., & Mello, N. K. (1999) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)35015-3 · Cited by 102 · see citing works
μ-Opiate receptor binding in the medial preoptic area is cyclical and sexually dimorphic
Hammer, R. P. (1990) · Brain Research · doi:10.1016/0006-8993(90)90595-3 · Cited by 100 · see citing works
Aloisi, A. M., & Ceccarelli, I. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00445-5 · Cited by 98 · see citing works
Self-citationRatka, A., & Simpkins, J. W. (1991) · Hormones and Behavior · doi:10.1016/0018-506x(91)90052-j · Cited by 95 · see citing works
Tershner, S. A., Mitchell, J., & Fields, H. L. (2000) · Pain · doi:10.1016/s0304-3959(99)00257-2 · Cited by 93 · see citing works
Intrathecal Infusion Systems for Treatment of Chronic Low Back and Leg Pain of Noncancer Origin
Tutak, U., & Doleys, D. M. (1996) · Southern Medical Journal · doi:10.1097/00007611-199603000-00007 · Cited by 91 · see citing works
Marek, P., Mogil, J. S., Sternberg, W. F., Panocka, I., & Liebeskind, J. C. (1992) · Brain Research · doi:10.1016/0006-8993(92)90248-8 · Cited by 90 · see citing works
Self-citationKrzanowska, E. K., Ogawa, S., Pfaff, D. W., & Bodnar, R. J. (2002) · Brain Research · doi:10.1016/s0006-8993(01)03350-9 · Cited by 88 · see citing works
Opioid-induced suppression of rat testicular function.
Adams, M. L., Sewing, B. N., Forman, J. B., Meyer, E. R., & Cicero, T. J. (1993) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)38343-6 · Cited by 87 · see citing works
Ali, B. H., Sharif, S. I., & El‐Kadi, A. O. S. (1995) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.1995.tb02012.x · Cited by 84 · see citing works
Smith, Y. R., Zubieta, J., Carmen, M. G. D., Dannals, R. F., Ravert, H. T., Zacur, H. A., & Frost, J. J. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.12.5351 · Cited by 81 · see citing works
Bai, Y., & Giguère, V. (2003) · Molecular Endocrinology · doi:10.1210/me.2002-0351 · Cited by 79 · see citing works
Kavaliers, M., & Choleris, E. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00569-6 · Cited by 78 · see citing works
Kelly, M. J., Rønnekleiv, O. K., Ibrahim, N., Lagrange, A. H., & Wagner, E. J. (2002) · Steroids · doi:10.1016/s0039-128x(01)00181-7 · Cited by 77 · see citing works
Ovarian steroids and modulation of morphine-induced analgesia and catalepsy in female rats
Banerjee, P., Chatterjee, T. K., & Ghosh, J. J. (1983) · European Journal of Pharmacology · doi:10.1016/0014-2999(83)90319-9 · Cited by 76 · see citing works
Berglund, L. A., Derendorf, H., & SIMPKIN, J. W. (1988) · Endocrinology · doi:10.1210/endo-122-6-2718 · Cited by 73 · see citing works
Sternberg, W. F., Mogil, J. S., Kest, B., Page, G. G., Leong, Y. L., Yam, V., & Liebeskind, J. C. (1995) · Pain · doi:10.1016/0304-3959(95)00059-3 · Cited by 72 · see citing works
Self-citationPermanence of brain sex differences and structural plasticity of the adult brain
McEwen, B. S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.13.7128 · Cited by 71 · see citing works
Dessein, H. P., Shipton, A. E., Joffe, I., Hadebe, P. D., Stanwix, E. A., & der Merwe, A. B. V. (1999) · Pain · doi:10.1016/s0304-3959(99)00113-x · Cited by 69 · see citing works
Modulation of gender-specific effects upon swim analgesia in gonadectomized rats
Romero, M.-T., Kepler, K. L., Cooper, M. L., Komisaruk, B. R., & Bodnar, R. J. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90183-1 · Cited by 67 · see citing works
Vaginal Stimulation‐Produced Analgesia in Rats and Womena
Komisaruk, B. R., & Whipple, B. (1986) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1986.tb14616.x · Cited by 64 · see citing works
Ceccarelli, I., Scaramuzzino, A., Massafra, C., & Aloisi, A. M. (2003) · Pain · doi:10.1016/s0304-3959(02)00460-8 · Cited by 64 · see citing works
Self-citationDecline of sexual behavior in castrated male rats: Effects of female precopulatory behavior
Madlafousek, J., Hlinak, Z., & Beran, J. (1976) · Hormones and Behavior · doi:10.1016/0018-506x(76)90051-9 · Cited by 64 · see citing works
Differential naltrexone antagonism of hydromorphone and pentazocine effects in human volunteers.
