Do sex hormones influence emotional modulation of pain and nociception in healthy women?

Biological Psychology

Volumn 94, Issue 3, 2013, Pages 534-544

  Rhudy, Jamie L ^a   Bartley, Emily J ^a   Palit, Shreela ^a   Kerr, Kara L ^a   Kuhn, Bethany L ^a   Martin, Satin L ^a   DelVentura, Jennifer L ^a   Terry, Ellen L ^a  

^a UNIVERSITY OF TULSA   (United States)

Author keywords

Affect; Descending modulation; Menstrual cycle; Nociceptive flexion reflex; Pain; Psychophysiology; Sex hormones

Indexed keywords

ESTRADIOL; PROGESTERONE; SEX HORMONE; TESTOSTERONE;

ADULT; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; EMOTION; FEMALE; FLEXOR REFLEX; FOLLICULAR PHASE; HEALTH STATUS; HUMAN; HUMAN EXPERIMENT; LUTEAL PHASE; MENSTRUAL CYCLE; NOCICEPTION; NORMAL HUMAN; OVULATION; PAIN; PRIORITY JOURNAL; RISK FACTOR; SALIVA LEVEL; WOMEN'S HEALTH;

AFFECT; DESCENDING MODULATION; MENSTRUAL CYCLE; NOCICEPTIVE FLEXION REFLEX; PAIN; PSYCHOPHYSIOLOGY; SEX HORMONES;

ADULT; ELECTRIC STIMULATION; EMOTIONS; ESTRADIOL; FEMALE; HUMANS; MENSTRUAL CYCLE; NOCICEPTION; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PROGESTERONE; SALIVA; TESTOSTERONE;

EID: 84887010314     PISSN: 03010511     EISSN: 18736246     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2013.10.003     Document Type: Article

References (76)

