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Contribution of ribcage movement to thoracolumbar posteroanterior stiffness
CONTRIBUTION OF RIBCAGE MOVEMENT TO THORACOLUMBAR POSTEROANTERIOR STIFFNESS Wunpen Chansirinukor, MAppSc (Phty),a Michael Lee,b and Jane Latimer, PhDc
ABSTRACT Objective: To investigate (1) whether thoracolumbar posteroanterior (PA) stiffness differs between 2 conditions of
ribcage movement: unconstrained and constrained, and (2) whether the effect of ribcage constraint on PA stiffness varies according to where the PA force is applied. Design: Two-factor within-subjects design. Setting: Spinal Mechanics Laboratory, University of Sydney. Intervention: A convenience sample of 41 subjects, asymptomatic for back pain, participated. PA stiffness at T12L4 was measured in the unconstrained and constrained ribcage conditions with a mechanical device. For the constrained condition, we used a clamping device to apply a force to the subject’s lower thorax to reduce movement. Main Outcome Measures: PA stiffness at T12-L4 under both ribcage conditions. Results: PA stiffness at T12-L4 significantly increased when the ribcage was constrained (P⬍ .05). However, the effect of ribcage movement did not depend on the location of the PA force. Conclusions: These findings suggest that the properties of the ribcage influence measures of PA stiffness in the thoracolumbar (T12-L4) spine uniformly. Variations in PA stiffness in segments T12-L4 may reflect the properties of the intervertebral joints. (J Manipulative Physiol Ther 2003;26:176-83) Key Indexing Terms: Thoracic Spine; Lumbar Spine; Stiffness; Ribcage
INTRODUCTION xamination of intervertebral responses is fundamental in the assessment and treatment of lumbar vertebral dysfunction for many clinicians. One such examination is lumbar posteroanterior (PA) mobilization, in which a PA pressure is manually applied to a spinous process of a patient’s lumbar vertebra to reproduce the patient’s symptoms and to allow the examining clinician to perceive the muscle responses and stiffness of the intervertebral joints. The stiffness is perceived in relation to the applied force and displacement, and compared to the response at adjacent vertebrae to help the therapist judge whether the movements of intervertebral joints
E
a
Graduate Student, School of Exercise and Sport Science, University of Sydney, Sydney, Australia. b Lecturer, School of Exercise and Sport Science, University of Sydney, Sydney, Australia. c Lecturer, School of Physiotherapy, University of Sydney, Sydney, Australia. Submit requests for reprints to: Wunpen Chansirinukor, 1/13 Mary Street, Lidcombe NSW 2141, Australia. (e-mail: [email protected]). Paper submitted January 23, 2002; in revised form February 21, 2002. Copyright © 2003 by JMPT. 0161-4754/2003/$30.00 ⫹ 0 doi:10.1016/S0161-4754(02)54131-2
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are normal.1 PA mobilization is similar to, but distinct from, a tissue stiffness assessment approach in which a force is applied directly to soft tissue to perceive tissue stiffness or hardness.2 The difference between these approaches is that the latter is used to identify abnormalities of soft tissue, such as changes in muscle tone and local edema,2 whereas PA mobilization is used to assess joint stiffness. With regard to PA mobilization, reproduction of the patient’s symptoms corresponding to perception of abnormal PA stiffness is one factor used to determine the vertebral level for treatment.3 Although there is increasing emphasis on the reproduction of the patient’s symptoms as a method of identifying the vertebral level to be treated,4-6 the use of PA stiffness as an indicator of the stiffness of the intervertebral joints is still recommended in the clinical examination.3 Despite the common use of lumbar PA mobilization, little is known about which tissues determine the nature of PA stiffness and what causes variation in stiffness between individuals and between vertebral levels.7 Although researchers have used well-controlled procedures to study PA stiffness in reasonably homogeneous groups of subjects, previous research has shown substantial variations of lumbar PA stiffness between subjects.8,9 Variations in lumbar
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Fig 1. Schematic model of manual-applied force to spine, based on the findings of Lee et al.7,28 The force (A) is applied through a spring (B) representing the dorsal soft tissues. The head and the pelvis can be considered to be rigid bodies. The upper spine is supported by a series of springs (K) that represent the ribcage. The pelvis is supported by springs restraining horizontal (C) and vertical (D) movement, and by a spring that resists pelvic rotation about the axis of rotation (E).
PA stiffness have been shown to relate to a number of factors: direction of applied force, posture of lumbar spine, level of spinal muscle activity, rate of loading, position of load, and body type.8-13 It appears that the nature of the support and constraint applied to the spine by the adjacent structures is one factor determining the variations in thoracolumbar PA stiffness.7 Two studies of the effect of plinth surface on PA stiffness14,15 have demonstrated that when a subject lies on a padded plinth, measured PA stiffness is lower than when testing is performed on an unpadded plinth. Our previous study16 has shown that pelvic movement has a significant effect on lower lumbar PA stiffness but no significant effect on mid to upper lumbar PA stiffness. This result indicates that the nature of pelvic constraint is reflected in lumbar movements. Similarly, it has been suggested that the lower values of PA stiffness observed at upper and mid lumbar levels compared to lower lumbar levels are due to the less rigid support offered by the lower ribcage to the spine.7 Previous studies have investigated the ribcage properties17 and their possible relationship to the response to PA spinal loading.7,11 Lee et al17 measured anteroposterior (AP) ribcage stiffness of men and women in response to the load applied to the sternum and reported an average stiffness of 9.4 N/mm. The results showed that male subjects, with greater average AP chest diameters than female subjects, also had greater ribcage stiffness. Edmondston et al11 compared the PA stiffness of T4, T7, and T10 and AP ribcage stiffness. The average AP ribcage stiffness, 7.6 N/mm, was substantially lower than the stiffness in the study by Lee et al.17 They found a significant correlation between the thoracic PA stiffness and AP ribcage stiffness, with the latter accounting for 33% of the variations in thoracic PA stiffness. Lee et al7 investigated the thoracolumbar PA stiffness at T4, T7, T10, L1, and L4 and found that AP chest diameter accounted for 17% of variations in the PA stiffness at T7. They proposed a model of spinal PA loading in which the ribcage, represented by a series of springs, influenced the midthoracic PA stiffness (Fig 1). The findings from all these studies support the idea that ribcage behavior is directly involved in determining thoracic PA stiffness.