Preston, K. L., & Bigelow, G. E. (1993) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)10212-7 · Cited by 62 · see citing works
Influence of gonadectomy on the antinociceptive effects of opioids in male and female rats
Terner, J. M., Barrett, A. C., Grossell, E., & Picker, M. J. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1143-x · Cited by 61 · see citing works
Alterations in Brain Opiate Receptor Mechanisms on Proestrous Afternoon
Berglund, A., & Simpkins, J. W. (2008) · Neuroendocrinology · doi:10.1159/000125040 · Cited by 61 · see citing works
Kavaliers, M., & Galea, L. A. M. (1995) · Pain · doi:10.1016/0304-3959(95)00063-1 · Cited by 61 · see citing works
Watkins, L. R., Wiertelak, E. P., Grisel, J. E., Silbert, L. H., & Maier, S. F. (1992) · Brain Research · doi:10.1016/0006-8993(92)91033-b · Cited by 58 · see citing works
Possible physiological role of adrenal and gonadal steroids in morphine analgesia.
Chatterjee, T. K., Das, S., Banerjee, P., & Ghosh, J. J. (1982) · European Journal of Pharmacology · doi:10.1016/0014-2999(82)90005-x · Cited by 53 · see citing works
Castration Affects Male Rat Brain Opiate Receptor Content
Hahn, E. F., & Fishman, J. (2008) · Neuroendocrinology · doi:10.1159/000124154 · Cited by 52 · see citing works
Akinci, M., & Johnston, G. A. R. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb07472.x · Cited by 50 · see citing works
Baker, L., & Ratka, A. (2002) · Pain · doi:10.1016/s0304-3959(01)00376-1 · Cited by 50 · see citing works
South, S. M., Wright, A. W. E., Lau, M., et al. (2001) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)29556-2 · Cited by 49 · see citing works
Sexual dimorphism in very low dose nalbuphine postoperative analgesia
Gear, R. W., Gordon, N. C., Miaskowski, C. A., Paul, S. M., Heller, P. H., & Levine, J. D. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(02)01438-6 · Cited by 48 · see citing works
Role of testosterone on pain threshold in rats.
Pednekar, J. R., & Vk, M. (1995) · PubMed · Cited by 45 · see citing works
Schwarz, S., & Pohl, P. (1994) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(94)90080-9 · Cited by 43 · see citing works
Central Neural States Relating Sex and Pain
Bodnar, R. J. (2002) · Johns Hopkins University Press eBooks · doi:10.56021/9780801868276 · Cited by 42 · see citing works
Pfeiffer, D. G., Pfeiffer, A. F. H., Almeida, O. F. X., & Herz, A. (1987) · Journal of Endocrinology · doi:10.1677/joe.0.1140469 · Cited by 42 · see citing works
Marek, P., Page, G. G., Ben‐Eliyahu, S., & Liebeskind, J. C. (1991) · Brain Research · doi:10.1016/0006-8993(91)90943-p · Cited by 42 · see citing works
Dessein, P., Shipton, E. A., Stanwix, A. E., & Joffe, B. I. (2000) · Pain · doi:10.1016/s0304-3959(00)00302-x · Cited by 41 · see citing works
Preproenkephalin mRNA levels are regulated by acute stress and estrogen stimulation
Sinchak, K., Eckersell, C. B., Quezada, V., Norell, A., & Micevych, P. E. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00261-9 · Cited by 39 · see citing works
A Modulatory Role for Luteinizing Hormone-Releasing Hormone in Nociceptive Responses of Female Rats
Ratka, A., & Simpkins, J. W. (1990) · Endocrinology · doi:10.1210/endo-127-2-667 · Cited by 36 · see citing works
Action of naloxone on gender-dependent analgesic and antianalgesic effects of nalbuphine in humans
Gear, R. W., Miaskowski, C. A., Gordon, N. C., Paul, S. M., Heller, P. H., & Levine, J. D. (2000) · Journal of Pain · doi:10.1016/s1526-5900(00)90097-x · Cited by 36 · see citing works
Liu, N., & Gintzler, A. R. (1999) · Pain · doi:10.1016/s0304-3959(99)00120-7 · Cited by 34 · see citing works
Genetic Studies of the Human Melanocortin‐1 Receptor
Rees, J. L., Birch‐Machin, M. A., Flanagan, N., Healy, E., Phillips, S. R., & Todd, C. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08670.x · Cited by 34 · see citing works
Kavaliers, M., Colwell, D. D., & Choleris, E. (1998) · Pain · doi:10.1016/s0304-3959(98)00092-x · Cited by 33 · see citing works
Negus, S. S., & Mello, N. K. (2001) · Psychopharmacology · doi:10.1007/s002130100912 · Cited by 33 · see citing works
Estrogen treatment to ovariectomized rats modifies morphine-induced behavior
Nomikos, G. G., Spyraki, C., Kazandjian, A., et al. (1987) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(87)90182-1 · Cited by 30 · see citing works
Smith, Y. R. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.12.4498 · Cited by 30 · see citing works
Evidence for Multiple Opioid Receptors in the Human Posterior Pituitary
Jordan, D. C., Tafani, J. A. M., Ries, C., et al. (1996) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1996.53210.x · Cited by 29 · see citing works
