The influence of joint loading on bone marrow lesions in the knee

American Journal of Sports Medicine

Volumn 43, Issue 12, 2015, Pages 3093-3107

  Beckwée, David ^a   Vaes, Peter ^a   Shahabpour, Maryam ^b   Muyldermans, Ronald ^a   Rommers, Nikki ^a   Bautmans, Ivan ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

Author keywords

aging athlete; biology of bone; knee; magnetic resonance imaging

Indexed keywords

BODY COMPOSITION; BODY WEIGHT; BONE MARROW; DISEASE COURSE; HUMAN; KNEE; KNEE OSTEOARTHRITIS; META ANALYSIS; MOTOR ACTIVITY; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; WEIGHT BEARING;

BODY COMPOSITION; BODY WEIGHT; BONE MARROW; DISEASE PROGRESSION; HUMANS; KNEE JOINT; MAGNETIC RESONANCE IMAGING; MOTOR ACTIVITY; OSTEOARTHRITIS, KNEE; WEIGHT-BEARING;

EID: 84949024659     PISSN: 03635465     EISSN: 15523365     Source Type: Journal    
DOI: 10.1177/0363546514565092     Document Type: Article

References (74)

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 (9): 1922-1931.
2. Altman R, Asch E, Bloch D, et al. Development of criteria for the classification and reporting of osteoarthritis: classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum. 1986; 29 (8): 1039-1049.
3. Andriacchi TP, Mundermann A,. The role of ambulatory mechanics in the initiation and progression of knee osteoarthritis. Curr Opin Rheumatol. 2006; 18 (5): 514-518.
4. Baranyay FJ, Wang Y, Wluka AE, et al. Association of bone marrow lesions with knee structures and risk factors for bone marrow lesions in the knees of clinically healthy, community-based adults. Semin Arthritis Rheum. 2007; 37 (2): 112-118.
5. Beckwee D, Vaes P, Cnudde M, Swinnen E, Bautmans I,. Osteoarthritis of the knee: why does exercise work? A qualitative study of the literature. Ageing Res Rev. 2013; 12 (1): 226-236.
6. Bennell KL, Bowles KA, Payne C, et al. Lateral wedge insoles for medial knee osteoarthritis: 12 month randomised controlled trial. BMJ. 2011; 342: d2912.
7. Bennell KL, Bowles KA, Wang Y, Cicuttini F, Davies-Tuck M, Hinman RS,. Higher dynamic medial knee load predicts greater cartilage loss over 12 months in medial knee osteoarthritis. Ann Rheum Dis. 2011; 70 (10): 1770-1774.
8. Bennell KL, Creaby MW, Wrigley TV, et al. Bone marrow lesions are related to dynamic knee loading in medial knee osteoarthritis. Ann Rheum Dis. 2010; 69 (6): 1151-1154.
9. Berry PA, Wluka AE, Davies-Tuck ML, et al. The relationship between body composition and structural changes at the knee. Rheumatology (Oxford). 2010; 49 (12): 2362-2369.
10. Brennan SL, Cicuttini FM, Pasco JA, et al. Does an increase in body mass index over 10 years affect knee structure in a population-based cohort study of adult women? Arthritis Res Ther. 2010; 12 (4): R139.
11. Chaudhari AM, Briant PL, Bevill SL, Koo S, Andriacchi TP,. Knee kinematics, cartilage morphology, and osteoarthritis after ACL injury. Med Sci Sports Exerc. 2008; 40 (2): 215-222.
12. 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 (7): 1221-1226.
13. Clarys JP, Scafoglieri A, Provyn S, Bautmans I,. Body mass index as a measure of bone mass. J Sports Med Phys Fitness. 2010; 50 (2): 202-206.
14. Cochrane Collaboration. Beoordeling van de kwaliteit van een randomised controlled trial (RCT). 2014. Available at: http://ohg.cochrane.org/sites/ohg.cochrane.org/files/uploads/Risk%20of%20bias%20assessment%20tool.pdf. Accessed February 24, 2014.
15. Cochrane Collaboration. Data extraction template. Accessed February 25, 2014. Available at: http://chmg.cochrane.org/sites/chmg.cochrane.org/files/uploads/Template-Data%20Extraction-CHMG.pdf. Accessed February 24, 2014.
16. Davies-Tuck ML, Wluka AE, Forbes A, et al. Development of bone marrow lesions is associated with adverse effects on knee cartilage while resolution is associated with improvement: a potential target for prevention of knee osteoarthritis. A longitudinal study. Arthritis Res Ther. 2010; 12 (1): R10.
