Neural and psychosocial contributions to sex differences in knee osteoarthritic pain

Biology of Sex Differences

Kathleen A Sluka¹  Karen J Berkley²  Mary I O’Connor²  Daniel P Nicolella²  Roger M Enoka²  Barbara D Boyan²  David A Hart²  Eileen Resnick²  C Kent Kwoh²  Laura L Tosi²  Richard D Coutts²  Wendy M Kohrt² 

[1] Physical Therapy and Rehabilitation Science, 1–252 Medical Education Building, University of Iowa, 52242-1190, Iowa City, IA, USA

[2] Isis Research Network on Musculoskeletal Health, Iowa City, USA

关键词: Catastrophizing;    Psychosocial;    Central sensitization;    Nociceptor;    Gender;    Sex differences;    Pain;    Osteoarthritis;   

Others  :  793375
DOI  :  10.1186/2042-6410-3-26

 received in 2012-07-12, accepted in 2012-12-10,  发布年份 2012

【 摘 要 】

People with osteoarthritis (OA) can have significant pain that interferes with function and quality of life. Women with knee OA have greater pain and greater reductions in function and quality of life than men. In many cases, OA pain is directly related to sensitization and activation of nociceptors in the injured joint and correlates with the degree of joint effusion and synovial thickening. In some patients, however, the pain does not match the degree of injury and continues after removal of the nociceptors with a total joint replacement. Growth of new nociceptors, activation of nociceptors in the subchondral bone exposed after cartilage degradation, and nociceptors innervating synovium sensitized by inflammatory mediators could all augment the peripheral input to the central nervous system and result in pain. Enhanced central excitability and reduced central inhibition could lead to prolonged and enhanced pain that does not directly match the degree of injury. Psychosocial variables can influence pain and contribute to pain variability. This review explores the neural and psychosocial factors that contribute to knee OA pain with an emphasis on differences between the sexes and gaps in knowledge.

