Low Back Pain in Relation to Lumbar Disc Degeneration

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1 SPINE Volume 25, Number 4, pp , Lippincott Williams & Wilkins, Inc. Low Back Pain in Relation to Lumbar Disc Degeneration Katariina Luoma, MD,* Hilkka Riihimäki, DMedSc, MSc,* Ritva Luukkonen, PhD,* Raili Raininko, MD, DMedSc, Eira Viikari-Juntura, MD, DMedSc,* and Antti Lamminen, MD, DMedSc Study Design. Cross-sectional magnetic resonance imaging (MRI) study. Objectives. To study the relation of low back pain (LBP) to disc degeneration in the lumbar spine. Background Data. Controversy still prevails about the relationship between disc degeneration and LBP. Classification of disc degeneration and symptoms varies, hampering comparison of study results. Methods. Subjects comprised 164 men aged years 53 machine drivers, 51 construction carpenters, and 60 office workers. The data of different types of LBP, individual characteristics, and lifestyle factors were obtained from a questionnaire and a structured interview. Degeneration of discs L2/L3 L5/S1 (dark nucleus pulposus and posterior and anterior bulge) was assessed with MRI. Results. An increased risk of LBP (including all types) was found in relation to all signs of disc degeneration. An increased risk of sciatic pain was found in relation to posterior bulges, but local LBP was not related to disc degeneration. The risks of LBP and sciatic pain were strongly affected by occupation. Conclusions. Low back pain is associated with signs of disc degeneration and sciatic pain with posterior disc bulges. Low back pain is strongly associated with occupation. [Key words: intervertebral disc abnormalities, work-related risk factors, low back pain, epidemiology, occupational load] Spine 2000;25: Disc degeneration of the lumbar spine is considered as one of the underlying factors of low back pain (LBP), but controversy still prevails about their relationship. An association between radiographic film findings and LBP has been found in many cross-sectional population studies, but not in many case-referent studies, and there is no firm evidence of the presence or absence of a causal relationship between radiographic findings and nonspecific LBP. 29 In some magnetic resonance imaging (MRI) studies an association has been found, 6,19,27 but degenerative changes have been found to be common in asymptomatic people as well. 2,10,20 In most studies the temporal relationship between the radiologic findings and the symptoms is obscure. Little is From the *Finnish Institute of al Health, Helsinki, Finland; Uppsala University, Uppsala, Sweden; Helsinki University Central Hospital, Helsinki, Finland. This work has been supported by the Work Environment Fund, Finland. Acknowledgment date: March 17, Acceptance date: May 26, Device status category: 1. Conflict of interest category: 14. known about the effect of occupation on the association between LBP and disc degeneration. There is no generally accepted classification for LBP. Variation in the criteria for disc degeneration and nonspecificity of the symptoms may partly explain differences between the results of epidemiologic studies. In this study, we have analyzed three signs of disc degeneration separately: signal intensity of the nucleus pulposus and anterior and posterior bulges of the disc. We have studied the associations of disc degeneration of the lumbar spine with different types of LBP. Subjects and Methods Subjects. The primary cohort consisted of yearold men 688 machine drivers, 553 carpenters, and 591 office workers, who had participated 7 and 4 years before the present study in questionnaire studies concerning occupational effects on LBP. 21,23 The subjects of this study were a subgroup of the cohort selected, using age (40 45 years) and place of residence as inclusion criteria. The participation rate was 71%. The final study group comprised 53 machine operators, 51 construction carpenters, and 60 municipal office workers. al load imposed on the back was distinctly different in each group. The machine drivers (earth mover operators, longshoremen) were exposed to whole-body vibration and prolonged sitting. Occasionally, they were exposed to manual material handling, particularly in maintenance work. The carpenters were exposed to dynamic physical work, including material handling and postural load, and to a high accident risk due to climbing, walking on rough surfaces with obstacles, etc. The office workers had sedentary work but were free to change posture and move around. Questionnaire and Interview. A self-administered questionnaire included the same questions as the previous questionnaires about occurrence, duration, and type of low back symptoms during the preceding 12 months and 4 years, about occupational history (e.g., years in occupation and exposures at work), individual characteristics (e.g., anthropometric measures and level of education), and lifestyle factors (e.g., annual car driving, smoking). A structured interview with complementary questions about LBP and potential risk factors was performed by a nurse, who also checked the questionnaire for the completeness of the answers. The questions concerning LBP were as follows: Have you had low back pain during your lifetime; during the past 4 years; during the previous 12 months? What kind of low back pain have you had: lumbago (meaning sudden attack of low back pain); sciatic pain (meaning low back pain radiating to the lower limb); other low back pain? The concept of sciatic pain is 487

