Mechanical contributors to sex differences in idiopathic knee osteoarthritis

Daniel P Nicolella, Mary I O'Connor, Roger M Enoka, Barbara D Boyan, David A Hart, Eileen Resnick, Karen J Berkley, Kathleen A Sluka, C Kent Kwoh, Laura L Tosi, Richard D Coutts, Lorena M Havill, Wendy M Kohrt, Daniel P Nicolella, Mary I O'Connor, Roger M Enoka, Barbara D Boyan, David A Hart, Eileen Resnick, Karen J Berkley, Kathleen A Sluka, C Kent Kwoh, Laura L Tosi, Richard D Coutts, Lorena M Havill, Wendy M Kohrt

Abstract

The occurrence of knee osteoarthritis (OA) increases with age and is more common in women compared with men, especially after the age of 50 years. Recent work suggests that contact stress in the knee cartilage is a significant predictor of the risk for developing knee OA. Significant gaps in knowledge remain, however, as to how changes in musculoskeletal traits disturb the normal mechanical environment of the knee and contribute to sex differences in the initiation and progression of idiopathic knee OA. To illustrate this knowledge deficit, we summarize what is known about the influence of limb alignment, muscle function, and obesity on sex differences in knee OA. Observational data suggest that limb alignment can predict the development of radiographic signs of knee OA, potentially due to increased stresses and strains within the joint. However, these data do not indicate how limb alignment could contribute to sex differences in either the development or worsening of knee OA. Similarly, the strength of the knee extensor muscles is compromised in women who develop radiographic and symptomatic signs of knee OA, but the extent to which the decline in muscle function precedes the development of the disease is uncertain. Even less is known about how changes in muscle function might contribute to the worsening of knee OA. Conversely, obesity is a stronger predictor of developing knee OA symptoms in women than in men. The influence of obesity on developing knee OA symptoms is not associated with deviation in limb alignment, but BMI predicts the worsening of the symptoms only in individuals with neutral and valgus (knock-kneed) knees. It is more likely, however, that obesity modulates OA through a combination of systemic effects, particularly an increase in inflammatory cytokines, and mechanical factors within the joint. The absence of strong associations of these surrogate measures of the mechanical environment in the knee joint with sex differences in the development and progression of knee OA suggests that a more multifactorial and integrative approach in the study of this disease is needed. We identify gaps in knowledge related to mechanical influences on the sex differences in knee OA.

Figures

Figure 1
Figure 1
Full-length radiographs of both lower extremities showing neutral (left), varus (middle), and valgus (right) limb alignment. A line is drawn on each image from the center of the femoral head (representing the center of the hip joint) to the center of the ankle joint (talus). Left. When the line transects the knee joint, as in the neutral alignment, the weight-bearing stresses are well distributed in the lower extremity. Middle. When the line is medial to the center of the knee joint (varus alignment), there is an abnormal distribution of weight-bearing stresses on the medial (inner) aspect of the knee joint. Right. Conversely, when the line is located lateral to the center of the knee joint (valgus alignment), the weight-bearing stresses are greater on the lateral aspect of the knee joint.
Figure 2
Figure 2
Associations between knee extensor strength and the incidence of developing radiographic signs of tibiofemoral OA at 30 months of follow-up [20]. Those men (n = 70) and women (n = 198) in the MOST study who exhibited the radiographic signs are indicated in black bars and those who did not (men: 1,110; women: 2,679) are shown in grey bars. The data are plotted as percentages of the number of subjects in each group. Strength was measured on an isokinetic dynamometer using shortening contractions performed at 60º/s. Data were provided by Neil A. Segal, M.D.
Figure 3
Figure 3
Associations between knee extensor strength and the incidence of developing symptomatic and radiographic signs of knee OA at 30 months of follow-up [20]. Those men (n = 101) and women (n = 217) in the MOST study who exhibited both signs of knee OA are indicated in black bars and those who did not (men: 1,535; women: 2,223) are shown in grey bars. The data are plotted as percentages of the number of subjects in each group. Strength was measured on an isokinetic dynamometer using shortening contractions performed at 60º/s. Data were provided by Neil A. Segal, M.D.

