Skip to main content
Top
Published in: Arthritis Research & Therapy 1/2015

Open Access 01-12-2015 | Research article

Bone marrow lesions can be subtyped into groups with different clinical outcomes using two magnetic resonance imaging (MRI) sequences

Authors: Anita E. Wluka, Andrew J. Teichtahl, Rheza Maulana, Bonnie M. Liu, Yuanyuan Wang, Graham G. Giles, Richard O’Sullivan, David Findlay, Flavia M. Cicuttini

Published in: Arthritis Research & Therapy | Issue 1/2015

Login to get access

Abstract

Introduction

Bone marrow lesions (BMLs) are features detected on MRI that are important in the pathogenesis of knee osteoarthritis. Since BMLs reflect heterogeneous pathologies this prospective cohort study examined whether BMLs detected using different MRI sequences are associated with distinct structural and clinical endpoints.

Methods

A total of 297 community-based adults without knee pain were examined to identify BMLs visualised using three-dimensional T1-weighted gradient-echo fat-suppressed (T1-weighted sequences) fat-suppressed and fat-saturated FSE T2-weighted MRI sequences (T2-weighted sequences) at baseline. Cartilage volume was measured at baseline and follow-up, while incident knee pain was assessed at follow-up, an average of 2.3 years later.

Results

At baseline, 46 BMLs were visualised in 39 participants. Of the 45 BMLs visualised on T2-weighted sequences, 34 (74 %) were also seen on T1-weighted sequences. One BML was seen on only T1-weighted sequences. Knees with BMLs visualised on both T1- and T2-weighted sequences had significantly higher medial tibial cartilage volume loss (45 mm3/annum, standard error of the mean (SEM) 14) than those with BMLs identified on only T2-weighted sequences (−13 mm3/annum SEM 19), after adjustment for age, gender and body mass index (p = 0.01). Incident knee pain was more likely in individuals with BMLs in the medial compartment visualised on both T1- and T2-weighted (eight participants, 53 %) compared to those with BMLs on only T2-weighted sequences (0 %) or no BMLs (76 participants, 31 %, p = 0.02).