17. Deeks JJ, Higgins JPT, Altman DG,. Analysing data and undertaking meta-analyses. In: Higgins JPT, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions: Version 5.0.1 [Updated September 2008]. Oxford: Cochrane Collaboration; 2008:9.1-9.43
18. DerSimonian R, Laird N,. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7 (3): 177-188.
19. Doré D, Quinn S, Ding C, et al. 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 (6): R223.
20. Doré DA, Winzenberg TM, Ding C, et al. The association between objectively measured physical activity and knee structural change using MRI. Ann Rheum Dis. 2013; 72 (7): 1170-1175.
21. Dutch Cochrane Collaboration. Formulier III voor het beoordelen van cohortonderzoek. Available at: http://dcc.cochrane.org/sites/dcc.cochrane.org/files/uploads/cohort.pdf. Accessed February 24, 2014.
22. Dutch Cochrane Collaboration. Formulier IV voor het beoordelen van een patiënt-controleonderzoek. Available at: http://dcc.cochrane.org/sites/dcc.cochrane.org/files/uploads/patient-controleonderzoek.pdf. Accessed February 24, 2014.
23. Englund M, Guermazi A, Roemer FW, et al. Meniscal pathology on MRI increases the risk for both incident and enlarging subchondral bone marrow lesions of the knee: the MOST Study. Ann Rheum Dis. 2010; 69 (10): 1796-1802.
24. Felson DT, McLaughlin S, Goggins J, et al. Bone marrow edema and its relation to progression of knee osteoarthritis. Ann Intern Med. 2003; 139 (5 Pt 1): 330-336.
25. Felson DT, Niu J, Guermazi A, et al. Correlation of the development of knee pain with enlarging bone marrow lesions on magnetic resonance imaging. Arthritis Rheum. 2007; 56 (9): 2986-2992.
26. Fernandes L, Hagen KB, Bijlsma JW, et al. EULAR recommendations for the non-pharmacological core management of hip and knee osteoarthritis. Ann Rheum Dis. 2013; 72 (7): 1125-1135.
27. Frobell RB, Le Graverand MP, Buck R, et al. The acutely ACL injured knee assessed by MRI: changes in joint fluid, bone marrow lesions, and cartilage during the first year. Osteoarthritis Cartilage. 2009; 17 (2): 161-167.
28. Gaugler M, Wirz D, Ronken S, et al. Fibrous cartilage of human menisci is less shock-absorbing and energy-dissipating than hyaline cartilage. [published online March 11, 2014]. Knee Surg Sports Traumatol Arthrosc. doi: 10.1007/s00167-014-2926-4.
29. Gudbergsen H, Boesen M, Christensen R, et al. Changes in bone marrow lesions in response to weight-loss in obese knee osteoarthritis patients: a prospective cohort study. BMC Musculoskelet Disord. 2013; 14: 106.
30. Guermazi A, Niu J, Hayashi D, et al. Prevalence of abnormalities in knees detected by MRI in adults without knee osteoarthritis: population based observational study (Framingham Osteoarthritis Study). BMJ. 2012; 345: e5339.
31. Guymer E, Baranyay F, Wluka AE, et al. A study of the prevalence and associations of subchondral bone marrow lesions in the knees of healthy, middle-aged women. Osteoarthritis Cartilage. 2007; 15 (12): 1437-1442.
32. Hayashi D, Englund M, Roemer FW, et al. Knee malalignment is associated with an increased risk for incident and enlarging bone marrow lesions in the more loaded compartments: the MOST study. Osteoarthritis Cartilage. 2012; 20 (11): 1227-1233.
33. Higgins JP, Thompson SG, Deeks JJ, Altman DG,. Measuring inconsistency in meta-analyses. BMJ. 2003; 327 (7414): 557-560.
34. Hinman RS, Payne C, Metcalf BR, Wrigley TV, Bennell KL,. Lateral wedges in knee osteoarthritis: what are their immediate clinical and biomechanical effects and can these predict a three-month clinical outcome? Arthritis Rheum. 2008; 59 (3): 408-415.
35. Hohmann E, Wortler K, Imhoff AB,. MR imaging of the hip and knee before and after marathon running. Am J Sports Med. 2004; 32 (1): 55-59.