1. Asso D. Levels of arousal in the premenstrual phase. British Journal of Social and Clinical Psychology 1978, 17(1):47-55. 10.1111/j.2044-8260.1978.tb00896.x.
2. Bartley E.J., Rhudy J.L. Comparing pain sensitivity and the nociceptive flexion reflex threshold across the mid-follicular and late-luteal menstrual phases in healthy women. Clinical Journal of Pain 2013, 29(2):154-161.
3. Bolles R.C., Fanselow M.S. A perceptual-defensive-recuperative model of fear and pain. Behavioral & Brain Sciences 1980, 3(2):291-323.
4. Bradley M.M., Codispoti M., Cuthbert B.N., Lang P.J. Emotion and motivation I: Defensive and appetitive reactions in picture processing. Emotion 2001, 1(3):276-298.
5. Bradley M.M., Lang P.J. Measuring emotion: The Self-Assessment Manikin and the semantic differential. Journal of Behavior Therapy & Experimental Psychiatry 1994, 25(1):49-59.
6. Cahill L. Why sex matters for neuroscience. Nature Reviews Neuroscience 2006, 7(6):477.
7. Chan C.W., Dallaire M. Subjective pain sensation is linearly correlated with the flexion reflex in man. Brain Research 1989, 479(1):145-150.
8. Childs E., Van Dam N.T., Wit H.d. Effects of acute progesterone administration upon responses to acute psychosocial stress in men. Experimental and Clinical Psychopharmacology 2010, 18(1):78-86. 10.1037/a0018060.
9. Conway C.A., Jones B.C., DeBruine L.M., Welling L.L.M., Smith M.J.L., Perrett D.I., et al. Salience of emotional displays of danger and contagion in faces is enhanced when progesterone levels are raised. Hormones and Behavior 2007, 51(2):202-206. 10.1016/j.yhbeh.2006.10.002.
10. Craft R.M. Modulation of pain by estrogens. Pain 2007, 132(Suppl. 1):S3-S12.
11. DelVentura J.L., Terry E.L., Bartley E.J., Kerr K.L., Rhudy J.L. Emotional modulation of pain is disrupted in persons with insomnia. Program No. 703.11. Neuroscience Meeting Planner 2011, Washington, DC, Society for Neuroscience, Online.
12. DelVentura J.L., Terry E.L., Bartley E.J., Rhudy J.L. Emotional modulation of pain and spinal nociception in persons with severe insomnia symptoms. Annals of Behavioral Medicine 2013, 10.1007/s12160-013-9551-1.
13. Edwards R.R. Individual differences in endogenous pain modulation as a risk factor for chronic pain. Neurology 2005, 65(3):437-443.
14. Fields H.L., Basbaum A.I., Heinricher M.M. Central nervous system mechanisms of pain modulation. Textbook of pain 2006, 125-143. Elsevier/Churchill Livingstone, Philadelphia. 5th ed. S.B. McMahon, M. Koltzenburg (Eds.).
15. Fillingim R.B. Sex, gender, and pain 2000, IASP Press, Seattle, WA, US.
16. Fillingim R.B., Maixner W., Girdler S.S., Light K.C., Harris M.B., Sheps D.S., et al. Ischemic but not thermal pain sensitivity varies across the menstrual cycle. Psychosomatic Medicine 1997, 59(5):512-520.
17. First M.B., Spitzer R.L., Gibbons M., Williams J.B.W. Structured Clinical Interview for DSM-IV Axis I Disorders 2002, Biometrics Research Department, New York State Psychiatric Institute, New York, NY.
18. Foo H., Mason P. Analgesia accompanying food consumption requires ingestion of hedonic foods. Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2009, 29(41):13053-13062. 10.1523/jneurosci.3514-09.2009.
19. France C.R., France J.L., al'Absi M., Ring C., McIntyre D. Catastrophizing is related to pain ratings, but not nociceptive flexion reflex threshold. Pain 2002, 99(3):459-463.
20. France C.R., Suchowiecki S. Assessing supraspinal modulation of pain perception in individuals at risk for hypertension. Psychophysiology 2001, 38(1):107-113.
21. Gandara B., LeResche L., Mancl L. Patterns of salivary estradiol and progesterone across the menstrual cycle. New York Academy of Sciences 2007, 1098:446-450.
22. Gann P.H., Giovanazzi S., Van Horn L., Branning A., Chatterton R.T. Saliva as a medium for investigating intra- and interindividual differences in sex hormone levels in premenopausal women. Cancer Epidemiology, Biomarkers & Prevention: A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology 2001, 10(1):59-64.
23. Gupta A., Silman A.J., Ray D., Morriss R., Dickens C., MacFarlane G.J., et al. The role of psychosocial factors in predicting the onset of chronic widespread pain: Results from a prospective population-based study. Rheumatology (Oxford, England) 2007, 46(4):666-671.
24. Hox J.J. Multilevel analysis: Techniques and applications 2010, Lawrence Erlbaum Associates, Mahwah, NJ. 2nd ed.
25. Klatzkin R.R., Mechlin B., Girdler S.S. Menstrual cycle phase does not influence gender differences in experimental pain sensitivity. European Journal of Pain 2010, 14(1):77-82. 10.1016/j.ejpain.2009.01.002.
26. Komisaruk B.R., Whipple B. How does vaginal stimulation produce pleasure, pain and analgesia?. Sex, gender and pain, progress in pain research and management 2000, Vol. 17:109-134. IASP Press, Washington DC, USA.