Conclusions

BMLs present on both T1- and T2-weighted MRI sequences were associated with increased medial tibial cartilage loss and incident knee pain compared with those BMLs seen only on T2-weighted sequences. This suggests that combining different MRI sequences may provide more informative targets in the prevention and treatment of knee osteoarthritis.
Literature
1.
go back to reference Felson DT, Chaisson CE, Hill CL, Totterman SM, Gale ME, Skinner KM, et al. The association of bone marrow lesions with pain in knee osteoarthritis. Ann Intern Med. 2001;134:541–9.CrossRefPubMed Felson DT, Chaisson CE, Hill CL, Totterman SM, Gale ME, Skinner KM, et al. The association of bone marrow lesions with pain in knee osteoarthritis. Ann Intern Med. 2001;134:541–9.CrossRefPubMed
2.
go back to reference Davies-Tuck ML, Wluka AE, Wang Y, English DR, Giles GG, Cicuttini F. The natural history of bone marrow lesions in community-based adults with no clinical knee osteoarthritis. Ann Rheum Dis. 2009;68:904–8.CrossRefPubMed Davies-Tuck ML, Wluka AE, Wang Y, English DR, Giles GG, Cicuttini F. The natural history of bone marrow lesions in community-based adults with no clinical knee osteoarthritis. Ann Rheum Dis. 2009;68:904–8.CrossRefPubMed
3.
go back to reference Dore D, Martens A, Quinn S, Ding C, Winzenberg T, Zhai G, et al. Bone marrow lesions predict site-specific cartilage defect development and volume loss: a prospective study in older adults. Arthritis Res Ther. 2010;12:R222.PubMedCentralCrossRefPubMed Dore D, Martens A, Quinn S, Ding C, Winzenberg T, Zhai G, et al. Bone marrow lesions predict site-specific cartilage defect development and volume loss: a prospective study in older adults. Arthritis Res Ther. 2010;12:R222.PubMedCentralCrossRefPubMed
4.
go back to reference Wluka AE, Hanna F, Davies-Tuck M, Wang Y, Bell RJ, Davis SR, et al. Bone marrow lesions predict increase in knee cartilage defects and loss of cartilage volume in middle-aged women without knee pain over 2 years. Ann Rheum Dis. 2009;68:850–5.CrossRefPubMed Wluka AE, Hanna F, Davies-Tuck M, Wang Y, Bell RJ, Davis SR, et al. Bone marrow lesions predict increase in knee cartilage defects and loss of cartilage volume in middle-aged women without knee pain over 2 years. Ann Rheum Dis. 2009;68:850–5.CrossRefPubMed
5.
go back to reference Felson DT, McLaughlin S, Goggins J, LaValley MP, Gale ME, Totterman S, et al. Bone marrow edema and its relation to progression of knee osteoarthritis. Ann Intern Med. 2003;139:330–6.CrossRefPubMed Felson DT, McLaughlin S, Goggins J, LaValley MP, Gale ME, Totterman S, et al. Bone marrow edema and its relation to progression of knee osteoarthritis. Ann Intern Med. 2003;139:330–6.CrossRefPubMed
6.
go back to reference Raynauld JP, Martel-Pelletier J, Haraoui B, Choquette D, Dorais M, Wildi LM, et al. Risk factors predictive of joint replacement in a 2-year multicentre clinical trial in knee osteoarthritis using MRI: results from over 6 years of observation. Ann Rheum Dis. 2011;70:1382–8. doi:10.1136/ard.2010.146407.CrossRefPubMed Raynauld JP, Martel-Pelletier J, Haraoui B, Choquette D, Dorais M, Wildi LM, et al. Risk factors predictive of joint replacement in a 2-year multicentre clinical trial in knee osteoarthritis using MRI: results from over 6 years of observation. Ann Rheum Dis. 2011;70:1382–8. doi:10.​1136/​ard.​2010.​146407.CrossRefPubMed
7.
go back to reference Tanamas SK, Wluka AE, Pelletier JP, Pelletier JM, Abram F, Berry PA, et al. Bone marrow lesions in people with knee osteoarthritis predict progression of disease and joint replacement: a longitudinal study. Rheumatology. 2010;49:2413–9.CrossRefPubMed Tanamas SK, Wluka AE, Pelletier JP, Pelletier JM, Abram F, Berry PA, et al. Bone marrow lesions in people with knee osteoarthritis predict progression of disease and joint replacement: a longitudinal study. Rheumatology. 2010;49:2413–9.CrossRefPubMed
8.