References

    1. Brandt KD, Dieppe P, Radin E. Etiopathogenesis of osteoarthritis. Med Clin North Am. 2009;93:1–24. doi: 10.1016/j.mcna.2008.08.009. xv.
    1. Segal NA, Anderson DD, Iyer KS, Baker J, Torner JC, Lynch JA, Felson DT, Lewis CE, Brown TD. Baseline articular contact stress levels predict incident symptomatic knee osteoarthritis development in the MOST cohort. J Orthop Res. 2009;27:1562–1568. doi: 10.1002/jor.20936.
    1. Andriacchi TP, Mundermann A. The role of ambulatory mechanics in the initiation and progression of knee osteoarthritis. Curr Opin Rheumatol. 2006;18:514–518. doi: 10.1097/01.bor.0000240365.16842.4e.
    1. Mow VC, Ratcliffe A. In: Basic orthopaedic biomechanics. 2. Mow VC, Hayes WC, editor. New York: Lippincott Raven; 1997. Structure and function of articular cartilage and meniscus.
    1. Hsu RW, Himeno S, Coventry MB, Chao EY. Normal axial alignment of the lower extremity and load-bearing distribution at the knee. Clin Orthop Relat Res. 1990;255:215–227.
    1. Sharma L, Hurwitz DE, Thonar EJ, Sum JA, Lenz ME, Dunlop DD, Schnitzer TJ, Kirwan-Mellis G, Andriacchi T. Knee adduction moment, serum hyaluronan level, and disease severity in medial tibiofemoral osteoarthritis. Arthritis Rheum. 1998;41:1233–1240. doi: 10.1002/1529-0131(199807)41:7<1233::AID-ART14>;2-L.
    1. Bellemans J, Colyn W, Vandenneucker H, Victor J. The Chitranjan Ranawat Award: Is neutral mechanical alignment normal for all patients? The concept of constitutional varus. Clin Orthoped Related Res. 2012;470:45–53. doi: 10.1007/s11999-011-1936-5.
    1. Sharma L, Song J, Dunlop D, Felson D, Lewis CE, Segal N, Torner J, Cooke TDV, Hietpas J, Lynch J, Nevitt M. Varus and valgus alignment and incident and progressive knee osteoarthritis. Ann Rheum Dis. 2010;69:1940–1945. doi: 10.1136/ard.2010.129742.
    1. Brouwer GM, van Tol AW, Bergink AP, Belo JN, Bernsen RM, Reijman M, Pols HA, Bierma-Zeinstra SM. Association between valgus and varus alignment and the development and progression of radiographic osteoarthritis of the knee. Arthritis Rheum. 2007;56:1204–1211. doi: 10.1002/art.22515.
    1. Hunter DJ, Niu J, Felson DT, Harvey WF, Gross KD, McCree P, Aliabadi P, Sack B, Zhang Y. Knee alignment does not predict incident osteoarthritis: The Framingham osteoarthritis study. Arthritis Rheum. 2007;56:1212–1218. doi: 10.1002/art.22508.
    1. Yang NH, Canavan PK, Nayeb-Hashemi H. The effect of the frontal plane tibiofemoral angle and varus knee moment on the contact stress and strain at the knee cartilage. J Appl Biomech. 2010;26:432–443.
    1. Sheehy L, Felson D, Zhang Y, Niu J, Lam Y-M, Segal N, Lynch J, Cooke TDV. Does measurement of the anatomic axis consistently predict hip-knee-ankle angle (hka) for knee alignment studies in osteoarthritis? Analysis of long limb radiographs from the multicenter osteoarthritis (MOST) study. Osteoarthr Cartil. 2010;56:1212–1218.
    1. Cooke D, Scudamore A, Li J, Wyss U, Bryant T, Costigan P. Axial lower-limb alignment: Comparison of knee geometry in normal volunteers and osteoarthritis patients. Osteoarthritis Cartilage Osteoarthritis Res Soc. 1997;5:39–47. doi: 10.1016/S1063-4584(97)80030-1.
    1. Hovinga KR, Lerner AL. Anatomic variations between Japanese and Caucasian populations in the healthy young adult knee joint. J Orthop Res. 2009;27:1191–1196. doi: 10.1002/jor.20858.
    1. Tang WM, Zhu YH, Chiu KY. Axial alignment of the lower extremity in Chinese adults. J Bone Joint Surg. 2000;82-A:1603–1608.