Although previous research11 has demonstrated an association between AP ribcage stiffness and the variations in the thoracic PA stiffness, no causal relationship has been demonstrated. The model proposed by Lee et al7 predicts that thoracic and lumbar PA stiffness depend on the amount of deformation of the ribcage. However, this proposition has not been tested. Furthermore, if such a causal relationship does exist, the sensitivity of PA responses to ribcage deformation is unknown. Constraining the ribcage movement and measuring the effect on PA stiffness would show how much ribcage movement in the sagittal plane might contribute to PA stiffness. In terms of the model put forward by Lee et al7 represented in Figure 1, constraining the ribcage movements could increase the stiffness of the springs (Fig 1, K) and hence, increase the PA stiffness. Therefore, in our study we aimed to investigate (1) whether the thoracolumbar PA stiffness differed between 2 conditions of ribcage movement, unconstrained and constrained; and (2) whether the effect of ribcage constraint on PA stiffness varied according to where the PA force was applied.
METHODS Research Design We measured thoracolumbar PA stiffness by using a repeated-measures design with 2 within-subjects factors (vertebral level and ribcage condition) and 1 between-subjects factor (sex). The PA stiffness at T12, L1, L2, L3, and L4 was measured under 2 conditions of ribcage movement (unconstrained and constrained conditions).
Subjects Forty-one subjects (21 women and 20 men) participated in the study. All were students at the University of Sydney selected as a sample of convenience. The study was approved by the Human Ethics Committee of the University of Sydney, and informed consent was obtained from each subject prior to the study. Criteria for inclusion included no current symptoms of thoracic and lumbar pain, and no thoracic and lumbar symptoms that required consultation or treatment within the preceding 12 months. Criteria for exclusion included the
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Table 1. Subject characteristics
Procedure
Variables
Mean (SD)
Range
Age (y) Mass (kg) Height (cm) BMI* (kg/m2) Skinfold* (mm)
24.46 (5.37) 66.61 (10.96) 168.65 (8.51) 23.29 (2.31) 10.76 (4.05)
18–37 48–91 153.0–184.5 18.47–28.07 4.8–26.0
*Skinfold was measured at the level of the xiphisternal junction in the midaxillary line.
presence of pain during testing or of any known spinal or systemic disease, such as inflammatory diseases and infections of the spine, that contraindicated the use of mobilization forces.18 Subjects’ age, sex, mass, and height were recorded. It has been shown that 2 body-type parameters, body mass index (BMI or mass/height)2 and local skinfold thickness, influence lower lumbar PA stiffness.7,9 To evaluate this effect in the thoracolumbar region, we measured midaxillary skinfold thickness at the level of the xiphisternal junction in the midaxillary line, using a skinfold caliper (John Bull British Indicators, Ltd, Burgess Hill, UK) when the subject was standing. We measured the skinfold thickness 3 times and used the average value. The BMI was also calculated to allow an exploration of the relation of overall body type to PA stiffness. The characteristics of the subject group are listed in Table 1.
Equipment We used the Spinal Physiotherapy Simulator (SPS) to measure the PA stiffness. The principal components of the SPS include a variable speed motor, a cam, and a parallelogram linkage. The motor output shaft is connected to the cam by a V-belt and pulley system. Attached to the parallelogram linkage is a loadcell (XTRAN loadcell S1W 250 N, Applied Measurement Pty, Ltd, Eastwood, NSW, Australia) connected to a rubber-padded indenter, which is the part that contacts the subject’s skin while the SPS applies forces. The movement of the indenter is controlled by rotation of the cam, allowing movement of the parallelogram linkage under control of a dead weight. The main function of the SPS is to apply a force to the skin surface overlying a subject’s spinous process and to record the amount of skin displacement in response to the applied force. The force and displacement are then used to calculate stiffness.19 The direction of force applied by the SPS can be adjusted by tilting the device in a cephalad or caudad direction within the sagittal plane. The SPS has good reliability for repeated measurements of L3 PA stiffness (at 0.5 Hz), with an ICC (2,1) of 0.88 being obtained for measurement of 11 subjects without low back pain. It is also accurate in its measurement of stiffness. The maximum error when measuring stiffness of an aluminum beam was found to be less than 1%.19
The subject lay in a prone position on the examination couch, with arms placed by his/her sides. The examiner palpated and identified the spinous processes from C7 to L5. After identification, the spinous processes of T12 and L1-L4 were marked. Screening tests were then performed. A PA force was manually applied from T12 to L4 to ensure that the subject was pain free. The subject was then required to perform active trunk flexion and extension in the standing position. Subjects reporting pain related to the applied PA force or active movements were excluded from the study. The indenter of the SPS was positioned over the spinous process to be tested. By adjusting the SPS frame, then clamping it in the tilted position, the direction of indenter movement to be used for testing was set to the desired angle in the sagittal plane. In this study, the angles (degrees from vertical) used were 9° directed cephalad at T12, 6° cephalad at L1, 3° cephalad at L2, 1° caudad at L3, and 5° caudad at L4. These angles were based on data for sagittal spine curvature20 and on observations of experienced physiotherapists manually applying PA forces to the lumbar spine.21 In our study, we aimed to measure the thoracolumbar PA stiffness under 2 conditions—with ribcage constraint and without ribcage constraint. For the ribcage constraint condition, we used a device to attempt to limit the deformation and displacement of the thorax in the sagittal plane. The ribcage constraint device (Fig 2) consisted of a clamp with 2 curved wooden jaws. The jaws were padded with a thin layer of soft rubber (0.4 cm) for the subject’s comfort. The jaws were firmly pressed against the lateral aspects of the subject’s lower ribcage with a clamp. To standardize the amount of force provided by the clamp, a loadcell connected to a Transducer Readout (RD-201A, Applied Measurement Australia Pty, Ltd) was connected to one side of the ribcage constraint device. For all subjects, the constraint was initially applied with a lateral force of 135 N. The force was gradually increased to this point to ensure that the subjects could tolerate it. The protocol involved 2 tests: (1) the lower thoracic regional stiffness test and (2) the thoracolumbar PA stiffness tests at 5 locations. For every subject, the testing was begun with tests of the lower thoracic regional stiffness in both ribcage conditions to ensure that the ribcage constraint device was effective in reducing thoracic compressibility. The degree of ribcage constraint was evaluated by comparing lower thoracic regional stiffness in the constrained and unconstrained conditions. The force was applied by means of a large, padded (with a thin layer of soft rubber, 0.4 mm thick) wooden indenter (14 cm ⫻ 15 cm ⫻ 1.2 cm) placed on the lower thorax, with the lower edge at the spinous process of T11. The force was applied 5 cm from the lower edge of the wood in the same direction as that used for PA
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Fig 2. Photograph of subject in a constraint device with jaws positioned for the constrained ribcage condition. On the left of the constraint device is a loadcell with readout, which was used to standardize the force used in the constraint.