go back to reference Hayashi D, Guermazi A, Kwoh CK, Hannon MJ, Moore C, Jakicic JM, et al. Semiquantitative assessment of subchondral bone marrow edema-like lesions and subchondral cysts of the knee at 3T MRI: a comparison between intermediate-weighted fat-suppressed spin echo and Dual Echo Steady State sequences. BMC Musculoskelet Disord. 2011;12:198. doi:10.1186/1471-2474-1112-1198.PubMedCentralCrossRefPubMed Hayashi D, Guermazi A, Kwoh CK, Hannon MJ, Moore C, Jakicic JM, et al. Semiquantitative assessment of subchondral bone marrow edema-like lesions and subchondral cysts of the knee at 3T MRI: a comparison between intermediate-weighted fat-suppressed spin echo and Dual Echo Steady State sequences. BMC Musculoskelet Disord. 2011;12:198. doi:10.​1186/​1471-2474-1112-1198.PubMedCentralCrossRefPubMed
9.
go back to reference Zanetti M, Bruder E, Romero J, Hodler J. Bone marrow edema pattern in osteoarthritic knees: correlation between MR imaging and histologic findings. Radiology. 2000;215:835–40.CrossRefPubMed Zanetti M, Bruder E, Romero J, Hodler J. Bone marrow edema pattern in osteoarthritic knees: correlation between MR imaging and histologic findings. Radiology. 2000;215:835–40.CrossRefPubMed
10.
go back to reference Hunter DJ, Gerstenfeld L, Bishop G, Davis AD, Mason ZD, Einhorn TA, et al. Bone marrow lesions from osteoarthritis knees are characterized by sclerotic bone that is less well mineralized. Arthritis Res Ther. 2009;11:R11. doi:10.1186/ar2601.PubMedCentralCrossRefPubMed Hunter DJ, Gerstenfeld L, Bishop G, Davis AD, Mason ZD, Einhorn TA, et al. Bone marrow lesions from osteoarthritis knees are characterized by sclerotic bone that is less well mineralized. Arthritis Res Ther. 2009;11:R11. doi:10.​1186/​ar2601.PubMedCentralCrossRefPubMed
11.
go back to reference Modic MT, Steinberg PM, Ross JS, Masaryk TJ, Carter JR. Degenerative disk disease: assessment of changes in vertebral body marrow with MR imaging. Radiology. 1988;166:193–9.CrossRefPubMed Modic MT, Steinberg PM, Ross JS, Masaryk TJ, Carter JR. Degenerative disk disease: assessment of changes in vertebral body marrow with MR imaging. Radiology. 1988;166:193–9.CrossRefPubMed
12.
go back to reference Kuisma M, Karppinen J, Niinimaki J, Ojala R, Haapea M, Heliovaara M, et al. Modic changes in endplates of lumbar vertebral bodies: prevalence and association with low back and sciatic pain among middle-aged male workers. Spine. 2007;32:1116–22.CrossRefPubMed Kuisma M, Karppinen J, Niinimaki J, Ojala R, Haapea M, Heliovaara M, et al. Modic changes in endplates of lumbar vertebral bodies: prevalence and association with low back and sciatic pain among middle-aged male workers. Spine. 2007;32:1116–22.CrossRefPubMed
13.
go back to reference Mitra D, Cassar-Pullicino VN, McCall IW. Longitudinal study of vertebral type-1 end-plate changes on MR of the lumbar spine. Eur Radiol. 2004;14:1574–81.CrossRefPubMed Mitra D, Cassar-Pullicino VN, McCall IW. Longitudinal study of vertebral type-1 end-plate changes on MR of the lumbar spine. Eur Radiol. 2004;14:1574–81.CrossRefPubMed
14.
go back to reference Toyone T, Takahashi K, Kitahara H, Yamagata M, Murakami M, Moriya H. Vertebral bone-marrow changes in degenerative lumbar disc disease. An MRI study of 74 patients with low back pain. J Bone Joint Surg Br. 1994;76:757–64.PubMed Toyone T, Takahashi K, Kitahara H, Yamagata M, Murakami M, Moriya H. Vertebral bone-marrow changes in degenerative lumbar disc disease. An MRI study of 74 patients with low back pain. J Bone Joint Surg Br. 1994;76:757–64.PubMed
16.
go back to reference Bram J, Zanetti M, Min K, Hodler J. MR abnormalities of the intervertebral disks and adjacent bone marrow as predictors of segmental instability of the lumbar spine. Acta Radiol. 1998;39:18–23.CrossRefPubMed Bram J, Zanetti M, Min K, Hodler J. MR abnormalities of the intervertebral disks and adjacent bone marrow as predictors of segmental instability of the lumbar spine. Acta Radiol. 1998;39:18–23.CrossRefPubMed
17.
18.
19.
go back to reference Weishaupt D, Zanetti M, Hodler J, Boos N. MR imaging of the lumbar spine: prevalence of intervertebral disk extrusion and sequestration, nerve root compression, end plate abnormalities, and osteoarthritis of the facet joints in asymptomatic volunteers. Radiology. 1998;209:661–6.CrossRefPubMed Weishaupt D, Zanetti M, Hodler J, Boos N. MR imaging of the lumbar spine: prevalence of intervertebral disk extrusion and sequestration, nerve root compression, end plate abnormalities, and osteoarthritis of the facet joints in asymptomatic volunteers. Radiology. 1998;209:661–6.CrossRefPubMed
