DEGENERATIVE LUMBAR DISC DISEASE

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1 VERTEBRAL BONE-MARROW CHANGES IN DEGENERATIVE LUMBAR DISC DISEASE AN MRI STUDY OF 74 PATIENTS WITh LOW BACK PAIN T. TOYONE, K. TAKAHASHI, H. KITAHARA, M. YAMAGATA, M. MURAKAMI, H. MORIYA From Chiba University, Japan We carried out MM studies of 74 patients with endplate and vertebral bone-marrow changes associated with degenerative lumbar disc disease. Abnormalities were classified into type A, with decreased signal intensities, and type B, with increased signal intensities on Ti-weighted spin-echo images. Twenty-seven (73 %) of the 37 patients with type- A changes had low back pain, in contrast to only four (1 1 %) of the 37 patients with type-b changes. Lateral flexion-extension radiographs showed hypermobility in 26 patients (70%) with type-a changes, and in only six (16%) with type-b changes. Type-A changes correlated with segmental hypermobility and low back pain, while type-b changes were more common in patients with stable degenerative disc disease. J BoneJoint Surg [Br] 1994; 76-B: Received 21 December 1993; Accepted after revision 14 March 1994 Bone remodelling is thought to be induced by changes in the mechanical stress on vertebral bodies caused by degenerative disc disease. Such stresses could also result in pathological changes in the vertebra! bone marrow, but we could find few published reports of such studies. MRI is used to detect bone-marrow abnormalities. de Roos et a! (1987) have described marrow changes adjacent to degenerative intervertebral discs in 29 patients and Modic et a! (1988a) described two types of change in signal intensity in such bone marrow in five patients. Type 1, with decreased signal intensity on Ti-weighted spin-echo images and increased signal intensity on the T2-weighted images, subsequently changed to type 2, with increased signal intensity on Ti-weighted images and isointense or slightly increased signal intensity on T2-weighted images. Lang et a! (1990) studied 33 patients after lumbar fusion and found high signal intensities on Ti-weighted images in the 16 patients with a solid fusion. Neither the mechanism nor the clinical significance, however, was established. We have used MRI to investigate the clinical significance of the changes in the vertebral bone marrow in degenerative disc disease. PATIENTS AND METhODS We reviewed MR images of the lumbar spines of 500 patients with degenerative disc disease and chronic low back pain, seen at Chiba University from April 1990 to March Disc degeneration was identified by the decreased signal intensity ofthe nucleus and inner annulus on T2-weighted images (Gibson et a! i986). We analysed results from 1500 disc levels (L3-L4 to L5-S1), finding disc degeneration at 822 levels. Of these, 94 patients (19%) had focal alterations in the end plate and marrow adjacent to a degenerative disc (Fig. 1). We excluded T. Toyone, MD, Orthopaedic Surgeon K. Takahashi, MD, Consultant Orthopaedic Surgeon H. Kitahara, MD, Associate Professor M. Yamagata, MD, Consultant Orthopaedic Surgeon M. Murakami, MD, Consultant Orthopaedic Surgeon H. Moriya, MD, Professor and Chairman Departmentof Orthopaedic Surgery, School of Medicine, Chiba University, Inohana, Chuo-ku, Chiba 260, Japan. Correspondence should be sent to Dr T. Toyone at the Department of Orthopaedic Surgery, Kimitsu Chuo Hospital, 1010 Sakurai, Kisarazu City, Chiba 292, Japan British Editorial Society of Bone and Joint Surgery X/94/5851 $2.00 Number of degenerative discs - Number of end-plate changes Fig. 1 The levels and frequency of disc degeneration and end-plate changes in 500 patients with low back pain. Seventy-four of the 94 with end-plate changes were studied in detail. VOL. 76-B, No. 5, SEPTEMBER