testing at T12. The order of presentation of constraint of the ribcage was counterbalanced, in that half the subjects received the unconstrained condition followed by the constrained condition, and the other half received the constrained condition followed by the unconstrained condition. After the tests of lower thoracic regional stiffness were completed, we performed the thoracolumbar PA stiffness tests in which the PA force was localized to 1 spinous process at a time. The order of testing at the different vertebral levels was randomly assigned to minimize any systematic effect. In each test, prior to data collection, we applied 3 cycles of force from 0 N to 120 N, using the SPS to precondition the tissues. The aim of preconditioning was to give more reproducible behavior of soft tissues and to familiarize the subject with the testing procedure. Immediately after preconditioning, 5 loading cycles were applied while the force and displacement data were collected. The data were passed to a 12-bit analogue-to-digital converter (DT2801A, Data Translation, Inc, Marlboro, Mass) and stored for subsequent analysis. During each phase of data collection, subjects held their breath at the end of normal expiration. This was done to maintain a lung volume during stiffness testing and to prevent the spinal movement associated with breathing that could confound the stiffness data. Breathing during stiffness testing has been shown to affect PA stiffness.22
Intraexaminer Reliability To investigate the variability in repeated measurements of lower thoracic regional stiffness, a second test in the
unconstrained ribcage condition was conducted immediately after all other tests were performed.
Data Analysis Raw data of force/time and displacement/time were analyzed with special purpose software. The main variables examined in this study were the thoracolumbar PA stiffness values. The stiffness is calculated from the slope of the least-squares regression line fitted to the force-displacement curve between 30 N and 100 N of force.7,9 Lower thoracic regional stiffness was evaluated in the same way. A 3-factor repeated measures analysis of variance ([ANOVA] SPSS, Inc, Chicago, Ill) was used to analyze PA responses. The effect of 2 within-subjects factors (ribcage condition and vertebral level) and 1 between-subjects factor (sex) was examined. The Pearson correlation coefficient was also used to investigate whether PA stiffness in the unconstrained condition was related to skinfold thickness and BMI. We compared the lower thoracic regional stiffness in the unconstrained and constrained conditions, together with analysis of the effect of sex, using ANOVA. Test-retest reliability in measurement of lower thoracic regional stiffness was expressed as an intraclass correlation coefficient (ICC [2,1]). A significance level of P ⬍ .05 was used for all statistical tests.
RESULTS Figure 3 shows the mean PA stiffness at 5 vertebral levels for both conditions of ribcage constraint. The average PA stiffness was lowest at L3 in both conditions (12.8 N/mm unconstrained, 13.4 N/mm constrained). The mean PA stiffness was greatest at T12 in the unconstrained ribcage con-
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Fig 3. PA stiffness at T12-L4 for the unconstrained and constrained ribcage conditions. Error bars represent standard deviations. Table 2. Pearson correlation coefficient values for correlation between PA stiffness* and BMI and skinfold thickness†
PA PA PA PA PA
stiffness stiffness stiffness stiffness stiffness
T12 L1 L2 L3 L4
BMI
Skinfold
0.05 0.28 0.27 0.13 ⫺0.09
⫺0.29 ⫺0.09 ⫺0.14 ⫺0.25 ⫺0.29
*PA stiffness corresponds to the unconstrained condition when loads were applied to T12, L1, L2, L3 and L4. † Skinfold was measured at the level of the xiphisternal junction in the midaxillary line.
dition (14.4 N/mm) and at L4 in the constrained condition (15.2 N/mm). The ANOVA showed a significant difference in the PA stiffness between ribcage conditions (F1,40 ⫽ 14.03), with the mean PA stiffness in the constrained condition being 0.9 N/mm higher than in the unconstrained condition. There was also a significant quadratic trend (F1,40 ⫽ 13.22); that is, as shown in Figure 3, there were high values at both the cephalad and caudad ends of the region tested, and lower values in the middle. Pairwise comparisons indicated that the mean PA stiffness at L3 was lower than the stiffness at T12 and L4. There was no significant interaction between the 2 experimental ribcage conditions and vertebral level of load location. There was no significant variation of PA stiffness due to sex (14.8 N/mm for men, 13.1 N/mm for women). The ANOVA showed that the mean lower thoracic regional stiffness in the constrained condition (12.9 N/mm) was significantly greater than that in the unconstrained
condition (12.0 N/mm) (F1,40 ⫽ 16.16). This indicated that the ribcage constraint device was effective in decreasing thoracic deformation. There was no significant variation in the lower thoracic regional stiffness due to sex. The results of the correlations between PA stiffness and measures of body type are listed in Table 2. For the lower thoracic regional stiffness, the test-retest reliability, ICC (2,1), was 0.82, with a 95% CI of 0.68-0.90.