27. Kroenke K., Wu J., Bair M.J., Krebs E.E., Damush T.M., Tu W. Reciprocal relationship between pain and depression: A 12-month longitudinal analysis in primary care. Journal of Pain 2011, 12(9):964-973.
28. Lang P.J., Bradley M.M., Cuthbert B.N. International affective picture system (IAPS): Instruction manual and affective ratings. Technical Report A-4 1999, The Center for Research in Psychophysiology, University of Florida.
29. Lang P.J., Greenwald M.K., Bradley M.M., Hamm A.O. Looking at pictures: Affective, facial, visceral, and behavioral reactions. Psychophysiology 1993, 30(3):261-273.
30. Lautenbacher S., Rollman G.B. Possible deficiencies of pain modulation in fibromyalgia. Clinical Journal of Pain 1997, 13(3):189.
31. LeResche L., Mancl L., Sherman J.J., Gandara B., Dworkin S.F. Changes in temporomandibular pain and other symptoms across the menstrual cycle. Pain 2003, 106(3):253.
32. Little B.C., Zahn T.P. Changes in mood and autonomic functioning during the menstrual cycle. Psychophysiology 1974, 11(5):579-590. 10.1111/j.1469-8986.1974.tb01118.x.
33. Lu Y., Bentley G.R., Gann P.H., Hodges K.R., Chatterton R.T. Salivary estradiol and progesterone levels in conception and nonconception cycles in women: Evaluation of a new assay for salivary estradiol. Fertility and Sterility 1999, 71(5):863-868.
34. Meriggiola M.C., Nanni M., Bachiocco V., Vodo S., Aloisi A.M. Menopause affects pain depending on pain type and characteristics. Menopause (New York, N.Y.) 2012, 19(5):517-523. 10.1097/gme.0b013e318240fe3d.
35. Millan M.J. Descending control of pain. Progress in Neurobiology 2002, 66(6):355-474.
36. Okifuji A., Turk D.C. Sex hormones and pain in regularly menstruating women with fibromyalgia syndrome. Journal of Pain: Official Journal of the American Pain Society 2006, 7(11):851.
37. Pielsticker A., Haag G., Zaudig M., Lautenbacher S. Impairment of pain inhibition in chronic tension-type headache. Pain 2005, 118(1):215-223.
38. Reid R.L. Premenstrual syndrome. Current problems in obstetrics, gynecology, & fertility 1985, 345-353. Year Book Medical Publishers, Chicago. J.M. Leventhal, J.J. Hoffman, L.G. Keith, P.J. Taylor (Eds.).
39. Rezaii T., Hirschberg A.L., Carlström K., Ernberg M. The influence of menstrual phases on pain modulation in healthy women. Journal of Pain 2012, 13(7):646-655. 10.1016/j.jpain.2012.04.002.
40. Rhudy J.L., Arnau R.C., Green B.A., France C.R. Taxometric analysis of biceps femoris EMG following electrocutaneous stimulation over the sural nerve: Determining the latent structure of the nociceptive flexion reflex (NFR). International Journal of Psychophysiology 2008, 69(1):18-26.
41. Rhudy J.L., Bartley E.J. The effect of the menstrual cycle on affective modulation of pain and nociception in healthy women. Pain 2010, 149:365-372.
42. Rhudy J.L., Bartley E.J., Williams A.E. Habituation, sensitization, and emotional valence modulation of pain responses. Pain 2010, 148(2):320-327.
43. Rhudy J.L., Bartley E.J., Williams A.E., McCabe K.M., Chandler M.C., Russell J.L., et al. Are there sex differences in affective modulation of spinal nociception and pain?. Journal of Pain 2010, 11:1429-1441.
44. Rhudy J.L., DelVentura J.L., Terry E.L., Bartley E.J., Olech E., Palit S., et al. Emotional modulation of pain and spinal nociception in fibromyalgia. Pain 2013, 154(7):1045-1056.
45. Rhudy J.L., France C.R. Defining the nociceptive flexion reflex (NFR) threshold in human participants: A comparison of different scoring criteria. Pain 2007, 128:244-253.
46. Rhudy J.L., France C.R., Bartley E.J., McCabe K.M., Williams A.E. Psychophysiological responses to pain: Further validation of the nociceptive flexion reflex (NFR) as a measure of nociception using multilevel modeling. Psychophysiology 2009, 46(5):939-948.
47. Rhudy J.L., Williams A.E. Gender differences in pain: Do emotions play a role?. Gender Medicine 2005, 2(4):208-226.
48. Rhudy J.L., Williams A.E., McCabe K., Nguyen M.A., Rambo P. Affective modulation of nociception at spinal and supraspinal levels. Psychophysiology 2005, 42:579-587.
49. Rhudy J.L., Williams A.E., McCabe K.M., Russell J.L., Maynard L.J. Emotional control of nociceptive reactions (ECON): Do affective valence and arousal play a role?. Pain 2008, 136(3):250-261.
50. Riedel W., Layka H., Neeck G. Secretory pattern of GH, TSH, thyroid hormones, ACTH, cortisol, FSH, and LH in patients with fibromyalgia syndrome following systemic injection of the relevant hypothalamic-releasing hormones. Zeitschrift fur Rheumatologie 1998, 57(Suppl. 2):81-87.
51. Riley J.L., Robinson M.E., Wise E.A., Myers C.D., Fillingim R.B. Sex differences in the perception of noxious experimental stimuli: A meta-analysis. Pain 1998, 74(2-3):181-187.
52. Riley J.L., Robinson M.E., Wise E.A., Price D.D. A meta-analytic review of pain perception across the menstrual cycle. Pain 1999, 81(3):225.