2 488 Spine Volume 25 Number Table 1. Distribution of Subjects by Explanatory Variables (N 164) Number of discs with dark nucleus pulposus Number of discs with posterior bulge Number of discs with anterior bulge Office worker 36.6 Carpenter 31.1 Machine driver 32.3 Height 175 cm cm 38.4 History of overweight No overweight* 21.3 Others 59.1 Constant overweight 19.5 History of smoking No smoking ever 31.7 Smoking in the past 32.9 Present smoking 35.4 History of car driving km/year km/year 35.6 * BMI 24.0 kg/m 2 at 25 years and currently. BMI 27.0 kg/m 2 at 25 years and currently. At the time of the present study and of the studies 4 and 7 years before. a nonspecific one including symptoms associated with true sciatica but also, e.g., referred pain felt in the thigh. In the analysis, lumbago and other LBP were combined as local LBP. Job title was used as the measure of occupational load. The subjects had worked for 26 years on average in the present occupation. The other potential confounding factors and the percentages of the subjects according to each variable are presented in Table 1. MRI Examination. The lumbar spines were examined with a 0.1 T Imager (Mega4, Instrumentarium, Helsinki, Finland) and a surface coil. Proton density and T2-weighted images in sagittal plane were obtained using a dual echo technique (TR 2000/TE 25-86) with two acquisitions. The first echo was a gradient echo and the second one a spin echo. Slice thickness was 7 mm, field of view 410 mm 410 mm (imaging area L1 S1), matrix , and pixel size 1.6 mm. There were no gaps between the slices. All examinations were included in the study, even though the general image quality was not optimal in 16 cases (9.8%). The peripheral regions are the most vulnerable for technical reasons. Disc L1/L2 was excluded from the analysis, as the image quality was low in the majority of the examinations. Observation was recorded as missing if the image quality was not high enough for reliable evaluation, which was the case in 9-25/164 observations of the L5/S1 discs, depending on the sign of disc degeneration. % Signal Intensity of the Nucleus Pulposus. Signal intensity of the nucleus pulposus of the discs L2/L3 L5/S1 on T2-weighted images was visually estimated by three radiologists on a four point scale (1 bright, 2 grey, 3 dark, 4 black), using the cerebrospinal fluid (CSF) in the adjacent dural sac as an intensity reference. 11,12 Interobserver agreement (weighted kappa) between each pair of the radiologists ranged from 0.59 to 0.83 for individual disc levels L2/L3 L5/S1. Twenty-two of the images were reevaluated by one of the radiologists. Intraobserver agreement rate was 57% to 81%. The interpretation of the most experienced radiologist was used in data analysis. The signal intensity of the nucleus pulposus was dichotomized before the final data analysis; intensity lower than that of the adjacent CSF (grades 3 or 4) was considered as a positive finding, called dark nucleus pulposus (Figure 1A). Anterior and Posterior Bulge of the Intervertebral Disc. All images were visually evaluated by the three radiologists. None of the subjects had a major asymmetric bulge or herniation. The magnitude of disc bulges was measured by one of the radiologists in the middle line of the disc from the proton density-weighted sagittal images (Figure 1B), with the facility of the MRI device as presented earlier. 13 A bulge measuring 3.2 mm or more was considered as a positive finding. The measurements were repeated for 25 of the images to estimate intraobserver agreement. Agreement rate was 86% to 100% for anterior bulges and 81% to 92% for posterior bulges, lowest for L5/S1 disc. Statistical Analysis. The association of LBP with disc degeneration and the covariates was analyzed by multivariate modeling. The dependent variables were the 12-month and the 4-year prevalence of LBP (including all types of LBP) and sciatic pain. The numbers of discs with different signs of degeneration were used as determinants, and occupation, height, history of overweight, smoking, and car driving were adjusted for as confounders. Logistic regression analysis was performed using Genmod procedure of statistical analysis system (SAS) to estimate the odds ratios (OR) and their 95% confidence intervals (CI). For each sign of degeneration a separate analysis was made. The number of discs either with dark nucleus pulposus or with posterior or ante- Figure 1. Decreased signal intensity of the nucleus pulposus in the L5/S1 disc in a T2-weighted image (A). The posterior bulge in the L5/S1 disc was more clearly demonstrated in the proton densityweighted image (B).