DISCUSSION Our intent in this study was to examine the effect of ribcage constraint on thoracolumbar PA stiffness and also whether this effect varied in relation to the vertebral level where the PA force was applied. Our results show that ribcage movement does alter thoracolumbar PA stiffness, but for PA forces applied at T12 to L4, the effect does not depend on the location of the applied force. We used a ribcage constraint device to reduce the movement of the posterior ribcage in the sagittal plane and investigate whether that movement was a determinant of thoracolumbar PA stiffness. Effectiveness of the constraint device was shown by a significant increase in the lower thoracic regional stiffness in the constrained compared to the unconstrained ribcage condition. The lower thoracic regional stiffness in the constrained condition was approximately 7% greater than that in the unconstrained condition, corresponding to 0.38 mm (5.57 mm vs 5.96 mm) less displacement of the indenter over the 70 N range of forces considered. Even though this change in stiffness is too small to be clinically detectable,23 it demonstrates the mechanism involved. Despite the fact that the ribcage deformation and displacement were only partially restrained, this amount of
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change was sufficient to show the contribution of the ribcage to the thoracolumbar PA stiffness. The 0.38-mm reduction in posterior ribcage movement produced a mean 0.24-mm decrease in thoracolumbar PA displacement over the same force range; that is, the percentage of reduction in the thoracolumbar PA displacement was 63% of the reduction in posterior ribcage movement. This ratio suggests a high sensitivity of thoracolumbar PA stiffness to posterior ribcage movements. We could therefore speculate that complete prevention of posterior ribcage movement would be likely to result in substantially greater increases in PA thoracolumbar stiffness. In this study, the PA stiffness values corresponding to unconstrained ribcage movement are similar to those in previous studies. The PA stiffness values at L1-L4 reported in previous studies, using the same frequency of loading, ranged between 14.1 N/mm and 17.5 N/mm in asymptomatic subjects.8,9,14 The slightly lower PA stiffness at L1-L4 in our study (12.8-14.0 N/mm) compared to previous studies could be due to the difference in subject characteristics and directions of applied load. In addition, the PA stiffness value at T10 reported in previous studies, using a slower frequency (0.05 Hz), was 10.4 N/mm.7,11 The higher PA stiffness at T12 in our study (14.4 N/mm) compared to previous studies could be due to the differences in frequency of applied force13 and vertebral level. The effect of sex on thoracolumbar PA stiffness of subjects without low back pain in the unconstrained ribcage condition has been previously studied, with different outcomes.7,24,25 Lee et al7 found no effect of sex on PA stiffness at T4, T7, T10, L1, and L4, whereas Allison et al25 reported a 24% greater PA stiffness at L1 and L3 in men compared with women. When considering the material properties of the ribcage related to sex, Lee et al17 found that the mean AP ribcage stiffness, in response to AP load over the sternum, was 8.4 N/mm in women and 10.5 N/mm in men. In our study, we examined the effect of sex on both lower thoracic regional stiffness and thoracolumbar PA stiffness. The mean lower thoracic regional stiffness values in women and men were both 12.0 N/mm. The mean thoracolumbar PA stiffness values in women and men were 12.7 N/mm and 14.3 N/mm, respectively. There were no significant differences between sexes for lower thoracic regional stiffness and thoracolumbar PA stiffness. Previous studies have measured AP ribcage stiffness as 7.6-9.4 N/mm.11,17 We observed lower thoracic regional stiffness of approximately 12 N/mm, which is higher. Lower stiffness might have been expected in the lower thoracic region as a result of the presence of floating ribs in this region and of relatively longer costal cartilages, which have lower stiffness than ribs.26 This apparent paradox may be related to the way the structure stiffness (the ribcage stiffness) has been tested (ie, AP vs PA load, indenter size difference, force direction, and frequency) or the smaller AP diameter in the lower thoracic region. Further investigation
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of the variation of regional stiffness would be required to resolve this issue. Skinfold thickness and BMI have been previously shown to influence lower lumbar PA stiffness. Viner et al9 found that suprailiac skinfold thickness was a significant determinant of PA stiffness in the low lumbar region (r2 ⫽ .28-.50 at L3-L5). Lee et al7 also found that suprailiac skinfold thickness was significantly correlated (r2 ⫽ .18) with PA stiffness at L4. It has been reported that midaxillary and suprailiac skinfold thickness are highly correlated (r ⫽ .83).7 Therefore, we would expect that the use of midaxillary skinfold thickness would yield a similar outcome to the use of suprailiac skinfold. However, the PA stiffness values in our study showed only weak correlations with midaxillary skinfold thickness (Table 2). This suggests that the amount of subcutaneous fat may not be an important determinant of variation in thoracolumbar PA stiffness. A plausible reason why our results did not show the same relationship between BMI and PA stiffness observed by Viner et al9 is that their subjects showed a larger range of BMI values. Among their subjects were 3 overweight subjects, whose BMIs were more than 30 kg/m2, and 5 underweight subjects, whose BMIs were less than 20 kg/m2. In contrast, the subjects in our study showed more uniform BMIs, with the maximum BMI being 28.07 kg/m2. Interestingly, we found a low correlation between BMI and skinfold thickness (r ⫽ .45, P ⫽ .003), and there was a negative correlation between BMI and skinfold except at the L4 level. This result suggests that the midaxillary skinfold thickness may not correlate well with the subjects’ overall fatness. The model of Lee et al7 suggests that PA stiffness would reflect the stiffness of elements supporting the spine. They hypothesized that PA stiffness would be highest near the pelvis and lower in the midlumbar region (because there is a lack of supporting structures), and increasing in the thorax but lower than near the pelvis (because the ribcage has lower stiffness than the pelvis). In our study, the PA stiffness value at L3 was lower than those values at T12 and L4, and there was a significant quadratic trend of PA stiffness values (Fig 3). This pattern of PA stiffness variation is consistent with the model proposed by Lee et al.7 Our results support the concept behind this model: The deformation and displacement of the structures that support the spine are major contributors to PA displacement. In unconstrained ribcage movement, a thoracolumbar PA force applied to a spinous process may produce a number of responses: intervertebral displacements at many thoracic and lumbar levels, compression of soft tissues on the anterior body surface and overlying the loaded vertebra, deformation and rigid-body displacement of the ribcage, and compression of the abdomen and pelvic rotation.7,13,27,28 There are many possible explanations by which the ribcage constraint could bring about increased thoracolumbar PA stiffness, most of which would be expected also to affect the lower thoracic regional stiffness. When the anterolateral