53. Ring C., van Zanten J.J.C.S.V., Kavussanu M. Effects of sex, phase of the menstrual cycle and gonadal hormones on pain in healthy humans. Biological Psychology 2009, 81(3):189-191. 10.1016/j.biopsycho.2009.04.004.
54. Rosenberg E.J. The relationship between hormonal changes and psychophysiological measures in women. Biological Psychology Bulletin 1980, 6(1):46-56.
55. Roy M., Piche M., Chen J.-I., Peretz I., Rainville P. Cerebral and spinal modulation of pain by emotions. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(49):20900-20905. 10.1073/pnas.0904706106.
56. Salimetrics Saliva collection and handling advice 2009, Salimetrics, LLC.
57. Sandrini G., Serrao M., Rossi P., Romaniello A., Cruccu G., Willer J.C. The lower limb flexion reflex in humans. Progress in Neurobiology 2005, 77(6):353-395.
58. Sherman J.J., LeResche L. Does experimental pain response vary across the menstrual cycle? A methodological review. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2006, 291(2):R245-R256.
59. Smith Y.R., Stohler C.S., Nichols T.E., Bueller J.A., Koeppe R.A., Zubieta J.-K. Pronociceptive and antinociceptive effects of estradiol through endogenous opioid neurotransmission in women. Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2006, 26(21):5777-5785.
60. Smith Y.R., Zubieta J.K., delCarmen M.G. Brain opioid receptor measurements by positron emission tomography in normal cycling women: Relationship to luteinizing hormone pulsatility and gonadal steroid hormones. Journal of Clinical Endocrinology and Metabolism 1998, 83:4498.
61. Soderberg K., Poromaa I.S., Nyberg S., Backstrom T., Nordh E. Psychophysically determined thresholds for thermal perception and pain perception in healthy women across the menstrual cycle. Clinical Journal of Pain 2006, 22(7):610.
62. SPSS Inc. Linear mixed-effects modeling in SPSS: An introduction to the MIXED procedure 2005, From. http://www.spss.ch/upload/1126184451_Linear%20Mixed%20Effects%20Modeling%20in%20SPSS.pdf.
63. Stening K., Eriksson O., Wahren L., Berg G., Hammar M., Blomqvist A. Pain sensations to the cold pressor test in normally menstruating women: Comparison with men and relation to menstrual phase and serum sex steroid levels. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 2007, 293(4):R1711-R1716.
64. Straneva P.A., Maixner W., Light K.C., Pedersen C.A., Costello N.L., Girdler S.S. Menstrual cycle, beta-endorphins, and pain sensitivity in premenstrual dysphoric disorder. Health Psychology 2002, 21(4):358.
65. Teepker M., Peters M., Vedder H., Schepelmann K., Lautenbacher S. Menstrual variation in experimental pain: Correlation with gonadal hormones. Neuropsychobiology 2010, 61(3):131-140. 10.1159/000279303.
66. Terry E.L., DelVentura J.L., Bartley E.J., Vincent A., Rhudy J.L. Emotional modulation of pain and spinal nociception in persons with major depressive disorder (MDD). Pain 2013, 10.1016/j.pain.2013.08.009.
67. Terry E.L., France C.R., Bartley E.J., DelVentura J.L., Kerr K.L., Vincent A.L., et al. Standardizing procedures to study sensitization of human spinal nociceptive processes: Comparing parameters for temporal summation of the nociceptive flexion reflex (TS-NFR). International Journal of Psychophysiology 2011, 81:263-274.
68. Tershner S.A., Mitchell J.M., Fields H.L. Brainstem pain modulating circuitry is sexually dimorphic with respect to mu and kappa opioid receptor function. Pain 2000, 85:153.
69. Tousignant-Laflamme Y., Marchand S. Excitatory and inhibitory pain mechanisms during the menstrual cycle in healthy women. Pain 2009, 146(1-2):47-55. 10.1016/j.pain.2009.06.018.
70. Unruh A.M. Gender variations in clinical pain experience. Pain 1996, 65:123-167.
71. Vincent K., Tracey I. Sex hormones and pain: The evidence from functional imaging. Current Pain and Headache Reports 2010, 14(5):396-403. 10.1007/s11916-010-0139-1.
72. Vitzthum V.J. The ecology and evolutionary endocrinology of reproduction in the human female. American Journal of Physical Anthropology 2009, 140(Suppl. 49):95-136. 10.1002/ajpa.21195.
73. Walters E.T. Injury related behavior and neural plasticity: An evolutionary perspective on sensitization, hyperalgesia, and analgesia. International Review of Neurobiology 1994, 36:325-426.
74. Yarnitsky D. Conditioned pain modulation (the diffuse noxious inhibitory control-like effect): Its relevance for acute and chronic pain states. Current Opinion in Anaesthesiology 2010, 23(5):611-615.
75. Yarnitsky D., Crispel Y., Eisenberg E., Granovsky Y., Ben-Nun A., Sprecher E., et al. Prediction of chronic post-operative pain: Pre-operative DNIC testing identifies patients at risk. Pain 2008, 138(1):22-28. 10.1016/j.pain.2007.10.033.
76. Zubieta J.-K., Smith Y.R., Bueller J.A., Xu Y., Kilbourn M.R., Jewett D.M., et al. Mu-opioid receptor-mediated antinociceptive responses differ in men and women. Journal of Neuroscience 2002, 22(12):5100-5107.