20.
go back to reference Modic MT, Masaryk TJ, Ross JS, Carter JR. Imaging of degenerative disk disease. Radiology. 1988;168:177–86.CrossRefPubMed Modic MT, Masaryk TJ, Ross JS, Carter JR. Imaging of degenerative disk disease. Radiology. 1988;168:177–86.CrossRefPubMed
22.
go back to reference Yoshioka H, Stevens K, Hargreaves BA, Steines D, Genovese M, Dillingham MF, et al. Magnetic resonance imaging of articular cartilage of the knee: comparison between fat-suppressed three-dimensional SPGR imaging, fat-suppressed FSE imaging, and fat-suppressed three-dimensional DEFT imaging, and correlation with arthroscopy. J Magn Reson Imaging. 2004;20:857–64.CrossRefPubMed Yoshioka H, Stevens K, Hargreaves BA, Steines D, Genovese M, Dillingham MF, et al. Magnetic resonance imaging of articular cartilage of the knee: comparison between fat-suppressed three-dimensional SPGR imaging, fat-suppressed FSE imaging, and fat-suppressed three-dimensional DEFT imaging, and correlation with arthroscopy. J Magn Reson Imaging. 2004;20:857–64.CrossRefPubMed
23.
go back to reference Duc SR, Koch P, Schmid MR, Horger W, Hodler J, Pfirrmann CW. Diagnosis of articular cartilage abnormalities of the knee: prospective clinical evaluation of a 3D water-excitation true FISP sequence. Radiology. 2007;243:475–82.CrossRefPubMed Duc SR, Koch P, Schmid MR, Horger W, Hodler J, Pfirrmann CW. Diagnosis of articular cartilage abnormalities of the knee: prospective clinical evaluation of a 3D water-excitation true FISP sequence. Radiology. 2007;243:475–82.CrossRefPubMed
24.
go back to reference Tanamas SK, Wluka AE, Pelletier JP, Pelletier JM, Abram F, Berry PA, et al. Bone marrow lesions in people with knee osteoarthritis predict progression of disease and joint replacement: a longitudinal study. Rheumatology (Oxford). 2010;49:2413–9. doi:10.1093/rheumatology/keq2286.CrossRef Tanamas SK, Wluka AE, Pelletier JP, Pelletier JM, Abram F, Berry PA, et al. Bone marrow lesions in people with knee osteoarthritis predict progression of disease and joint replacement: a longitudinal study. Rheumatology (Oxford). 2010;49:2413–9. doi:10.​1093/​rheumatology/​keq2286.CrossRef
25.
go back to reference Giles GG, English DR. The Melbourne Collaborative Cohort Study. IARC Sci Publ. 2002;156:69–70.PubMed Giles GG, English DR. The Melbourne Collaborative Cohort Study. IARC Sci Publ. 2002;156:69–70.PubMed
26.
go back to reference Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, 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;29:1039–49.CrossRefPubMed Altman R, Asch E, Bloch D, Bole G, Borenstein D, Brandt K, 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;29:1039–49.CrossRefPubMed
27.
go back to reference Hanna F, Teichtahl A, Bell R, Davis S, Wluka A, O'Sullivan R, et al. The cross-sectional relationship between fortnightly exercise and knee cartilage properties in healthy adult women in midlife. Menopause. 2007;14:830–4.CrossRefPubMed Hanna F, Teichtahl A, Bell R, Davis S, Wluka A, O'Sullivan R, et al. The cross-sectional relationship between fortnightly exercise and knee cartilage properties in healthy adult women in midlife. Menopause. 2007;14:830–4.CrossRefPubMed
28.
go back to reference McAlindon TE, Watt I, McCrae F, Goddard P, Dieppe PA. Magnetic resonance imaging in osteoarthritis of the knee: correlation with radiographic and scintigraphic findings. Ann Rheum Dis. 1991;50:14–9.PubMedCentralCrossRefPubMed McAlindon TE, Watt I, McCrae F, Goddard P, Dieppe PA. Magnetic resonance imaging in osteoarthritis of the knee: correlation with radiographic and scintigraphic findings. Ann Rheum Dis. 1991;50:14–9.PubMedCentralCrossRefPubMed
29.
go back to reference Wluka AE, Wang Y, Davies-Tuck M, English DR, Giles GG, Cicuttini FM. Bone marrow lesions predict progression of cartilage defects and loss of cartilage volume in healthy middle-aged adults without knee pain over 2 yrs. Rheumatology (Oxford). 2008;47:1392–6.CrossRef Wluka AE, Wang Y, Davies-Tuck M, English DR, Giles GG, Cicuttini FM. Bone marrow lesions predict progression of cartilage defects and loss of cartilage volume in healthy middle-aged adults without knee pain over 2 yrs. Rheumatology (Oxford). 2008;47:1392–6.CrossRef