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clamping of the ribcage was applied, there could have been less movement at the costovertebral and costotransverse joints, less rigid-body motion of the lower thorax, smaller rib and costal cartilage deformations, and less compression of anterior soft tissues. Any of these effects could produce less movement of the vertebral column as a whole. Because we did not measure movements of the individual vertebrae, the extent of contribution of interverebral joints to the reduction in PA movement (and hence increased PA stiffness) is not known. In relation to our experiment, the structures contributing to PA displacement can be hypothesized as originating from 2 major groups—ribcage and nonribcage components (the nonribcage component includes intervertebral joints). Our study showed that the increase in PA stiffness, and hence the reduction in PA displacement due to ribcage constraint, did not significantly differ between vertebral levels, whereas the unconstrained PA stiffness did show significant variations. The findings suggest that although the PA displacement includes substantial contributions from nonspinal structures, the level-to-level variations in PA displacement may be indicative of behavior of the spine. Therefore, the clinical practice of comparing responses between vertebral levels29 may have some validity. We need to remember, however, that these findings cannot necessarily be directly applied to patients with low back pain. The presence of low back pain may be associated with involuntary hyperactivity of the paraspinal muscles. Changes in lumbar extensor muscle activity have been previously shown to increase lumbar PA stiffness.12 Hence, it is possible that the muscle activity of patients with low back pain may also contribute to variations in PA stiffness, and therefore alter the relative importance of the contributions of ribcage and nonribcage components. In the context of decreasing emphasis on the PA stiffness response as a clinically useful sign of spinal disorders,4-6 our results provide a mixed message to clinicians. On one hand, the finding that the thoracolumbar PA stiffness is sensitive to ribcage movements confirms the role of another nonspinal variable as a determinant of the PA response. On the other hand, the relative consistency of the ribcage contribution across a range of vertebral locations allows the possibility that the observed level-to-level variations in PA stiffness may be attributable to spinal tissues, and hence may be of clinical value.
CONCLUSIONS The contribution of the ribcage movement as one part of the mechanism determining the thoracolumbar PA stiffness has been demonstrated. The role of ribcage movement appears uniform across a range of vertebral locations (T12-L4) of the applied force. This finding suggests that although the PA stiffness values along the thoracolumbar spine reflect the properties of nonspinal structures associated with the
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ribcage, these structures may have a similar influence at many locations, and intersegmental variations in PA stiffness might be more indicative of the properties of other tissues, such as intervertebral joints.
REFERENCES 1. Maitland GD, Banks K, English K, Hengeveld E, editors. Maitland’s vertebral manipulation. 6th ed. Oxford, UK: Butterworth-Heinemann; 2001. p. 351-3. 2. Kawchuk G, Herzog W. A new technique of tissue stiffness (compliance) assessment: its reliability, accuracy and comparison with an existing method. J Manipulative Physiol Ther 1996;19:13-8. 3. Edwards BC. Examination. In: Maitland GD, Banks K, English K, Hengeveld E, editors. Maitland’s vertebral manipulation. 6th ed. Oxford, UK: Butterworth-Heinemann; 2001. p. 146-58. 4. Maher C, Latimer J. Pain or resistance—the manual therapists’ dilemma. Aust J Physiother 1992;38:257-60. 5. Lee M, Latimer J, Maher C. Manipulation: investigation of a proposed mechanism. Clin Biomech 1993;8:302-6. 6. Maher C, Adams R. Reliability of pain and stiffness assessments in clinical manual lumbar spine examination. Phys Ther 1994;74:801-11. 7. Lee M, Steven GP, Crosbie J, Higgs R. Variations in posteroanterior stiffness in the thoracolumbar spine: preliminary observations and proposed mechanisms. Phys Ther 1998;78: 1277-87. 8. Lee M, Liversidge K. Posteroanterior stiffness at three locations in the lumbar spine. J Manipulative Physiol Ther 1994; 17:511-6. 9. Viner A, Lee M, Adams R. Posteroanterior stiffness in the lumbosacral spine: the correlation between adjacent vertebral levels. Spine 1997;22:2724-30. 10. Caling B, Lee M. Effect of direction of applied mobilization force on the posteroanterior response in the lumbar spine. J Manipulative Physiol Ther 2001;24:71-8. 11. Edmondston SJ, Allison GT, Gregg CD, Purden SM, Svansson GR, Watson AE. Effect of position on the posteroanterior stiffness of the lumbar spine. Man Ther 1998;3:21-6. 12. Lee M, Esler M-A, Mildren J, Herbert R. Effect of extensor muscle activation on the response to lumbar posteroanterior forces. Clin Biomech 1993;8:115-9. 13. Lee M, Svensson NL. Effect of loading frequency on response of the spine to lumbar posteroanterior forces. J Manipulative Physiol Ther 1993;16:439-46. 14. Latimer J, Holland M, Lee M, Adams R. Plinth padding and measures of posteroanterior lumbar spine. J Manipulative Physiol Ther 1997;20:315-9. 15. Maher CG, Latimer J, Holland MJ. Plinth padding confounds measures of posteroanterior spinal stiffness. Man Ther 1999; 4:145-50. 16. Chansirinukor W, Lee M, Latimer J. Contribution of pelvic rotation to lumbar posteroanterior movement. Man Ther 2001; 6:242-9. 17. Lee M, Hill S, Scullin J. Ribcage compressibility in living subjects. Clin Biomech 1994;9:379-80. 18. Brewerton DA. The doctor’s role in diagnosis and prescribing vertebral manipulation. In: Maitland GD, Banks K, English K, Hengeveld E, editors. Maitland’s vertebral manipulation. 6th ed. Oxford, UK: Butterworth-Heinemann; 2001. p. 17-9. 19. Lee M, Svensson NL. Measurement of stiffness during simulated spinal physiotherapy. Clin Phys Physiol Meas 1990;11: 201-7.