3 Low Back Pain and Disc Degeneration Luoma et al 489 Results The 12-month prevalence of LBP was 74.4% and the 4-year prevalence was 81.1%. For sciatic pain the prevalence rates were 29.9% and 39.0%, respectively. In Figure 2, the prevalences are presented by occupation. Low back pain was more common among machine drivers and carpenters than among office workers. Sciatic pain was most common among machine drivers and local LBP among carpenters. The prevalence of sciatic pain increased with increasing numbers of degenerated discs for each sign of degeneration (Figure 3). The prevalence of local LBP was similar across all signs of disc degeneration and did not seem to depend on the number of degenerated discs. All signs of disc degeneration were associated with an increased risk of LBP during the past 12 months, adjusted odds ratios ranging from 2.0 to 3.4 for one unit change in the degeneration variable (Table 2). The relationship between LBP and posterior or anterior bulge was weaker for the 4-year prevalence of LBP, but regarding dark nucleus pulposus it was of the same magnitude as for the 12-month prevalence. Low back pain and sciatic pain were distinctly related to occupation. The adjusted OR of machine drivers (8.1) was considerably higher than the crude OR (4.7), suggesting a negative confounding effect. The confounding effects of other explanatory variables were small. Sciatic pain had a weaker relation to all signs of disc degeneration than LBP (Table 3). The association was most distinct between 12-month prevalence of sciatic pain and posterior disc bulge (adjusted OR 2.0, 95% CI for one unit change). Discussion In this study, LBP during the preceding 12 months was found to be significantly associated with disc degeneration, assessed either as dark nucleus pulposus or posterior or anterior disc bulge. Sciatic pain was associated with posterior disc bulge. Weaker associations were found regarding LBP during the preceding 4 years. Oc- Figure 2. Twelve-month and 4-year prevalence of low back pain (LBP) (%) by occupation and type of LBP. rior bulges was handled as a count term (0,1,2,3,4) in the analysis, assuming that the risk of LBP or sciatic pain for each unit change is increased with the same magnitude. This means that if the OR is, e.g., 1.5, and the person has one disc affected, the odds in favor of them having LBP are 1.5 times greater than the odds of them not having LBP. If the patient has three discs affected, the odds are 4.5 times (3 1.5) in favor of them having LBP. Figure 3. Twelve-month and 4-year prevalence of low back pain (LBP) (%) in relation to the number of degenerated discs L2/L3 L5/S1, with three signs of degeneration.