36. Hovis KK, Alizai H, Tham S-C, et al. Non-traumatic anterior cruciate ligament abnormalities and their relationship to osteoarthritis using morphological grading and cartilage T2 relaxation times: data from the Osteoarthritis Initiative (OAI). Skeletal Radiol. 2012; 41 (11): 1435-1443.
37. Huetink K, Nelissen RGHH, Watt I, van Erkel AR, Bloem JL,. Localized development of knee osteoarthritis can be predicted from MR imaging findings a decade earlier. Radiology. 2010; 256 (2): 536-546.
38. Hunter DJ, Gerstenfeld L, Bishop G, et al. Bone marrow lesions from osteoarthritis knees are characterized by sclerotic bone that is less well mineralized. Arthritis Res Ther. 2009; 11 (1): R11.
39. 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 (2): 206-211.
40. Hunter DJ, Zhang Y, Niu J, et al. Increase in bone marrow lesions associated with cartilage loss: a longitudinal magnetic resonance imaging study of knee osteoarthritis. Arthritis Rheum. 2006; 54 (5): 1529-1535.
41. Issa SN, Dunlop D, Chang A, et al. Full-limb and knee radiography assessments of varus-valgus alignment and their relationship to osteoarthritis disease features by magnetic resonance imaging. Arthritis Rheum. 2007; 57 (3): 398-406.
42. Karsdal MA, Christiansen C, Ladel C, Henriksen K, Kraus VB, Bay-Jensen AC,. Osteoarthritis: a case for personalized health care? Osteoarthritis Cartilage. 2014; 22 (1): 7-16.
43. Kean CO, Hinman RS, Bowles KA, Cicuttini F, Davies-Tuck M, Bennell KL,. Comparison of peak knee adduction moment and knee adduction moment impulse in distinguishing between severities of knee osteoarthritis. Clin Biomech (Bristol, Avon). 2012; 27 (5): 520-523.
44. Krampla W, Mayrhofer R, Malcher J, Kristen KH, Urban M, Hruby W,. MR imaging of the knee in marathon runners before and after competition. Skeletal Radiol. 2001; 30 (2): 72-76.
45. Laberge MA, Baum T, Virayavanich W, et al. 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. 2012; 41 (6): 633-641.
46. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009; 339: b2700.
47. Lim YZ, Wang Y, Wluka AE, et al. Are biomechanical factors, meniscal pathology, and physical activity risk factors for bone marrow lesions at the knee? A systematic review. Semin Arthritis Rheum. 2013; 43 (2): 187-194.
48. Litwic A, Edwards MH, Dennison EM, Cooper C,. Epidemiology and burden of osteoarthritis. Br Med Bull. 2013; 105: 185-199.
49. Lo GH, Hunter DJ, Nevitt M, Lynch J, McAlindon TE,. Strong association of MRI meniscal derangement and bone marrow lesions in knee osteoarthritis: data from the Osteoarthritis Initiative. Osteoarthritis Cartilage. 2009; 17 (6): 743-747.
50. Lowitz T, Museyko O, Bousson V, et al. Bone marrow lesions identified by MRI in knee osteoarthritis are associated with locally increased bone mineral density measured by QCT. Osteoarthritis Cartilage. 2013; 21 (7): 957-964.
51. McAlindon TE, Bannuru RR, Sullivan MC, et al. OARSI guidelines for the non-surgical management of knee osteoarthritis. Osteoarthritis Cartilage. 2014; 22 (3): 363-388.
52. 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 (7): 2026-2032.
53. Messier SP, Legault C, Loeser RF, et al. Does high weight loss in older adults with knee osteoarthritis affect bone-on-bone joint loads and muscle forces during walking? Osteoarthritis Cartilage. 2011; 19 (3): 272-280.
54. Oberlander KD, Bruggemann GP, Hoher J, Karamanidis K,. Knee mechanics during landing in anterior cruciate ligament patients: a longitudinal study from pre- to 12 months post-reconstruction. Clin Biomech (Bristol, Avon). 2014; 29 (5): 512-517.
55. 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 (2): 161-166.
56. Pottie P, Presle N, Terlain B, Netter P, Mainard D, Berenbaum F,. Obesity and osteoarthritis: more complex than predicted! Ann Rheum Dis. 2006; 65 (11): 1403-1405.