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20. Reynolds HM, Rechtien JJ, Marshall GW, Marshall S. Spinal curvature of young adult females. Hum Biol 1986;58:88391. 21. Viner A, Lee M. Direction of manual force applied during assessment of stiffness in the lumbosacral spine. J Manipulative Physiol Ther 1995;18:441-7. 22. Beaumont A, McCrum C, Lee M. The effects of tidal breathing and breath-holding on the postero-anterior stiffness of the lumbar spine. Proceedings of the 7th Biennial Conference of the Manipulative Physiotherapists Association of Australia; 1991 Nov 27-30; Leura, NSW, Australia. Victoria, Australia: Manipulative Physiotherapists Assoc of Australia; 1991. 23. Nicholson L, Adams R, Maher C. Reliability of a discriminant measure for judgements of non-biological stiffness. Man Ther 1997;2:150-6. 24. Lee M, Steven GP. Modelling the trunk responses to lumbar manipulative forces. In: Middleton J, Jones ML, Pande GN, editors. Computer methods in biomechanics and biomedical
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25.
26. 27. 28. 29.
engineering—2. Amsterdam: Gordon and Breach Science Pub; 1998. p. 371-8. Allison GT, Edmondston SJ, Roe CP, Reid SE, Toy DA, Lundgren HE. Influence of load orientation on the posteroanterior stiffness of the lumbar spine. J Manipulative Physiol Ther 1998;21:1-5. Roberts SB, Chen PH. Elastostatic analysis of the human thoracic skeleton. J Biomech 1970;9:185-92. Lee M, Lau H, Lau T. Sagittal plane rotation of the pelvis during lumbar posteroanterior loading. J Manipulative Physiol Ther 1994;17:149-55. Lee M, Kelly DW, Steven GP. A model of spine, ribcage and pelvic responses to a specific lumbar manipulative force in relaxed subjects. J Biomech 1995;28:1403-8. Jull G. Examination of the articular system. In: Boyling J, Palastanga N, editors. Grieve’s modern manual therapy: the vertebral column. Edinburgh, Scotland: Churchill Livingstone; 1994. p. 520-2.
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ABSTRACT Objective: To investigate (1) whether thoracolumbar posteroanterior (PA) stiffness differs between 2 conditions of
ribcage movement: unconstrained and constrained, and (2) whether the effect of ribcage constraint on PA stiffness varies according to where the PA force is applied. Design: Two-factor within-subjects design. Setting: Spinal Mechanics Laboratory, University of Sydney. Intervention: A convenience sample of 41 subjects, asymptomatic for back pain, participated. PA stiffness at T12L4 was measured in the unconstrained and constrained ribcage conditions with a mechanical device. For the constrained condition, we used a clamping device to apply a force to the subject’s lower thorax to reduce movement. Main Outcome Measures: PA stiffness at T12-L4 under both ribcage conditions. Results: PA stiffness at T12-L4 significantly increased when the ribcage was constrained (P⬍ .05). However, the effect of ribcage movement did not depend on the location of the PA force. Conclusions: These findings suggest that the properties of the ribcage influence measures of PA stiffness in the thoracolumbar (T12-L4) spine uniformly. Variations in PA stiffness in segments T12-L4 may reflect the properties of the intervertebral joints. (J Manipulative Physiol Ther 2003;26:176-83) Key Indexing Terms: Thoracic Spine; Lumbar Spine; Stiffness; Ribcage
INTRODUCTION xamination of intervertebral responses is fundamental in the assessment and treatment of lumbar vertebral dysfunction for many clinicians. One such examination is lumbar posteroanterior (PA) mobilization, in which a PA pressure is manually applied to a spinous process of a patient’s lumbar vertebra to reproduce the patient’s symptoms and to allow the examining clinician to perceive the muscle responses and stiffness of the intervertebral joints. The stiffness is perceived in relation to the applied force and displacement, and compared to the response at adjacent vertebrae to help the therapist judge whether the movements of intervertebral joints
E
a
Graduate Student, School of Exercise and Sport Science, University of Sydney, Sydney, Australia. b Lecturer, School of Exercise and Sport Science, University of Sydney, Sydney, Australia. c Lecturer, School of Physiotherapy, University of Sydney, Sydney, Australia. Submit requests for reprints to: Wunpen Chansirinukor, 1/13 Mary Street, Lidcombe NSW 2141, Australia. (e-mail: [email protected]). Paper submitted January 23, 2002; in revised form February 21, 2002. Copyright © 2003 by JMPT. 0161-4754/2003/$30.00 ⫹ 0 doi:10.1016/S0161-4754(02)54131-2
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are normal.1 PA mobilization is similar to, but distinct from, a tissue stiffness assessment approach in which a force is applied directly to soft tissue to perceive tissue stiffness or hardness.2 The difference between these approaches is that the latter is used to identify abnormalities of soft tissue, such as changes in muscle tone and local edema,2 whereas PA mobilization is used to assess joint stiffness. With regard to PA mobilization, reproduction of the patient’s symptoms corresponding to perception of abnormal PA stiffness is one factor used to determine the vertebral level for treatment.3 Although there is increasing emphasis on the reproduction of the patient’s symptoms as a method of identifying the vertebral level to be treated,4-6 the use of PA stiffness as an indicator of the stiffness of the intervertebral joints is still recommended in the clinical examination.3 Despite the common use of lumbar PA mobilization, little is known about which tissues determine the nature of PA stiffness and what causes variation in stiffness between individuals and between vertebral levels.7 Although researchers have used well-controlled procedures to study PA stiffness in reasonably homogeneous groups of subjects, previous research has shown substantial variations of lumbar PA stiffness between subjects.8,9 Variations in lumbar
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Fig 1. Schematic model of manual-applied force to spine, based on the findings of Lee et al.7,28 The force (A) is applied through a spring (B) representing the dorsal soft tissues. The head and the pelvis can be considered to be rigid bodies. The upper spine is supported by a series of springs (K) that represent the ribcage. The pelvis is supported by springs restraining horizontal (C) and vertical (D) movement, and by a spring that resists pelvic rotation about the axis of rotation (E).