4 490 Spine Volume 25 Number Table 2. Low Back Pain (LBP) in Relation to Different Signs of Disc Degeneration (L2/L3 L5/S1) and ; Odds Ratios (OR), and Their 95% Confidence Intervals (CI) 12-Month Prevalence 4-Year Prevalence Crude Adjusted* Crude Adjusted* Determinant OR 95% CI OR 95% CI OR 95% CI OR 95% CI Posterior bulge Carpenter Machine driver Anterior bulge Carpenter Machine driver Dark nucleus pulposus Carpenter Machine driver * Adjusted for height and for history of car driving, smoking and overweight. Change of OR per one unit change in the number of discs with the sign. cupation proved to be a strong predictor of LBP and sciatic pain. To study the association between LBP and disc degeneration, we chose the nonspecific concept of LBP, including all types, and sciatic pain as dependent variables. Local LBP includes pain, e.g., caused by distensions and other traumas of soft tissues, in addition to possible discogenic pain. Sciatic pain includes pain radiating below the knee, including pain symptoms associated with true sciatica, but also other pains such as referred pain thought to originate from the deep structures surrounding the disc and felt in the thigh. Eighty percent of men with sciatic pain in the questionnaire also reported having had LBP radiating below the knee in the interview. Recall error is known to affect reporting of LBP. According to a previous report, recall error is differential across occupational groups so that it is highest among office workers and lowest among machine drivers. 23 Sciatic pain is remembered better than other types of LBP. Recall is also affected by the recentness and severity of symptoms. 22 For the classification of disc degeneration we used three signs that often coexisted. The repeatability of the signs of degeneration of discs L2/L3 L5/S1 was good. Table 3. Sciatic Pain in Relation to Different Signs of Disc Degeneration (L2/L3 L5/S1) and ; Odds Ratios (OR), and Their 95% Confidence Intervals (CI) 12-Month Prevalence 4-Year Prevalence Crude Adjusted* Crude Adjusted* Determinant OR 95% CI OR 95% CI OR 95% CI OR 95% CI Posterior bulge Carpenter Machine driver Anterior bulge Carpenter Machine driver Dark nucleus pulposus Carpenter Machine driver * Adjusted for height and for history of car driving, smoking and overweight. Change of OR per one unit change in the number of discs with the sign.

5 Low Back Pain and Disc Degeneration Luoma et al 491 The signal intensity of the intervertebral disc correlates with its water and proteoglycan content. 15,26 It is decreased in most discs with a radial fissure, 5,32 which is also considered as a sign of disc degeneration. 8 We estimated the signal intensity in the nucleus pulposus, the region with the highest water content. The effect of the arbitrary scaling of the MR images and the distance of the disc from the surface coil on the signal intensity was corrected by using adjacent CSF as an intensity reference. 11,12 An association between disc bulge and radial fissure has been found, 3,28,33 in particular, for bulges of the size of 2.5 mm or more. 33 The size of 3.2 mm or more was chosen as the criterion for a positive finding for a bulge. It was considered as the minimum size to be assessed reliably. Only a few of the posterior bulges were 4.8 mm or more in size, but none of the subjects had major asymmetric bulges or herniations. The measurement was performed in the midsagittal slice because the projectional distortion affects the measurements in the more lateral slices. Differentiation between diffuse bulging or focal bulge of the disc was not attempted. Part of the lateral or posterolateral disc bulges may not have been detected in sagittal slices. We did not attempt to assess a possible nerve root compromise. In the neutral supine position, even in axial slices, the degree of compression of the dural sac or nerve roots by disc bulges may be underestimated as compared with the situation in the upright position with normal axial load on the discs. Thus, the true degree of compromise cannot be accurately measured as recently suggested. 7 Odds ratio is known to overestimate the risk of common events. In our analysis we could not estimate the risk ratios (RR) because available multivariate methods were not applicable to the data. The crude OR versus RR of 12-month LBP was 2.9 versus 1.4 for carpenters and 4.7 versus 1.5 for machine drivers. For sciatic pain the figures were 1.7 versus 1.6 and 6.4 versus 3.5, respectively. Pain felt in the low back may originate from the vertebrae, ligaments, fascias, muscles, facet joints, or intervertebral discs. Intradiscal pathology is assumed to play a major role in nonspecific LBP syndromes 30 and chronic LBP. 17 There are pain sensitive nerve endings in the fibers of annulus fibrosus, even in the inner parts of a degenerated disc. 4 Nucleus pulposus tissue is known to have marked inflammatory properties. 