31.
go back to reference Cicuttini FM, Wluka AE, Wang Y, Stuckey SL. Longitudinal study of changes in tibial and femoral cartilage in knee osteoarthritis. Arthritis Rheumat. 2004;50:94–7.CrossRefPubMed Cicuttini FM, Wluka AE, Wang Y, Stuckey SL. Longitudinal study of changes in tibial and femoral cartilage in knee osteoarthritis. Arthritis Rheumat. 2004;50:94–7.CrossRefPubMed
32.
go back to reference Ding C, Garnero P, Cicuttini F, Scott F, Cooley H, Jones G. Knee cartilage defects: association with early radiographic osteoarthritis, decreased cartilage volume, increased joint surface area and type II collagen breakdown. Osteoarthritis Cartilage. 2005;13:198–205.CrossRefPubMed Ding C, Garnero P, Cicuttini F, Scott F, Cooley H, Jones G. Knee cartilage defects: association with early radiographic osteoarthritis, decreased cartilage volume, increased joint surface area and type II collagen breakdown. Osteoarthritis Cartilage. 2005;13:198–205.CrossRefPubMed
34.
go back to reference Calvo E, Palacios I, Delgado E, Ruiz-Cabello J, Hernandez P, Sanchez-Pemaute O, et al. High-resolution MRI detects cartilage swelling at the early stages of experimental osteoarthritis. Osteoarthritis Cartilage. 2001;9:463–72.CrossRefPubMed Calvo E, Palacios I, Delgado E, Ruiz-Cabello J, Hernandez P, Sanchez-Pemaute O, et al. High-resolution MRI detects cartilage swelling at the early stages of experimental osteoarthritis. Osteoarthritis Cartilage. 2001;9:463–72.CrossRefPubMed
35.
go back to reference Felson DT, Niu J, Guermazi A, Roemer F, Aliabadi P, Clancy M, et al. Correlation of the development of knee pain with enlarging bone marrow lesions on magnetic resonance imaging. Arthritis Rheum. 2007;56:2986–92.CrossRefPubMed Felson DT, Niu J, Guermazi A, Roemer F, Aliabadi P, Clancy M, et al. Correlation of the development of knee pain with enlarging bone marrow lesions on magnetic resonance imaging. Arthritis Rheum. 2007;56:2986–92.CrossRefPubMed
36.
go back to reference Bollet AJ. Edema of the bone marrow can cause pain in osteoarthritis and other diseases of bone and joints. Ann Intern Med. 2001;134:591–3.CrossRefPubMed Bollet AJ. Edema of the bone marrow can cause pain in osteoarthritis and other diseases of bone and joints. Ann Intern Med. 2001;134:591–3.CrossRefPubMed
37.
go back to reference Hunter DJ, Zhang Y, Niu J, Goggins J, Amin S, LaValley MP, et al. Increase in bone marrow lesions associated with cartilage loss: a longitudinal magnetic resonance imaging study of knee osteoarthritis. Arthritis Rheum. 2006;54:1529–35.CrossRefPubMed Hunter DJ, Zhang Y, Niu J, Goggins J, Amin S, LaValley MP, et al. Increase in bone marrow lesions associated with cartilage loss: a longitudinal magnetic resonance imaging study of knee osteoarthritis. Arthritis Rheum. 2006;54:1529–35.CrossRefPubMed
38.
go back to reference Raynauld JP, Martel-Pelletier J, Berthiaume MJ, Abram F, Choquette D, Haraoui B, et al. Correlation between bone lesion changes and cartilage volume loss in patients with osteoarthritis of the knee as assessed by quantitative magnetic resonance imaging over a 24-month period. Ann Rheum Dis. 2008;67:683–8.CrossRefPubMed Raynauld JP, Martel-Pelletier J, Berthiaume MJ, Abram F, Choquette D, Haraoui B, et al. Correlation between bone lesion changes and cartilage volume loss in patients with osteoarthritis of the knee as assessed by quantitative magnetic resonance imaging over a 24-month period. Ann Rheum Dis. 2008;67:683–8.CrossRefPubMed
Metadata
Title
Bone marrow lesions can be subtyped into groups with different clinical outcomes using two magnetic resonance imaging (MRI) sequences
Authors
Anita E. Wluka
Andrew J. Teichtahl
Rheza Maulana
Bonnie M. Liu
Yuanyuan Wang
Graham G. Giles
Richard O’Sullivan
David Findlay
Flavia M. Cicuttini
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2015
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/s13075-015-0780-5

Other articles of this Issue 1/2015

Arthritis Research & Therapy 1/2015 Go to the issue