【 授权许可】

   
2012 Sluka et al; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]O'Connor MI: Implant survival, knee function, and pain relief after TKA. Are there differences between men and women? Clin Orthop Relat Res 2011, 469:1846-1851.
• [2]Singh JA, Gabriel S, Lewallen D: The impact of gender, age, and preoperative pain severity on pain after TKA. Clin Orthop Relat Res 2008, 466:2717-2723.
• [3]Beattie KA, Boulos P, Pui M, O'Neill J, Inglis D, Webber CE, Adachi JD: Abnormalities identified in the knees of asymptomatic volunteers using peripheral magnetic resonance imaging. Osteoarthritis Cartilage 2005, 13:181-186.
• [4]Lethbridge-Cejku M, Scott WW Jr, Reichle R, Ettinger WH, Zonderman A, Costa P, Plato CC, Tobin JD, Hochberg MC: Association of radiographic features of osteoarthritis of the knee with knee pain: data from the Baltimore Longitudinal Study of Aging. Arthritis Care Res 1995, 8:182-188.
• [5]Arendt-Nielsen L, Nie H, Laursen MB, Laursen BS, Madeleine P, Simonsen OH, Graven-Nielsen T: Sensitization in patients with painful knee osteoarthritis. Pain 2010, 149:573-581.
• [6]Stehling C, Liebl H, Krug R, Lane NE, Nevitt MC, Lynch J, McCulloch CE, Link TM: Patellar cartilage: T2 values and morphologic abnormalities at 3.0-T MR imaging in relation to physical activity in asymptomatic subjects from the osteoarthritis initiative. Radiology 2010, 254:509-520.
• [7]Stratton P, Berkley KJ: Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications. Hum Reprod Update 2011, 17:327-346.
• [8]Fei AI, Yu C, Zhang W, Morelli JN, Xiaoming L: MR imaging of knee osteoarthritis and correlation of findings with reported patient pain. J Huazhong Univ Sci Technol 2010, 30:248-254.
• [9]Hill CL, Gale DG, Chaisson CE, Skinner K, Kazis L, Gale ME, Felson DT: Knee effusions, popliteal cysts, and synovial thickening: association with knee pain in osteoarthritis. J Rheumatol 2001, 28:1330-1337.
• [10]Puolakka PA, Rorarius MG, Roviola M, Puolakka TJ, Nordhausen K, Lindgren L: Persistent pain following knee arthroplasty. Eur J Anaesthesiol 2010, 27:455-460.
• [11]Brander VA, Stulberg SD, Adams AD, Harden RN, Bruehl S, Stanos SP, Houle T: Predicting total knee replacement pain: a prospective, observational study. Clin Orthop Relat Res 2003, 416:27-36.
• [12]Garcia JA, Bewley B, Redden JF: The St. Leger total knee replacement-a 7-year clinical assessment and survivorship analysis. Knee 2003, 10:173-177.
• [13]Forsythe ME, Dunbar MJ, Hennigar AW, Sullivan MJ, Gross M: Prospective relation between catastrophizing and residual pain following knee arthroplasty: two-year follow-up. Pain Res Manag 2008, 13:335-341.
• [14]Sullivan M, Tanzer M, Stanish W, Fallaha M, Keefe FJ, Simmonds M, Dunbar M: Psychological determinants of problematic outcomes following Total Knee Arthroplasty. Pain 2009, 143:123-129.
• [15]Tonelli SM, Rakel BA, Cooper NA, Angstom WL, Sluka KA: Women with knee osteoarthritis have more pain and poorer function than men, but similar physical activity prior to total knee replacement. Biol Sex Differ 2011, 2:12. BioMed Central Full Text
• [16]Lamb SE, Toye F, Barker KL: Chronic disease management programme in people with severe knee osteoarthritis: efficacy and moderators of response. Clin Rehabil 2008, 22:169-178.
• [17]Dekker J, van Dijk GM, Veenhof C: Risk factors for functional decline in osteoarthritis of the hip or knee. Curr Opin Rheumatol 2009, 21:520-524.
• [18]Marks R: Comorbid depression and anxiety impact hip osteoarthritis disability. Disabil Health J 2009, 2:27-35.
• [19]Lorig KR, Ritter PL, Laurent DD, Plant K: The internet-based arthritis self-management program: a one-year randomized trial for patients with arthritis or fibromyalgia. Arthritis Rheum 2008, 59:1009-1017.
• [20]Berkley KJ: Sex differences in pain. Behav Brain Sci 1997, 20:371-380.
• [21]Heppelmann B: Anatomy and histology of joint innervation. J Peripher Nerv Syst 1997, 2:5-16.
• [22]Schwab W, Funk RH: Innervation pattern of different cartilaginous tissues in the rat. Acta Anat (Basel) 1998, 163:184-190.
• [23]Suri S, Gill SE, Massena CS de, Wilson D, McWilliams DF, Walsh DA: Neurovascular invasion at the osteochondral junction and in osteophytes in osteoarthritis. Ann Rheum Dis 2007, 66:1423-1428.
• [24]Walsh DA, McWilliams DF, Turley MJ, Dixon MR, Franses RE, Mapp PI, Wilson D: Angiogenesis and nerve growth factor at the osteochondral junction in rheumatoid arthritis and osteoarthritis. Rheumatology (Oxford) 2010, 49:1852-1861.
