Changes in bone marrow lesions in response to weight-loss in obese knee osteoarthritis patients: a prospective cohort study

BMC Musculoskeletal Disorders

Henning Bliddal¹  Bente Danneskiold-Samsøe¹  Marius Henriksen⁴  Else Marie Bartels⁴  Robin Christensen²  Mikael Boesen³  Henrik Gudbergsen⁴ 

[1] SMI, Aalborg University, Aalborg, Denmark;Institute of Sports Science and Clinical Biomechanics, University of Southern, Odense, Denmark;Department of Radiology, Copenhagen University Hospital, Frederiksberg, Denmark;The Parker Institute, Department of Rheumatology, Copenhagen University Hospital, Frederiksberg, Denmark

关键词: Obesity;    Weight-loss;    Bone marrow lesions;    Knee osteoarthritis;    MRI;   

Others  :  1133251
DOI  :  10.1186/1471-2474-14-106

 received in 2012-08-04, accepted in 2013-03-05,  发布年份 2013

【 摘 要 】

Background

Patients are susceptible for knee osteoarthritis (KOA) with increasing age and obesity and KOA is expected to become a major disabling disease in the future. An important feature of KOA on magnetic resonance imaging (MRI) is changes in the subchondral bone, bone marrow lesions (BMLs), which are related to the future degeneration of the knee joint as well as prevalent clinical symptoms. The aim of this study was to investigate the changes in BMLs after a 16-week weight-loss period in obese subjects with KOA and relate changes in BMLs to the effects of weight-loss on clinical symptoms.

Methods

This prospective cohort study included patients with a body mass index ≥ 30 kg/m², an age ≥ 50 years and primary KOA. Patients underwent a 16 weeks supervised diet program which included formula products and dietetic counselling (ClinicalTrials.gov: NCT00655941). BMLs in tibia and femur were assessed on MRI before and after the weight-loss using the Boston-Leeds Osteoarthritis Knee Score. Response to weight-loss in BML scores was dichotomised to patients experiencing a decrease in BML scores (responders) and patients who did not (non-responders). The association of BMLs to weight-loss was assessed by logistic regressions and correlation analyses.

Results

39 patients (23%) were classified as responders in the sum of all BML size scores whereas 130 patients (77%) deteriorated or remained stable and were categorized as non-responders. Logistic regression analyses revealed no association between weight-loss < or ≥ 10% and response in BMLs in the most affected compartment (OR 1.86 [CI 0.66 to 5.26, p=0.24]). There was no association between weight-loss and response in maximum BML score (OR 1.13 [CI 0.39 to 3.28, p=0.81]). The relationship between changes in BMLs and clinical symptoms revealed that an equal proportion of patients classified as BML responders and non-responders experienced an OMERACT-OARSI response (69 vs. 71%, p=0.86).

Conclusions

Weight-loss did not improve the sum of tibiofemoral BML size scores or the maximum tibiofemoral BML score, suggesting that BMLs do not respond to a rapidly decreased body weight. The missing relationship between clinical symptoms and BMLs calls for further investigation.