    1. Tamari K, Tinley P, Briffa K, Aoyagi K. Ethnic-, gender-, and age-related differences in femorotibial angle, femoral antetorsion, and tibiofibular torsion: Cross-sectional study among healthy Japanese and Australian Caucasians. Clin Anat. 2006;19:59–67.
    1. Pandy MG, Andriacchi TP. Muscle and joint function in human locomotion. Ann Rev Biomed Engin. 2010;12:401–433. doi: 10.1146/annurev-bioeng-070909-105259.
    1. Baker KR, Xu L, Zhang Y, Nevitt M, Niu J, Aliabadi P, Yu W, Felson D. Quadriceps weakness and its relationship to tibiofemoral and patellofemoral knee osteoarthritis in Chinese: The Beijing osteoarthritis study. Arthritis Rheum. 2004;50:1815–1821. doi: 10.1002/art.20261.
    1. Palmieri-Smith RM, Thomas AC, Karvonen-Gutierrez C, Sowers MF. Isometric quadriceps strength in women with mild, moderate, and severe knee osteoarthritis. Amer J Physical Med Rehab. 2010;89:541–548. doi: 10.1097/PHM.0b013e3181ddd5c3.
    1. Segal NA, Torner JC, Felson D, Niu J, Sharma L, Lewis CE, Nevitt M. Effect of thigh strength on incident radiographic and symptomatic knee osteoarthritis in a longitudinal cohort. Arthritis Rheum. 2009;61:1210–1217. doi: 10.1002/art.24541.
    1. Amin S, Baker K, Niu J, Clancy M, Goggins J, Guermazi A, Grigoryan M, Hunter DJ, Felson DT. Quadriceps strength and the risk of cartilage loss and symptom progression in knee osteoarthritis. Arthritis Rheum. 2009;60:189–198. doi: 10.1002/art.24182.
    1. Brandt KD, Heilman DK, Slemenda C, Katz BP, Mazzuca SA, Braunstein EM, Byrd D. Quadriceps strength in women with radiographically progressive osteoarthritis of the knee and those with stable radiographic changes. J Rheum. 1999;26:2431–2437.
    1. Segal NA, Yack HJ, Brubaker M, Torner JC, Wallace R. Association of dynamic joint power with functional limitations in older adults with symptomatic knee osteoarthritis. Arch Phys Med Rehab. 2009;90:1821–1828. doi: 10.1016/j.apmr.2009.07.009.
    1. Astephen JL, Deluzio KJ, Caldwell GE, Dunbar MJ, Hubley-Kozey CL. Gait and neuromuscular pattern changes are associated with differences in knee osteoarthritis severity levels. J Biomech. 2008;41:868–876. doi: 10.1016/j.jbiomech.2007.10.016.
    1. Briem K, Snyder-Mackler L. Proximal gait adaptations in medial knee OA. J Orthop Res. 2009;27:78–83. doi: 10.1002/jor.20718.
    1. Mundermann A, Dyrby CO, Andriacchi TP. Secondary gait changes in patients with medial compartment knee osteoarthritis: Increased load at the ankle, knee, and hip during walking. Arthritis Rheum. 2005;52:2835–2844. doi: 10.1002/art.21262.
    1. Thorstensson CA, Petersson IF, Jacobsson LT, Boegard TL, Roos EM. Reduced functional performance in the lower extremity predicted radiographic knee osteoarthritis five years later. Ann Rheum Dis. 2004;63:402–407. doi: 10.1136/ard.2003.007583.
    1. Richards C, Higginson JS. Knee contact force in subjects with symmetrical OA grades: Differences between OA severities. J Biomech. 2010;43:2595–2600. doi: 10.1016/j.jbiomech.2010.05.006.
    1. Messier SP, Gutekunst DJ, Davis C, DeVita P. Weight loss reduces knee-joint loads in overweight and obese older adults with knee osteoarthritis. Arthritis Rheum. 2005;52:2026–2032. doi: 10.1002/art.21139.
    1. Gushue DL, Houck J, Lerner AL. Effects of childhood obesity on three-dimensional knee joint biomechanics during walking. J Ped Orthoped. 2005;25:763–768. doi: 10.1097/01.bpo.0000176163.17098.f4.
    1. Sibella F, Galli M, Romei M, Montesano A, Crivellini M. Biomechanical analysis of sit-to-stand movement in normal and obese subjects. Clin Biomech. 2003;18:745–750. doi: 10.1016/S0268-0033(03)00144-X.