14,18 Neural compromise is a known cause of sciatic pain. Disc herniation or bulge or narrowing osteoarthritic changes may cause mechanical compression or distension of the lumbar nerve root, dorsal root ganglion, or smaller nerves surrounding the disc. In recent studies, chemical irritation has been suggested to be a more important cause of sciatic pain. 24 Most of the bulges in our study were small to cause neural compromise, but of the size likely to be associated with a radial tear. Posterior disc bulge was a stronger risk factor for recent than for earlier LBP and sciatic pain as expected. Low back pain has been found to be associated with changes in the annulus fibrosus, 1,9,16,31 with disc protrusions, 27, and with the decrease of signal intensity of the disc. 6,19 An association between LBP and radiographic film findings has been found in some studies, among them one follow-up study, 25 although van Tulder 29 concluded that there is no firm evidence of a causal relationship. The presence of degenerative changes is not diagnostic of low back pain. Indeed some 30% of asymptomatic individuals have such changes. 2,10,20,27 However, the present data indicate that these changes render low back pain to be more likely and more so the greater the number of discs affected. had a strong effect on the prevalence of LBP in our study. Machine drivers exposed to wholebody vibration and prolonged constrained sitting had the highest prevalence of sciatic pain. The prevalence of local LBP was highest among carpenters exposed to dynamic physical work and high accident risk. Adjustment for the potential confounding factors had a minor effect on the relationships between LBP and the signs of disc degeneration, with the exception of occupation, which had a negative confounding effect on the relationship between LBP and posterior bulges. Even if the crude OR for machine drivers and carpenters was higher than that for the signs of disc degeneration, the association between LBP and disc degeneration prevailed in multivariate modeling when the occupation and other confounding factors were added to the model. In cross-sectional studies and also in case-referent studies the problem concerning the temporal relationship between radiologic findings and symptoms is present: the timing of the occurrence of LBP and the appearance of the signs of disc degeneration is not known. In the future, the association between LBP and disc degeneration should be studied with longitudinal study designs, using repeated assessment of the occurrence of LBP and repeated MRIs in order to unravel the temporal relations between the incidence of low back symptoms and appearance of disc degeneration. It seems beneficial to differentiate between various types of LBP and various signs of disc degeneration in epidemiologic studies on low back disorders. Conclusions In this cross-sectional MRI study, LBP was associated with signs of disc degeneration and sciatic pain with posterior disc bulges. The risks of LBP and sciatic pain were strongly affected by occupation. References 1. Aprill C, Bogduk N. High-intensity zone: A diagnostic sign of painful lumbar disc on magnetic resonance imaging. Br J Radiol 1992;65: Boden SD, Davis DO, Dina TS, Patronas NJ, Wiesel SW. Abnormal magnetic-resonance scans of the lumbar spine in asymptomatic subjects. A prospective investigation. J Bone J Surg 1990;72-A: Buirski G. Magnetic resonance signal patterns of lumbar discs in patients