【 授权许可】

   
2013 Gudbergsen et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Dillon CF, Rasch EK, Gu Q, Hirsch R: Prevalence of knee osteoarthritis in the United States: arthritis data from the Third National Health and Nutrition Examination Survey 1991–94. J Rheumatol 2006, 33:2271-2279.
• [2]Lohmander LS, Gerhardsson D, Rollof J, Nilsson PM, Engstrom G: Incidence of severe knee and hip osteoarthritis in relation to different measures of body mass: a population-based prospective cohort study. Ann Rheum Dis 2009, 68:490-496.
• [3]Woolf AD, Pfleger B: Burden of major musculoskeletal conditions. Bull World Health Organ 2003, 81:646-656.
• [4]Blagojevic M, Jinks C, Jeffery A, Jordan KP: Risk factors for onset of osteoarthritis of the knee in older adults: a systematic review and meta-analysis. Osteoarthr Cartil 2010, 18:24-33.
• [5]Felson DT, Zhang Y, Anthony JM, Naimark A, Anderson JJ: Weight loss reduces the risk for symptomatic knee osteoarthritis in women. The Framingham Study. Ann Intern Med 1992, 116:535-539.
• [6]Jinks C, Jordan K, Croft P: Disabling knee pain–another consequence of obesity: results from a prospective cohort study. BMC Publ Health 2006, 6:258. BioMed Central Full Text
• [7]Messier SP, Loeser RF, Miller GD, Morgan TM, Rejeski WJ, Sevick MA: Exercise and dietary weight loss in overweight and obese older adults with knee osteoarthritis: the Arthritis, Diet, and Activity Promotion Trial. Arthritis Rheum 2004, 50:1501-1510.
• [8]Christensen R, Astrup A, Bliddal H: Weight loss: the treatment of choice for knee osteoarthritis? A randomized trial. Osteoarthr Cartil 2005, 13:20-27.
• [9]Gudbergsen H, Boesen M, Christensen R, Astrup A, Bliddal H: Radiographs and low field MRI (0.2T) as predictors of efficacy in a weight loss trial in obese women with knee osteoarthritis. BMC Musculoskelet Disord 2011, 12:56. BioMed Central Full Text
• [10]Gudbergsen H, Boesen M, Lohmander LS, Christensen R, Henriksen M, Bartels EM: Weight loss is effective for symptomatic relief in obese subjects with knee osteoarthritis independently of joint damage severity assessed by high-field MRI and radiography. Osteoarthr Cartil 2012, 20:495-502.
• [11]Hunter DJ, Lo GH, Gale D, Grainger AJ, Guermazi A, Conaghan PG: The reliability of a new scoring system for knee osteoarthritis MRI and the validity of bone marrow lesion assessment: BLOKS (Boston Leeds Osteoarthritis Knee Score). Ann Rheum Dis 2008, 67:206-211.
• [12]Hill CL, Hunter DJ, Niu J, Clancy M, Guermazi A, Genant H: Synovitis detected on magnetic resonance imaging and its relation to pain and cartilage loss in knee osteoarthritis. Ann Rheum Dis 2007, 66:1599-1603.
• [13]Felson DT, Chaisson CE, Hill CL, Totterman SM, Gale ME, Skinner KM: The association of bone marrow lesions with pain in knee osteoarthritis. Ann Intern Med 2001, 134:541-549.
• [14]Hunter DJ, March L, Sambrook PN: The association of cartilage volume with knee pain. Osteoarthr Cartil 2003, 11:725-729.
• [15]Cicuttini FM, Jones G, Forbes A, Wluka AE: Rate of cartilage loss at two years predicts subsequent total knee arthroplasty: a prospective study. Ann Rheum Dis 2004, 63:1124-1127.
• [16]Felson DT, Lawrence RC, Dieppe PA, Hirsch R, Helmick CG, Jordan JM: Osteoarthritis: new insights. Part 1: the disease and its risk factors. Ann Intern Med 2000, 133:635-646.
• [17]McAlindon TE, Cooper C, Kirwan JR, Dieppe PA: Determinants of disability in osteoarthritis of the knee. Ann Rheum Dis 1993, 52:258-262.
• [18]Dore D, Martens A, Quinn S, Ding CH, Winzenberg T, Zhai GJ: Bone marrow lesions predict site-specific cartilage defect development and volume loss: a prospective study in older adults. Arthritis Res Ther 2010, 12.
• [19]Felson DT, McLaughlin S, Goggins J, LaValley MP, Gale ME, Totterman S: Bone marrow edema and its relation to progression of knee osteoarthritis. Ann Intern Med 2003, 139:330-336.
• [20]Yusuf E, Kortekaas MC, Watt I, Huizinga TW, Kloppenburg M: Do knee abnormalities visualised on MRI explain knee pain in knee osteoarthritis? A systematic review. Ann Rheum Dis 2011, 70:60-67.