René, F., Muller, A., Jover, E., Kieffer, B. L., Koch, B., & Loeffler, J. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00199.x · Cited by 26 · see citing works
Effects of ovarian hormones on brain opioid binding sites in castrated female rats
Dondi, D., Limonta, P., Maggi, R., et al. (1992) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1992.263.3.e507 · Cited by 26 · see citing works
Brody, S., Carlström, K., Lagrelius, A., et al. (1987) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016348709103653 · Cited by 24 · see citing works
Maggi, R., Limonta, P., Dondi, D., et al. (1991) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(91)90174-4 · Cited by 23 · see citing works
Pentazocine-induced biphasic analgesia in mice
Suzuki, T., Narita, M., Misawa, M., et al. (1991) · Life Sciences · doi:10.1016/0024-3205(91)90238-7 · Cited by 22 · see citing works
Holtzman, D. A., Brooks, P. J., Pfaff, D. W., et al. (1997) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1997.00658.x · Cited by 21 · see citing works
Vasudevan, N., Kia, H. K., Inoue, S., Muramatsu, M., & Pfaff, D. W. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2002.00853.x · Cited by 21 · see citing works
Sex differences and endocrine regulation of morphine oxidation in rat liver
Blanck, A., Hansson, T., Näslund, B., et al. (1990) · Biochemical Pharmacology · doi:10.1016/0006-2952(90)90132-5 · Cited by 20 · see citing works
Levine, J. D., & Taiwo, Y. O. (1989) · Brain Research · doi:10.1016/0006-8993(89)90949-9 · Cited by 16 · see citing works
Mogil, J. S., Sternberg, W. F., Kest, B., et al. (1993) · Cited by 15 · see citing works
Self-citationCarter, A., & Soliman, M. R. I. (1997) · Life Sciences · doi:10.1016/s0024-3205(97)01056-4 · Cited by 14 · see citing works
Influence of testosterone on morphine analgesia in albino rats.
Ss, R., & Aq, S. (1986) · PubMed · Cited by 14 · see citing works
Sternberg, W. F., Mogil, J. S., Pilati, M. L., et al. (1994) · PubMed · Cited by 10 · see citing works
Self-citationKumru, S., Şimşek, M., Yılmaz, B., Sapmaz, E., Kutlu, S., Sandal, S., & Canpolat, S. (2001) · Physiological Research · doi:10.33549/physiolres.930062 · Cited by 8 · see citing works
Wong, C. (1988) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.1988.tb01021.x · Cited by 6 · see citing works
Effects of diabetes on the antinociceptive effect of (+/-)pentazocine in mice.
Kamei, J., Iwamoto, Y., Misawa, M., et al. (1994) · PubMed · Cited by 5 · see citing works
Interaction of morphine and steroid hormones in the postirradiation disease in rats.
Ratka, A. (1984) · PubMed · Cited by 4 · see citing works
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Straub, R. H. (2007) · Endocrine Reviews · doi:10.1210/er.2007-0001 · Cited by 1,950 · see citing works
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Self-citationRacine, M., Tousignant-Laflamme, Y., Kloda, L. A., Dion, D., Dupuis, G., & Choinière, M. (2012) · Pain · doi:10.1016/j.pain.2011.11.025 · Cited by 691 · see citing works
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Genazzani, A. R., Pluchino, N., Luisi, S., & Luisi, M. (2007) · Human Reproduction Update · doi:10.1093/humupd/dml042 · Cited by 237 · see citing works
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- Authors
- Craft, R. M., Mogil, J. S., & Aloisi, A. M.
- Affiliations
- Washington State University (US)
- McGill University (CA)
- University of Siena (IT)
- Corresponding author
- Craft, Rebecca M.
- Venue
- European Journal of Pain
- Publisher
- Wiley
- Published
- 2004-10
- Volume
- 8
- Issue
- 5
- Pages
- 397-411
- ISSN
- 1090-3801 (ISSN-L)
- 1532-2149
- OpenAlex
- W2073162601
- Cited by
- 570
- References
- 130
- Citations by year
- 2026: 14 · 2025: 25 · 2024: 31 · 2023: 31 · 2022: 18 · 2021: 26 · 2020: 20 · 2019: 24 · 2018: 22 · 2017: 22 · 2016: 28 · 2015: 18 · 2014: 16 · 2013: 30 · 2012: 36
- FWCI
- 3.10
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Pain (publishedVersion)
- PubMed (publishedVersion)
- Use Siena air (University of Siena) (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Pain Mechanisms and Treatments
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Sex and Gender in Healthcare
- Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Opioid Use
- Keywords
- sex differences in pain, analgesia, sex steroids, estradiol, testosterone, pain sensitivity, stress
- MeSH terms
- Analgesics, Animals, Drug Resistance, Female, Humans, Male, Neural Pathways, Pain, Receptors, Opioid, Sex Characteristics, Gonadal Steroid Hormones, Stress, Physiological, Opioid Peptides
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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