PA stiffness have been shown to relate to a number of factors: direction of applied force, posture of lumbar spine, level of spinal muscle activity, rate of loading, position of load, and body type.8-13 It appears that the nature of the support and constraint applied to the spine by the adjacent structures is one factor determining the variations in thoracolumbar PA stiffness.7 Two studies of the effect of plinth surface on PA stiffness14,15 have demonstrated that when a subject lies on a padded plinth, measured PA stiffness is lower than when testing is performed on an unpadded plinth. Our previous study16 has shown that pelvic movement has a significant effect on lower lumbar PA stiffness but no significant effect on mid to upper lumbar PA stiffness. This result indicates that the nature of pelvic constraint is reflected in lumbar movements. Similarly, it has been suggested that the lower values of PA stiffness observed at upper and mid lumbar levels compared to lower lumbar levels are due to the less rigid support offered by the lower ribcage to the spine.7 Previous studies have investigated the ribcage properties17 and their possible relationship to the response to PA spinal loading.7,11 Lee et al17 measured anteroposterior (AP) ribcage stiffness of men and women in response to the load applied to the sternum and reported an average stiffness of 9.4 N/mm. The results showed that male subjects, with greater average AP chest diameters than female subjects, also had greater ribcage stiffness. Edmondston et al11 compared the PA stiffness of T4, T7, and T10 and AP ribcage stiffness. The average AP ribcage stiffness, 7.6 N/mm, was substantially lower than the stiffness in the study by Lee et al.17 They found a significant correlation between the thoracic PA stiffness and AP ribcage stiffness, with the latter accounting for 33% of the variations in thoracic PA stiffness. Lee et al7 investigated the thoracolumbar PA stiffness at T4, T7, T10, L1, and L4 and found that AP chest diameter accounted for 17% of variations in the PA stiffness at T7. They proposed a model of spinal PA loading in which the ribcage, represented by a series of springs, influenced the midthoracic PA stiffness (Fig 1). The findings from all these studies support the idea that ribcage behavior is directly involved in determining thoracic PA stiffness.
Although previous research11 has demonstrated an association between AP ribcage stiffness and the variations in the thoracic PA stiffness, no causal relationship has been demonstrated. The model proposed by Lee et al7 predicts that thoracic and lumbar PA stiffness depend on the amount of deformation of the ribcage. However, this proposition has not been tested. Furthermore, if such a causal relationship does exist, the sensitivity of PA responses to ribcage deformation is unknown. Constraining the ribcage movement and measuring the effect on PA stiffness would show how much ribcage movement in the sagittal plane might contribute to PA stiffness. In terms of the model put forward by Lee et al7 represented in Figure 1, constraining the ribcage movements could increase the stiffness of the springs (Fig 1, K) and hence, increase the PA stiffness. Therefore, in our study we aimed to investigate (1) whether the thoracolumbar PA stiffness differed between 2 conditions of ribcage movement, unconstrained and constrained; and (2) whether the effect of ribcage constraint on PA stiffness varied according to where the PA force was applied.
METHODS Research Design We measured thoracolumbar PA stiffness by using a repeated-measures design with 2 within-subjects factors (vertebral level and ribcage condition) and 1 between-subjects factor (sex). The PA stiffness at T12, L1, L2, L3, and L4 was measured under 2 conditions of ribcage movement (unconstrained and constrained conditions).
Subjects Forty-one subjects (21 women and 20 men) participated in the study. All were students at the University of Sydney selected as a sample of convenience. The study was approved by the Human Ethics Committee of the University of Sydney, and informed consent was obtained from each subject prior to the study. Criteria for inclusion included no current symptoms of thoracic and lumbar pain, and no thoracic and lumbar symptoms that required consultation or treatment within the preceding 12 months. Criteria for exclusion included the
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Table 1. Subject characteristics
Procedure
Variables
Mean (SD)
Range
Age (y) Mass (kg) Height (cm) BMI* (kg/m2) Skinfold* (mm)
24.46 (5.37) 66.61 (10.96) 168.65 (8.51) 23.29 (2.31) 10.76 (4.05)
18–37 48–91 153.0–184.5 18.47–28.07 4.8–26.0
*Skinfold was measured at the level of the xiphisternal junction in the midaxillary line.
presence of pain during testing or of any known spinal or systemic disease, such as inflammatory diseases and infections of the spine, that contraindicated the use of mobilization forces.18 Subjects’ age, sex, mass, and height were recorded. It has been shown that 2 body-type parameters, body mass index (BMI or mass/height)2 and local skinfold thickness, influence lower lumbar PA stiffness.7,9 To evaluate this effect in the thoracolumbar region, we measured midaxillary skinfold thickness at the level of the xiphisternal junction in the midaxillary line, using a skinfold caliper (John Bull British Indicators, Ltd, Burgess Hill, UK) when the subject was standing. We measured the skinfold thickness 3 times and used the average value. The BMI was also calculated to allow an exploration of the relation of overall body type to PA stiffness. The characteristics of the subject group are listed in Table 1.