• [21]Hayashi D, Englund M, Roemer FW, Niu J, Sharma L, Felson DT: Knee malalignment is associated with an increased risk for incident and enlarging bone marrow lesions in the more loaded compartments: the MOST study. Osteoarthr Cartil 2012, 20:1227-1233.
• [22]Riecke BF, Christensen R, Christensen P, Leeds AR, Boesen M, Lohmander LS: Comparing two low-energy diets for the treatment of knee osteoarthritis symptoms in obese patients: a pragmatic randomized clinical trial. Osteoarthr Cartil 2010.
• [23]Altman RD: Criteria for the classification of osteoarthritis of the knee and hip. Scand J Rheumatol Suppl 1987, 65:31-39.
• [24]Crema MD, Roemer FW, Marra MD, Guermazi A: Magnetic resonance imaging assessment of subchondral bone and soft tissues in knee osteoarthritis. Rheum Dis Clin North Am 2009, 35:557-577.
• [25]Eckstein F, Sittek H, Milz S, Putz R, Reiser M: The morphology of articular cartilage assessed by magnetic resonance imaging (MRI). Reproducibility and anatomical correlation. Surg Radiol Anat 1994, 16:429-438.
• [26]Recht MP, Piraino DW, Paletta GA, Schils JP, Belhobek GH: Accuracy of fat-suppressed three-dimensional spoiled gradient-echo FLASH MR imaging in the detection of patellofemoral articular cartilage abnormalities. Radiology 1996, 198:209-212.
• [27]Rosset A, Spadola L, Ratib O: OsiriX: an open-source software for navigating in multidimensional DICOM images. J Digit Imaging 2004, 17:205-216.
• [28]Altman RD, Gold GE: Atlas of individual radiographic features in osteoarthritis, revised. Osteoarthr Cartil 2007, 15:A1-56.
• [29]Kellgren JH, Lawrence JS: Radiological assessment of osteo-arthrosis. Ann Rheum Dis 1957, 16:494-502.
• [30]Hart DJ, Spector TD: The classification and assessment of osteoarthritis. Baillieres Clin Rheumatol 1995, 9:407-432.
• [31]Mundermann A, Dyrby CO, Andriacchi TP: A comparison of measuring mechanical axis alignment using three-dimensional position capture with skin markers and radiographic measurements in patients with bilateral medial compartment knee osteoarthritis. Knee 2008, 15:480-485.
• [32]Lund H, Sondergaard K, Zachariassen T, Christensen R, Bulow P, Henriksen M: Learning effect of isokinetic measurements in healthy subjects, and reliability and comparability of Biodex and Lido dynamometers. Clin Physiol Funct Imaging 2005, 25:75-82.
• [33]Gudbergsen H, Bartels EM, Krusager P, Waehrens EE, Christensen R, Nneskiold-Samsoe B: Test-retest of computerized health status questionnaires frequently used in the monitoring of knee osteoarthritis: a randomized crossover trial. BMC Musculoskelet Disord 2011, 12:190. BioMed Central Full Text
• [34]Pham T, der HD V, Altman RD, Anderson JJ, Bellamy N, Hochberg M: OMERACT-OARSI initiative: Osteoarthritis Research Society International set of responder criteria for osteoarthritis clinical trials revisited. Osteoarthr Cartil 2004, 12:389-399.
• [35]Roos EM, Roos HP, Ekdahl C, Lohmander LS: Knee injury and Osteoarthritis Outcome Score (KOOS)–validation of a Swedish version. Scand J Med Sci Sports 1998, 8:439-448.
• [36]Nguyen TV, Eisman JA: Assessment of significant change in BMD: a new approach. J Bone Miner Res 2000, 15:369-372.
• [37]Dore D, Quinn S, Ding CH, Winzenberg T, Zhai GJ, Cicuttini F: Natural history and clinical significance of MRI-detected bone marrow lesions at the knee: a prospective study in community dwelling older adults. Arthritis Res Ther 2010, 12.
• [38]Hayes CW, Conway WF, Sundaram M: Misleading aggressive MR imaging appearance of some benign musculoskeletal lesions. RadioGraphics 1992, 12:1119-1134.
• [39]Zanetti M, Bruder E, Romero J, Hodler J: Bone marrow edema pattern in osteoarthritic knees: correlation between MR imaging and histologic findings. Radiology 2000, 215:835-840.
• [40]Lo GH, McAlindon TE, Niu J, Zhang Y, Beals C, Dabrowski C: Bone marrow lesions and joint effusion are strongly and independently associated with weight-bearing pain in knee osteoarthritis: data from the osteoarthritis initiative. Osteoarthr Cartil 2009.
• [41]Torres L, Dunlop DD, Peterfy C, Guermazi A, Prasad P, Hayes KW: The relationship between specific tissue lesions and pain severity in persons with knee osteoarthritis. Osteoarthr Cartil 2006, 14:1033-1040.