• [25]Schaible HG, Von Banchet GS, Boettger MK, Brauer R, Gajda M, Richter F, Hensellek S, Brenn D, Natura G: The role of proinflammatory cytokines in the generation and maintenance of joint pain. Ann N Y Acad Sci 2010, 1193:60-69.
• [26]Flake NM, Bonebreak DB, Gold MS: Estrogen and inflammation increase the excitability of rat temporomandibular joint afferent neurons. J Neurophysiol 2005, 93:1585-1597.
• [27]Cairns BE, Sessle BJ, Hu JW: Characteristics of glutamate-evoked temporomandibular joint afferent activity in the rat. J Neurophysiol 2001, 85:2446-2454.
• [28]Loyd DR, Murphy AZ: 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.
• [29]Craft RM, Mogil JS, Aloisi AM: Sex differences in pain and analgesia: the role of gonadal hormones. Eur J Pain 2004, 8:397-411.
• [30]Craft RM: Sex differences in opioid analgesia: "from mouse to man". Clin J Pain 2003, 19:175-186.
• [31]Cook CD, Nickerson MD: Nociceptive sensitivity and opioid antinociception and antihyperalgesia in Freund's adjuvant-induced arthritic male and female rats. J Pharmacol Exp Ther 2005, 313:449-459.
• [32]Niesters M, Dahan A, Kest B, Zacny J, Stijnen T, Aarts L, Sarton E: Do sex differences exist in opioid analgesia? A systematic review and meta-analysis of human experimental and clinical studies. Pain 2010, 151:61-68.
• [33]Avouac J, Gossec L, Dougados M: Efficacy and safety of opioids for osteoarthritis: a meta-analysis of randomized controlled trials. Osteoarthritis Cartilage 2007, 15:957-965.
• [34]Stein C: The control of pain in peripheral tissue by opioids. Mechanisms of Disease 1995, 332:1685-1690.
• [35]Bajaj P, Bajaj P, Graven-Nielsen T, Arendt-Nielsen L: Osteoarthritis and its association with muscle hyperalgesia: an experimental controlled study. Pain 2001, 93:107-114.
• [36]Kosek E, Ordeberg G: Lack of pressure pain modulation by heterotopic noxious conditioning stimulation in patients with painful osteoarthritis before, but not following, surgical pain relief. Pain 2000, 88:69-78.
• [37]LeBars D, Dickenson AH, Besson J-M: Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain 1979, 6:305-327.
• [38]Yarnitsky D, Crispel Y, Eisenberg E, Granovsky Y, Ben-Nun A, Sprecher E, Best LA, Granot M: Prediction of chronic post-operative pain: pre-operative DNIC testing identifies patients at risk. Pain 2008, 138:22-28.
• [39]Sarlani E, Greenspan JD: Gender differences in temporal summation of mechanically evoked pain. Pain 2002, 97:163-169.
• [40]Staud R, Robinson ME, Vierck CJ, Price DD: 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.
• [41]Arendt-Nielsen L, Sluka KA, Nie HL: Experimental muscle pain impairs descending inhibition. Pain 2008, 140:465-471.
• [42]Tousignant-Laflamme Y, Marchand S: Excitatory and inhibitory pain mechanisms during the menstrual cycle in healthy women. Pain 2009, 146:47-55.
• [43]Baliki MN, Geha PY, Jabakhanji R, Harden N, Schnitzer TJ, Apkarian AV: A preliminary fMRI study of analgesic treatment in chronic back pain and knee osteoarthritis. Mol Pain 2008, 4:47. BioMed Central Full Text
• [44]Kulkarni B, Bentley DE, Elliott R, Julyan PJ, Boger E, Watson A, Boyle Y, El-Deredy W, Jones AK: Arthritic pain is processed in brain areas concerned with emotions and fear. Arthritis Rheum 2007, 56:1345-1354.
• [45]Parks EL, Geha PY, Baliki MN, Katz J, Schnitzer TJ, Apkarian AV: Brain activity for chronic knee osteoarthritis: Dissociating evoked pain from spontaneous pain. Eur J Pain 2011, 15:843e1-843e14.
• [46]Gwilym SE, Filippini N, Douaud G, Carr AJ, Tracey I: Thalamic atrophy associated with painful osteoarthritis of the hip is reversible after arthroplasty: a longitudinal voxel-based morphometric study. Arthritis Rheum 2010, 62:2930-2940.
• [47]Apkarian AV, Bushnell MC, Treede RD, Zubieta JK: Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 2005, 9:463-484.
• [48]Gwilym SE, Keltner JR, Warnaby CE, Carr AJ, Chizh B, Chessell I, Tracey I: Psychophysical and functional imaging evidence supporting the presence of central sensitization in a cohort of osteoarthritis patients. Arthritis Rheum 2009, 61:1226-1234.
• [49]DeSantana JM, Sluka KA: Central mechanisms in the maintenance of chronic widespread noninflammatory muscle pain. Curr Pain Headache Rep 2008, 12:338-343.
• [50]Fillingim RB, Gear RW: Sex differences in opioid analgesia: clinical and experimental findings. Eur J Pain 2004, 8:413-425.
• [51]Chakrabarti S, Liu NJ, Gintzler AR: Formation of mu-/kappa-opioid receptor heterodimer is sex-dependent and mediates female-specific opioid analgesia. Proc Natl Acad Sci USA 2010, 107:20115-20119.