    1. Cooper C, Snow S, McAlindon TE, Kellingray S, Stuart B, Coggon D, Dieppe PA. Risk factors for the incidence and progression of radiographic knee osteoarthritis. Arthritis Rheum. 2000;43:995–1000. doi: 10.1002/1529-0131(200005)43:5<995::AID-ANR6>;2-1.
    1. Felson DT, Zhang Y, Hannan MT, Naimark A, Weissman B, Aliabadi P, Levy D. Risk factors for incident radiographic knee osteoarthritis in the elderly: The Framingham study. Arthritis Rheum. 1997;40:728–733. doi: 10.1002/art.1780400420.
    1. Felson DT, Lawrence RC, Dieppe PA, Hirsch R, Helmick CG, Jordan JM, Kington RS, Lane NE, Nevitt MC, Zhang Y, Sowers M, McAlindon T, Spector TD, Poole AR, Yanovski SZ, Ateshian G, Sharma L, Buckwalter JA, Brandt KD, Fries JF. Osteoarthritis: New insights. Part 1: The disease and its risk factors. Ann Internal Med. 2000;133:635–646.
    1. Anderson JJ, Felson DT. Factors associated with osteoarthritis of the knee in the first national health and nutrition examination survey (hanes i). Evidence for an association with overweight, race, and physical demands of work. Am J Epidem. 1988;128:179–189.
    1. Holliday KL, McWilliams DF, Maciewicz RA, Muir KR, Zhang W, Doherty M. Lifetime body mass index, other anthropometric measures of obesity and risk of knee or hip osteoarthritis in the goal case–control study. Osteoarthritis Cartilage/OARS Osteoarthritis Res Soc. 2011;19:37–43. doi: 10.1016/j.joca.2010.10.014.
    1. Felson DT, Niu J, Clancy M, Sack B, Aliabadi P, Zhang Y. Effect of recreational physical activities on the development of knee osteoarthritis in older adults of different weights: The framingham study. Arthritis Rheum. 2007;57:6–12. doi: 10.1002/art.22464.
    1. Gandhi R, Wasserstein D, Razak F, Davey JR, Mahomed NN. BMI independently predicts younger age at hip and knee replacement. Obesity. 2010;18:2362–2366. doi: 10.1038/oby.2010.72.
    1. Gushue DL, Houck J, Lerner AL. Effects of childhood obesity on three-dimensional knee joint biomechanics during walking. J Pediatr Orthop. 2005;25:763–768. doi: 10.1097/01.bpo.0000176163.17098.f4.
    1. Sharma L, Lou C, Cahue S, Dunlop DD. The mechanism of the effect of obesity in knee osteoarthritis: The mediating role of malalignment. Arthritis Rheum. 2000;43:568–575. doi: 10.1002/1529-0131(200003)43:3<568::AID-ANR13>;2-E.
    1. Niu J, Zhang YQ, Torner J, Nevitt M, Lewis CE, Aliabadi P, Sack B, Clancy M, Sharma L, Felson DT. Is obesity a risk factor for progressive radiographic knee osteoarthritis? Arthritis Rheum. 2009;61:329–335. doi: 10.1002/art.24337.
    1. Cicuttini FM, Forbes A, Yuanyuan W, Rush G, Stuckey SL. Rate of knee cartilage loss after partial meniscectomy. J Rheumatol. 2002;29:1954–1956.
    1. Englund M, Guermazi A, Roemer FW, Aliabadi P, Yang M, Lewis CE, Torner J, Nevitt MC, Sack B, Felson DT. Meniscal tear in knees without surgery and the development of radiographic osteoarthritis among middle-aged and elderly persons: The multicenter osteoarthritis study. Arthritis Rheum. 2009;60:831–839. doi: 10.1002/art.24383.
    1. Englund M, Lohmander LS. Risk factors for symptomatic knee osteoarthritis fifteen to twenty-two years after meniscectomy. Arthritis Rheum. 2004;50:2811–2819. doi: 10.1002/art.20489.
    1. Haemer JM, Song Y, Carter DR, Giori NJ. Changes in articular cartilage mechanics with meniscectomy: A novel image-based modeling approach and comparison to patterns of OA. J Biomech. 2011;44:2307–2312. doi: 10.1016/j.jbiomech.2011.04.014.