2 760 T. TOYONE, K. TAKAHASHI, H. KITAHARA, LIT AL Fig. 3d Dl and D2 - High-power photomicrographs showing thickened bone trabeculae (1) and vascularised fibrous marrow (2) (haematoxylin and eosin x90). D3 and D4 - A thickened cartilaginous end plate (3) is compared with the normal tide-mark of the end plate (4) (Safranin-O x90). Fig. 4 MRI of a patient (case 10) with low back pain who initially had type-a changes, which subsequently changed to type-b. A - Ti-weighted sagittal MRI on 12 October 1990 showing decreased signal intensity within the marrow of L5/S1. B - Ti-weighted sagittal MRI on 25 September 1992 showing increased intensity. in the T2-weighted images in patients with decreased signal intensity on Ti-weighted images. The clinical significance of this is not evident (Fig. 5). For our study therefore we included patients with Modic type-i and type-3 changes in our type A. Ross and Modic (1992) reported that the association of these changes with degenerative disc disease, regardless of symptomato!ogy, is obscure, and we could find no report of any association between MRI changes in vertebral bone marrow and symptoms or radiographic hypermobility. MRI cannot provide information on mechanical parameters, but we have found a clear correlation between the marrow changes on Ti-weighted images and the incidence of low back pain and segmental hypermobility. Histologically, type-a lesions were associated with thickened bony trabeculae and fibrovascularbone marrow, indicating injury and repair of the vertebral end plates, but type-b lesions with increased signal intensity on the Ti-weighted spin-echo images were associated with fatty replacement of the marrow. The latter changes are common in patients with late-stage degenerative disc disease, and may represent the restabilisation phase described by Kirkaldy-Willis and Farfan (1982). Lumbar segmental instability has been studied extensively, but the underlying pathophysiology is unknown. Knutsson (1944) used lateral flexion-extension radiographs to show that anterior translation of more than 3 mm was an early sign of instability, but Hayes et a! (1988) have questioned the reliability of flexion-extension examinations as primary determinants of instability. They report a wide range of motion abnormalities with a significant overlap between asymptomatic and symptomatic patients. Ashton-Miller and Schultz (i99i) have redefined instability as a large deformation of an already ThE JOURNAL OF BONE AND JOINT SURGERY

3 VERTEBRAL BONE-MARROW CHANGES IN DEGENERATIVE LUMBAR DISC DISEASE 761 Table II. Details of 37 patients with type-a end-plate and bone-marrow changes on MRI Age Level Case Sex (yr) of lesion Low back Leg AP pain pain translation Treatment 1 M 43 L4-L M Si F 57 L4-L M 60 LA-L M 49 L4-L M 26 L3-L F 58 L4-L M 35 L4-L M 59 L4-L F 49 L4-L M 1 7 L4-L5 12 M 32 L4-L M 46 L3-L F 44 li-si M 48 L4-L M 63 L4-L F 70 L4-L F 65 L5-S F Si + 20 M 65 L5-Sl M 17 L5-S F 50 L5-S F 16 L5-S F 40 L5-S1 + Decompression 25 F 13 L5-S F 26 L5-S F 63 L4-L F si M 48 [5-Si M Si F 46 L.5-S Decompression 32 F 65 L.5-S M 51 L5-S F 53 li-si M 65 L3-L4, L4.-L M 41 L3-L4, L4-L M 60 L3-L4 - + VOL 76-B, No. 5, SEPTEMBER 1994

4 762 T. TOYONE, K. TAKAHASHI, H. KITAHARA, cr t Table Ill. Details of 37 patients with type-b end-plate and bone-marrow changes on MRI Age Level of Low back Leg AP Case Sex (yr) lesion pain pain translation Treatment 38 F 57 L5-5l 39 F 50 L.5-Si M 56 L3-L M 45 LA-L5-42 F 42 L4-L F 45 IA-L5, L5-S1 44 F 64 LA-ES, 13-si 45 M 37 L5-S1 - + Decompression 46 M 62 L4-L5 + - Decompression 47 F Si F 67 L5-S M 47 L4-L5-50 F 44 L4-L F 44 L4-L F 39 L4-L F 52 L3-L F 68 L4-L M 63 L4-L5 + Decompression 56 F 55 L3-L4, LA-L F 64 L4-L F 54 L F 70 L.5-Sl - 60 M Si + 61 M 48 L.5-Sl F 39 L Decompression 63 M F 68 L4-L F 31 L5-S1 + - Decompression 66 M 67 L4-L5 67 M F 42 L3-L4, L4-L5-69 M 64 L3-L4-70 F 49 L4-L M 57 L3-L4 + + Decompression 72 M 67 L3-L4-73 F 40 L4-L F 54 L5-S1 + - THE JOURNAL OF BONE AND JOINT SURGERY