• [52]Bodnar RJ, Kest B: Sex differences in opioid analgesia, hyperalgesia, tolerance and withdrawal: central mechanisms of action and roles of gonadal hormones. Horm Behav 2010, 58:72-81.
• [53]Craft RM: Sex differences in analgesic, reinforcing, discriminative, and motoric effects of opioids. Exp Clin Psychopharmacol 2008, 16:376-385.
• [54]Dahan A, Kest B, Waxman AR, Sarton E: Sex-specific responses to opiates: animal and human studies. Anesth Analg 2008, 107:83-95.
• [55]Sorge RE, LaCroix-Fralish ML, Tuttle AH, Sotocinal SG, Austin JS, Ritchie J, Chanda ML, Graham AC, Topham L, Beggs S, Salter MW, Mogil JS: Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice. J Neurosci 2011, 31:15450-15454.
• [56]Ji Y, Murphy AZ, Traub RJ: Estrogen modulates the visceromotor reflex and responses of spinal dorsal horn neurons to colorectal stimulation in the rat. J Neurosci 2003, 23:3908-3915.
• [57]Ji Y, Tang B, Cao DY, Wang G, Traub RJ: Sex differences in spinal processing of transient and inflammatory colorectal stimuli in the rat. Pain 2012, 153:1965-1973.
• [58]Lawson KP, Nag S, Thompson AD, Mokha SS: Sex-specificity and estrogen-dependence of kappa opioid receptor-mediated antinociception and antihyperalgesia. Pain 2010, 151:806-815.
• [59]Mogil JS, Bailey AL: Sex and gender differences in pain and analgesia. Prog Brain Res 2010, 186:141-157.
• [60]Loyd DR, Wang X, Murphy AZ: Sex differences in μ-opioid receptor expression in the rat midbrain periaqueductal gray are essential for eliciting sex differences in morphine analgesia. J Neurosci 2008, 28:14007-14017.
• [61]Ge HY, 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.
• [62]Loyd DR, Murphy AZ: Sex differences in the anatomical and functional organization of the periaqueductal gray-rostral ventromedial medullary pathway in the rat: a potential circuit mediating the sexually dimorphic actions of morphine. J Comp Neurol 2006, 496:723-738.
• [63]Lopez-Olivo MA, Landon GC, Siff SJ, Edelstein D, Pak C, Kallen MA, Stanley M, Zhang H, Robinson KC, Suarez-Almazor ME: Psychosocial determinants of outcomes in knee replacement. Ann Rheum Dis 2011, 70:1775-1781.
• [64]Borkhoff CM, Hawker GA, Wright JG: Patient gender affects the referral and recommendation for total joint arthroplasty. Clin Orthop Relat Res 2011, 469:1829-1837.
• [65]Vranceanu AM, Barsky A, Ring D: Psychosocial aspects of disabling musculoskeletal pain. J Bone Joint Surg Am 2009, 91:2014-2018.
• [66]Perrot S, Poiraudeau S, Kabir M, Bertin P, Sichere P, Serrie A, Rannou F: Active or passive pain coping strategies in hip and knee osteoarthritis? Results of a national survey of 4,719 patients in a primary care setting. Arthritis Rheum 2008, 59:1555-1562.
• [67]Unruh AM: Gender variations in clinical pain experience. Pain 1996, 65:123-167.
• [68]Riddle DL, Wade JB, Jiranek WA, Kong X: Preoperative pain catastrophizing predicts pain outcome after knee arthroplasty. Clin Orthop Relat Res 2010, 468:798-806.
• [69]Pells JJ, Shelby RA, Keefe FJ, Dixon KE, Blumenthal JA, Lacaille L, Tucker JM, Schmitt D, Caldwell DS, Kraus VB: Arthritis self-efficacy and self-efficacy for resisting eating: relationships to pain, disability, and eating behavior in overweight and obese individuals with osteoarthritic knee pain. Pain 2008, 136:340-347.
• [70]Shelby RA, Somers TJ, Keefe FJ, Pells JJ, Dixon KE, Blumenthal JA: Domain specific self-efficacy mediates the impact of pain catastrophizing on pain and disability in overweight and obese osteoarthritis patients. J Pain 2008, 9:912-919.
• [71]Fransen M, McConnell S, Bell M: Therapeutic exercise for people with osteoarthritis of the hip or knee. A systematic review. J Rheumatol 2002, 29:1737-1745.
• [72]Somers TJ, Keefe FJ, Pells JJ, Dixon KE, Waters SJ, Riordan PA, Blumenthal JA, McKee DC, Lacaille L, Tucker JM, Schmitt D, Caldwell DS, Kraus VB, Sims EL, Shelby RA, Rice JR: Pain catastrophizing and pain-related fear in osteoarthritis patients: relationships to pain and disability. J Pain Symptom Manage 2009, 37:863-872.
• [73]Tsai YF: Gender differences in pain and depressive tendency among Chinese elders with knee osteoarthritis. Pain 2007, 130:188-194.
• [74]Racine M, Tousignant-Laflamme Y, Kloda LA, Dion D, Dupuis G, Choiniere M: A systematic literature review of 10 years of research on sex/gender and pain perception - part 2: do biopsychosocial factors alter pain sensitivity differently in women and men? Pain 2012, 153:619-635.