6 492 Spine Volume 25 Number with low back pain. A prospective study with discographic correlation. Spine 1992;17: Coppes MH, Marani E, Thomeer RTWM, Groen GJ. Innervation of painful lumbar discs. Spine 1997;22: Dullerud R, Johansen JG. CT-diskography in patients with sciatica. Comparison with plain CT and MR imaging. Acta Radiol 1995;36: Erkintalo MO, Salminen JJ, Alanen AM, Paajanen HEK, Kormano MJ. Development of degenerative changes in the lumbar intervertebral disk: Results of a prospective MR imaging study in adolescents with and without low-back pain. Radiology 1995;196: Haughton V. Spine imaging: Should we take this lying down? AJNR 1998; 19(9): Hirsch C, Schajowicz F. Studies on structural changes in the lumbar annulus fibrosus. Acta Orthop Scand 1952;22: Horton WC, Daftari TK. Which disc as visualized by magnetic resonance imaging is actually a source of pain? A correlation between magnetic resonance imaging and discography. Spine 1992;17:S Jensen MC, Brant-Zawadzki MN, Obuchowski N, Modic MT, Malkasian D, Ross JS. Magnetic resonance imaging of the lumbar spine in people without back pain. N Engl J Med 1995;331: Luoma EK, Raininko R, Nummi PJ, Luukkonen R, Manninen HI, Riihimäki HA. Suitability of cerebrospinal fluid as a signal intensity reference on MRI: Evaluation of signal-intensity variations in the lumbosacral dural sac. Neuroradiology 1997;39: Luoma K, Raininko R, Nummi P, Luukkonen R. Is the signal intensity of cerebrospinal fluid constant? Intensity measurements with high and low field magnetic resonance imagers. Magn Reson Imaging 1993;11: Luoma K, Riihimäki H, Raininko R, Luukkonen R, Lamminen A, Viikari- Juntura E. Lumbar disc degeneration in relation to occupation. Scand J Work Environ Health 1998;24(5): McCarron RF, Wimpee MW, Hudkins PG, Laros GS. The inflammatory effect of nucleus pulposus. A possible element in the pathogenesis of low-back pain. Spine 1987;12: Modic MT, Pavlicek W, Weinstein MA, et al. Magnetic resonance imaging of intervertebral disk disease: Clinical and pulse sequence considerations. Radiology 1984;152: Moneta GB, Videman T, Kaivanto K, et al. Reported pain during lumbar discography as a function of anular ruptures and disc degeneration. A re-analysis of 833 discograms. Spine 1994;19: Mooney V. Presidential Address to the International Society for the Study of the Lumbar Spine, Dallas, Where is the pain coming from? Spine 1987;12: Olmarker K, Blomquist J, Strömberg J, Nannmark U, Thomsen P, Rydevik B. Inflammatogenic properties of nucleus pulposus. Spine 1995;20: Paajanen H, Erkintalo M, Kuusela T, Dahlström S, Kormano M. Magnetic resonance study of disc degeneration in young low-back pain patients. Spine 1989;14: Powell MC, Wilson M, Szypryt S, Symonds EM. Prevalence of lumbar disc degeneration observed by magnetic resonance in symptomless women. Lancet 1986;2: Riihimäki H, Tola S, Videman T, Hänninen K. Low-back pain and occupation a cross-sectional questionnaire study of men in machine operating, dynamic physical work, and sedentary work. Spine 1989;14: Riihimäki H, Videman T, Tola S. Reliability of retrospective questionnaire data on the history of back trouble [Abstract]. Seventh International Symposium: Epidemiology in al Health. Tokyo, Japan, October, Riihimäki H, Viikari-Juntura E, Moneta G, Kuha J, Videman T, Tola S. Incidence of sciatic pain among men in machine operating, dynamic physical work, and sedentary work: A three-year follow-up. Spine 1994;19: Sella EJ. Noncompressive spinal radiculitis. Orthop Rev 1992;21: Symmons DPM, van Hemert AM, Vandenbroucke JP, Valkenburg HA. A longitudinal study of back pain and radiological changes in the lumbar spines of middle aged women. II. Radiographic findings. Ann Rheum Dis 1991;50: Tertti M, Paajanen H, Laato M, Aho H, Komu M, Kormano M. Disc degeneration in magnetic resonance imaging: A comparative biochemical, histologic and radiologic study in cadever spines. Spine 1991;16: Tertti M, Salminen JJ, Paajanen H, Terho P, Kormano M. Low-back pain and disc degeneration in children: A case control MRI study. Radiology 1991; 180: Tervonen O, Lähde S, Rydberg J. Lumbar disc degeneration. Correlation between CT and CT/discography. Acta Radiol 1990;31: van Tulder MW, Assendelft WJJ, Koes BW, Bouter LM. Spinal radiographic findings and nonspecific low back pain. A systematic review of observational studies. Spine 1997;22: Vanharanta H, Guyer RD, Ohnmeiss DD, et al. Disc deterioration in lowback syndromes. A prospective, multi-center CT/discography study. Spine 1988; 13: Vanharanta H, Sachs BL, Spivey MA, et al. The relationship of pain provocation to lumbar disc deterioration as seen by CT/discography. Spine 1987;12: Yu S, Haughton VM, Ho PSP, Sether LA, Wagner M, Ho KC. Progressive and regressive changes in the nucleus pulposus. Part II. The adult. Radiology 1988;169: Yu S, Haughton VM, Sether LA, Wagner M. Anulus fibrosus in bulging intervertebral disks. Radiology 1988;169: Address reprint requests to Katariina Luoma, MD Finnish Institute of al Health Topeliuksenkatu 41 a A FIN Helsinki, Finland kluoma@dlc.fi

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