    1. Kurosawa H, Fukubayashi T, Nakajima H. Load-bearing mode of the knee joint: Physical behavior of the knee joint with or without menisci. Clin Orthop Related Res. 1980;149:283–290.
    1. Allaire R, Muriuki M, Gilbertson L, Harner CD. Biomechanical consequences of a tear of the posterior root of the medial meniscus. Similar to total meniscectomy. J Bone Joint Surg Am. 2008;90:1922–1931. doi: 10.2106/JBJS.G.00748.
    1. Choi CJ, Choi YJ, Song IB, Choi CH. Characteristics of radial tears in the posterior horn of the medial meniscus compared to horizontal tears. Clin Orthop Surg. 2011;3:128–132. doi: 10.4055/cios.2011.3.2.128.
    1. Laberge MA, Baum T, Virayavanich W, Nardo L, Nevitt MC, Lynch J, McCulloch CE, Link TM. Obesity increases the prevalence and severity of focal knee abnormalities diagnosed using 3T MRI in middle-aged subjects-data from the Osteoarthritis Initiative. Skeletal Radiol. 2011;41:633–641.
    1. Oliveria SA, Felson DT, Cirillo PA, Reed JI, Walker AM. Body weight, body mass index, and incident symptomatic osteoarthritis of the hand, hip, and knee. Epidemiology. 1999;10:161–166. doi: 10.1097/00001648-199903000-00013.
    1. Srikanth VK, Fryer JL, Zhai G, Winzenberg TM, Hosmer D, Jones G. A meta-analysis of sex differences prevalence, incidence and severity of osteoarthritis. Osteoarthr Cartil. 2005;13:769–781. doi: 10.1016/j.joca.2005.04.014.
    1. Oliveria SA, Felson DT, Reed JI, Cirillo PA, Walker AM. Incidence of symptomatic hand, hip, and knee osteoarthritis among patients in a health maintenance organization. Arthritis Rheum. 1995;38:1134–1141. doi: 10.1002/art.1780380817.
    1. Sayer AA, Poole J, Cox V, Kuh D, Hardy R, Wadsworth M, Cooper C. Weight from birth to 53 years: A longitudinal study of the influence on clinical hand osteoarthritis. Arthritis Rheum. 2003;48:1030–1033. doi: 10.1002/art.10862.
    1. Cicuttini FM, Baker JR, Spector TD. The association of obesity with osteoarthritis of the hand and knee in women: A twin study. J Rheumatol. 1996;23:1221–1226.
    1. Griffin TM, Guilak F. Why is obesity associated with osteoarthritis? Insights from mouse models of obesity. Biorheology. 2008;45:387–398.
    1. Goldring MB, Otero M. Inflammation in osteoarthritis. Curr Opin Rheumatol. 2011;23:471–478. doi: 10.1097/BOR.0b013e328349c2b1.
    1. McNulty AL, Miller MR, O'Connor SK, Guilak F. The effects of adipokines on cartilage and meniscus catabolism. Connect Tissue Res. 2011;52:523–533. doi: 10.3109/03008207.2011.597902.
    1. Dumond H, Presle N, Terlain B, Mainard D, Loeuille D, Netter P, Pottie P. Evidence for a key role of leptin in osteoarthritis. Arthritis Rheum. 2003;48:3118–3129. doi: 10.1002/art.11303.
    1. Presle N, Pottie P, Dumond H, Guillaume C, Lapicque F, Pallu S, Mainard D, Netter P, Terlain B. Differential distribution of adipokines between serum and synovial fluid in patients with osteoarthritis. Contribution of joint tissues to their articular production. Osteoarthr Cartil. 2006;14:690–695. doi: 10.1016/j.joca.2006.01.009.
    1. Berry PA, Wluka AE, Davies-Tuck ML, Wang Y, Strauss BJ, Dixon JB, Proietto J, Jones G, Cicuttini FM. The relationship between body composition and structural changes at the knee. Rheumatol (Oxford) 2010;49:2362–2369. doi: 10.1093/rheumatology/keq255.
    1. Yang. The effect of the frontal plane tibiofemoral angle on the contact stress and strain at the knee joint. Ph.D. dissertation: Department of Mechanical and Industrial Engineering. Chicago, IL: Northeastern University; 2009.

Source: PubMed

3
Se inscrever