57. Racunica TL, Teichtahl AJ, Wang Y, et al. Effect of physical activity on articular knee joint structures in community-based adults. Arthritis Rheum. 2007; 57 (7): 1261-1268.
58. Ratzlaff C, Guermazi A, Collins J, et al. A rapid, novel method of volumetric assessment of MRI-detected subchondral bone marrow lesions in knee osteoarthritis. Osteoarthritis Cartilage. 2013; 21 (6): 806-814.
59. Roemer FW, Frobell R, Hunter DJ, et al. MRI-detected subchondral bone marrow signal alterations of the knee joint: terminology, imaging appearance, relevance and radiological differential diagnosis. Osteoarthritis Cartilage. 2009; 17 (9): 1115-1131.
60. Scafoglieri A, Provyn S, Bautmans I, Van Roy P, Clarys JP,. Body mass index: misleading popular science? In: Ergen E, Ulkar B, Guner R, eds. Proceedings of the 6th European Sports Medicine Congress (EFSMA). Bologna, Italy: Medimond International Proceedings; 2009: 15-20.
61. Scafoglieri A, Provyn S, Bautmans I, Van Roy P, Clarys JP,. Direct relationship of body mass index and waist circumference with body tissue distribution in elderly persons. J Nutr Health Aging. 2011; 15 (10): 924-931.
62. Schueller-Weidekamm C, Schueller G, Uffmann M, Bader T,. Incidence of chronic knee lesions in long-distance runners based on training level: findings at MRI. Eur J Radiol. 2006; 58 (2): 286-293.
63. Segal NA, Kern AM, Anderson DD, et al. Elevated tibiofemoral articular contact stress predicts risk for bone marrow lesions and cartilage damage at 30 months. Osteoarthritis Cartilage. 2012; 20 (10): 1120-1126.
64. Stahl R, Luke A, Ma CB, et al. Prevalence of pathologic findings in asymptomatic knees of marathon runners before and after a competition in comparison with physically active subjects: a 3.0 T magnetic resonance imaging study. Skeletal Radiol. 2008; 37 (7): 627-638.
65. Stehling C, Lane NE, Nevitt MC, Lynch J, McCulloch CE, Link TM,. Subjects with higher physical activity levels have more severe focal knee lesions diagnosed with 3 T MRI: analysis of a non-symptomatic cohort of the Osteoarthritis Initiative. Osteoarthritis Cartilage. 2010; 18 (6): 776-786.
66. Tanamas SK, Wluka AE, Pelletier JP, et al. Bone marrow lesions in people with knee osteoarthritis predict progression of disease and joint replacement: a longitudinal study. Rheumatology (Oxford). 2010; 49 (12): 2413-2419.
67. Thorp LE, Wimmer MA, Block JA, et al. Bone mineral density in the proximal tibia varies as a function of static alignment and knee adduction angular momentum in individuals with medial knee osteoarthritis. Bone. 2006; 39 (5): 1116-1122.
68. Wallace BC, Schmid CH, Lau J, Trikalinos TA,. Meta-Analyst: software for meta-analysis of binary, continuous and diagnostic data. BMC Med Res Methodol. 2009; 9: 80.
69. Wang Y, Wluka AE, Pelletier JP, et al. Meniscal extrusion predicts increases in subchondral bone marrow lesions and bone cysts and expansion of subchondral bone in osteoarthritic knees. Rheumatology (Oxford). 2010; 49 (5): 997-1004.
70. Wiegant K, van Roermund PM, Intema F, et al. Sustained clinical and structural benefit after joint distraction in the treatment of severe knee osteoarthritis. Osteoarthritis Cartilage. 2013; 21 (11): 1660-1667.
71. 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 (3): 835-840.
72. Zhai G, Blizzard L, Srikanth V, et al. Correlates of knee pain in older adults: Tasmanian Older Adult Cohort Study. Arthritis Rheum. 2006; 55 (2): 264-271.
73. Zhai G, Stankovich J, Cicuttini F, Ding C, Jones G,. Familial, structural, and environmental correlates of MRI-defined bone marrow lesions: a sibpair study. Arthritis Res Ther. 2006; 8 (4): R137.
74. Zhang Y, Nevitt M, Niu J, et al. Fluctuation of knee pain and changes in bone marrow lesions, effusions, and synovitis on magnetic resonance imaging. Arthritis Rheum. 2011; 63 (3): 691-699.