5 VERTEBRAL BONE-MARROW CHANGES IN DEGENERATIVE LUMBAR DISC DISEASE 763 Variations in the MRI appearance in patients with type-a changes. A - Ti-weighted sagittal image showing low signal intensity within the marrow of L4/L5. B - T2-weighted image showing increased signal intensity (case 12). C - Ti-weighted image showing decreased signal intensity in 13 and Si bodies. D - 12-weighted image showing an end plate with decreased signal intensity surrounded by increased signal intensity (case 29). Fig. 5 loaded structure by a small additional load, and consider that slightly increased flexibility cannot be thought of as unstable. Because of these arguments, we have used the term segmental hypermobility rather than the more ambiguous term, instability. Many attempts have been made to correlate radiographic spine abnormalities with symptoms, beginning with early Swedish studies of industrial workers (Hult 1954). MRI can now provide additional information about the vertebral end plates and bone marrow, and we have now related changes in these structures to the presence of low back pain and segmental hypermobility. The latter is associated with decreased signal intensity on Ti-weighted spin-echo images of the bone marrow adjacent to the disc space; stable degenerative disc disease is associated with increased signal intensity on Ti-weighted spin-echo images. Our findings provide little insight into the mechanisms linking stress to bone marrow changes, but may help to elucidate the pathogenesis of segmental hypermobility. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. REFERENCES Ashton-Miller ia, Schultz AB. Spine instability and segmental hypermobility biomechanics: a call for the definition and standard use of terms. Seminars in Spine Surgery 1991; 3: Boden SD, Wiesel SW. Lumbosacral segmental motion in normal individuals: have we been measuring instability properly? Spine 1990; 15: Dupuis PR, Yong-Hing K, Cassidy JD, Kirkaldy-Willis WH. Radiologic diagnosis of degenerative lumbar spinal instability. Spine 1985; io: Gibson Mi, Buckley J, Mawhinaey R, Mulhollaad RC, Worthington BS. Magnetic resonance imaging and discography in the diagnosis of disc degeneration.j BoneJoint Surg [Br] 1986; 68-B: VOL. 76-B, No. 5, SEPTEMBER 1994

6 764 T. TOYONE, K. TAKAHASHI, H. KITAHARA, sr AL Hayes MA, Howard TC, Gruel CR, Kopta JA. Roentgenographic McCoy CE, Selby D, Henderson R, et al. JOA scale and assessment of evaluation of lumbar spine flexion-extension in asymptomatic individ- surgical outcome. Proc International Society for Study of the Lumbar uals. Spine 1988; 14: Spine, Chicago, May 1992:56-7. Hult L. Cervical, dorsal and lumbar spinal syndromes. Acta Orthop Scand Modic MT Masaryk Ti, Ross is, Carter JR. Imaging of degenerative 1954; 24: disk disease. Radio/ogy 1988a; 168: Modic MT, Steinberg PM, Ross is, et al. Degenerative disk disease: Izumida S, Inoue S. Assessment of treatment for low back pain. J Jpn assessment of changes in vertebral body marrow with MR imaging. OrthopAssoc 1986; 60: Radio/ogy 1988b; 166: Janevic J, Ashton-Miller JA, Schultz AB. Large compressive preloads Morgan FP, King T. Primary instability of lumbar vertebrae as a common decrease lumbar motion segment flexibility. J Orthop Res 1991; 9: cause oflow back pain.j BoneJointSurg [Br] 1957; 39-B: de Roos A, Kressel H, Spritzer C, Dalinka M. MR imaging of marrow Kirkaldy-Willis WH, Farfan HF. Instability of the lumbar spine. C/in changes adjacent to end plates in degenerative lumbar disk disease. Orthop 1982; 165: AiR 1987; 149: Ross is, Modic MT. Current assessment of spinal degenerative disease Knutsson F. The instability associated with disk degeneration in the lumbar with magnetic resonance imaging. C/in Orthop 1992; 279: spine. Acta Radio/ 1944; 25: Shaffer WO, Spratt KF, Weinstein J, Lehmann TR, Goel V. The Lang P, Chafetz N, Genant HK, Morris JM. Lumbar spinal fusion: consistency and accuracy of roentgenograms for measuring sagittal assessment of functional stability with magnetic resonance imaging. translation in the lumbar vertebral motion segment: an experimental Spine 1990; 15: model. Spine 1990; 15: ThE JOURNAL OF BONE AND JOINT SURGERY

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