• [42]Kornaat PR, Kloppenburg M, Sharma R, Botha-Scheepers SA, Le Graverand MP, Coene LN: Bone marrow edema-like lesions change in volume in the majority of patients with osteoarthritis; associations with clinical features. Eur Radiol 2007, 17:3073-3078.
• [43]Hunter DJ, Zhang Y, Niu J, Goggins J, Amin S, LaValley MP: Increase in bone marrow lesions associated with cartilage loss: a longitudinal magnetic resonance imaging study of knee osteoarthritis. Arthritis Rheum 2006, 54:1529-1535.
• [44]Felson DT, Parkes MJ, Marjanovic EJ, Callaghan M, Gait A, Cootes T: Bone marrow lesions in knee osteoarthritis change in 6–12 weeks. Osteoarthr Cartil 2012, 20:1514-1518.
• [45]Zhang Y, Nevitt M, Niu J, Lewis C, Torner J, Guermazi A: Fluctuation of knee pain and changes in bone marrow lesions, effusions, and synovitis on magnetic resonance imaging. Arthritis Rheum 2011, 63:691-699.
• [46]Orita S, Koshi T, Mitsuka T, Miyagi M, Inoue G, Arai G: Associations between proinflammatory cytokines in the synovial fluid and radiographic grading and pain-related scores in 47 consecutive patients with osteoarthritis of the knee. BMC Musculoskelet Disord 2011, 12:144. BioMed Central Full Text
• [47]Griffin TM, Fermor B, Huebner JL, Kraus VB, Rodriguiz RM, Wetsel WC: Diet-induced obesity differentially regulates behavioral, biomechanical, and molecular risk factors for osteoarthritis in mice. Arthritis Res Ther 2010, 12:R130. BioMed Central Full Text
• [48]Bennell K, Creaby M, Wrigley T, Bowles K-A, Hinman R, Cicuttini F: The relation of dynamic mechanical loading to bone marrow lesions in medial knee osteoarthritis. QC Canada: Osteoarthritis and Cartilage Conference: 2009 World Congress on Osteoarthritis Montreal; 2009:S86-S87.
• [49]McDougall JJ: Arthritis and pain. Neurogenic origin of joint pain. Arthritis Res Ther 2006, 8:220. BioMed Central Full Text
• [50]Gwilym SE, Keltner JR, Warnaby CE, Carr AJ, Chizh B, Chessell I: Psychophysical and functional imaging evidence supporting the presence of central sensitization in a cohort of osteoarthritis patients. Arthritis Rheum 2009, 61:1226-1234.
• [51]Keefe FJ, Somers TJ: Psychological approaches to understanding and treating arthritis pain. Nat Rev Rheumatol 2010, 6:210-216.
• [52]Wager TD: Expectations and anxiety as mediators of placebo effects in pain. Pain 2005, 115:225-226.
• [53]Hunter DJ, Guermazi A, Lo GH, Grainger AJ, Conaghan PG, Boudreau RM: Evolution of semi-quantitative whole joint assessment of knee OA: MOAKS (MRI Osteoarthritis Knee Score). Osteoarthr Cartil 2011.
• [54]Reichmann WM, Maillefert JF, Hunter DJ, Katz JN, Conaghan PG, Losina E: Responsiveness to change and reliability of measurement of radiographic joint space width in osteoarthritis of the knee: a systematic review. Osteoarthr Cartil 2011.
• [55]Peterfy CG, Schneider E, Nevitt M: The osteoarthritis initiative: report on the design rationale for the magnetic resonance imaging protocol for the knee. Osteoarthr Cartil 2008.
• [56]Lynch JA, Roemer FW, Nevitt MC, Felson DT, Niu J, Eaton CB: Comparison of BLOKS and WORMS scoring systems part I. Cross sectional comparison of methods to assess cartilage morphology, meniscal damage and bone marrow lesions on knee MRI: Data from the osteoarthritis initiative. Osteoarthr Cartil 2010, 18:1393-1401.
• [57]Dore D, De HJ, Giles G, Ding C, Cicuttini F, Jones G: A longitudinal study of the association between dietary factors, serum lipids, and bone marrow lesions of the knee. Arthritis Res Ther 2012, 14:R13. BioMed Central Full Text
• [58]Meredith DS, Losina E, Neumann G, Yoshioka H, Lang PK, Katz JN: Empirical evaluation of the inter-relationship of articular elements involved in the pathoanatomy of knee osteoarthritis using magnetic resonance imaging. BMC Musculoskelet Disord 2009, 10:133. BioMed Central Full Text
• [59]Hernandez-Molina G, Neogi T, Hunter DJ, Niu J, Guermazi A, Reichenbach S: The association of bone attrition with knee pain and other MRI features of osteoarthritis. Ann Rheum Dis 2008, 67:43-47.