Equipment We used the Spinal Physiotherapy Simulator (SPS) to measure the PA stiffness. The principal components of the SPS include a variable speed motor, a cam, and a parallelogram linkage. The motor output shaft is connected to the cam by a V-belt and pulley system. Attached to the parallelogram linkage is a loadcell (XTRAN loadcell S1W 250 N, Applied Measurement Pty, Ltd, Eastwood, NSW, Australia) connected to a rubber-padded indenter, which is the part that contacts the subject’s skin while the SPS applies forces. The movement of the indenter is controlled by rotation of the cam, allowing movement of the parallelogram linkage under control of a dead weight. The main function of the SPS is to apply a force to the skin surface overlying a subject’s spinous process and to record the amount of skin displacement in response to the applied force. The force and displacement are then used to calculate stiffness.19 The direction of force applied by the SPS can be adjusted by tilting the device in a cephalad or caudad direction within the sagittal plane. The SPS has good reliability for repeated measurements of L3 PA stiffness (at 0.5 Hz), with an ICC (2,1) of 0.88 being obtained for measurement of 11 subjects without low back pain. It is also accurate in its measurement of stiffness. The maximum error when measuring stiffness of an aluminum beam was found to be less than 1%.19
The subject lay in a prone position on the examination couch, with arms placed by his/her sides. The examiner palpated and identified the spinous processes from C7 to L5. After identification, the spinous processes of T12 and L1-L4 were marked. Screening tests were then performed. A PA force was manually applied from T12 to L4 to ensure that the subject was pain free. The subject was then required to perform active trunk flexion and extension in the standing position. Subjects reporting pain related to the applied PA force or active movements were excluded from the study. The indenter of the SPS was positioned over the spinous process to be tested. By adjusting the SPS frame, then clamping it in the tilted position, the direction of indenter movement to be used for testing was set to the desired angle in the sagittal plane. In this study, the angles (degrees from vertical) used were 9° directed cephalad at T12, 6° cephalad at L1, 3° cephalad at L2, 1° caudad at L3, and 5° caudad at L4. These angles were based on data for sagittal spine curvature20 and on observations of experienced physiotherapists manually applying PA forces to the lumbar spine.21 In our study, we aimed to measure the thoracolumbar PA stiffness under 2 conditions—with ribcage constraint and without ribcage constraint. For the ribcage constraint condition, we used a device to attempt to limit the deformation and displacement of the thorax in the sagittal plane. The ribcage constraint device (Fig 2) consisted of a clamp with 2 curved wooden jaws. The jaws were padded with a thin layer of soft rubber (0.4 cm) for the subject’s comfort. The jaws were firmly pressed against the lateral aspects of the subject’s lower ribcage with a clamp. To standardize the amount of force provided by the clamp, a loadcell connected to a Transducer Readout (RD-201A, Applied Measurement Australia Pty, Ltd) was connected to one side of the ribcage constraint device. For all subjects, the constraint was initially applied with a lateral force of 135 N. The force was gradually increased to this point to ensure that the subjects could tolerate it. The protocol involved 2 tests: (1) the lower thoracic regional stiffness test and (2) the thoracolumbar PA stiffness tests at 5 locations. For every subject, the testing was begun with tests of the lower thoracic regional stiffness in both ribcage conditions to ensure that the ribcage constraint device was effective in reducing thoracic compressibility. The degree of ribcage constraint was evaluated by comparing lower thoracic regional stiffness in the constrained and unconstrained conditions. The force was applied by means of a large, padded (with a thin layer of soft rubber, 0.4 mm thick) wooden indenter (14 cm ⫻ 15 cm ⫻ 1.2 cm) placed on the lower thorax, with the lower edge at the spinous process of T11. The force was applied 5 cm from the lower edge of the wood in the same direction as that used for PA
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Fig 2. Photograph of subject in a constraint device with jaws positioned for the constrained ribcage condition. On the left of the constraint device is a loadcell with readout, which was used to standardize the force used in the constraint.
testing at T12. The order of presentation of constraint of the ribcage was counterbalanced, in that half the subjects received the unconstrained condition followed by the constrained condition, and the other half received the constrained condition followed by the unconstrained condition. After the tests of lower thoracic regional stiffness were completed, we performed the thoracolumbar PA stiffness tests in which the PA force was localized to 1 spinous process at a time. The order of testing at the different vertebral levels was randomly assigned to minimize any systematic effect. In each test, prior to data collection, we applied 3 cycles of force from 0 N to 120 N, using the SPS to precondition the tissues. The aim of preconditioning was to give more reproducible behavior of soft tissues and to familiarize the subject with the testing procedure. Immediately after preconditioning, 5 loading cycles were applied while the force and displacement data were collected. The data were passed to a 12-bit analogue-to-digital converter (DT2801A, Data Translation, Inc, Marlboro, Mass) and stored for subsequent analysis. During each phase of data collection, subjects held their breath at the end of normal expiration. This was done to maintain a lung volume during stiffness testing and to prevent the spinal movement associated with breathing that could confound the stiffness data. Breathing during stiffness testing has been shown to affect PA stiffness.22
Intraexaminer Reliability To investigate the variability in repeated measurements of lower thoracic regional stiffness, a second test in the
unconstrained ribcage condition was conducted immediately after all other tests were performed.
Data Analysis Raw data of force/time and displacement/time were analyzed with special purpose software. The main variables examined in this study were the thoracolumbar PA stiffness values. The stiffness is calculated from the slope of the least-squares regression line fitted to the force-displacement curve between 30 N and 100 N of force.7,9 Lower thoracic regional stiffness was evaluated in the same way. A 3-factor repeated measures analysis of variance ([ANOVA] SPSS, Inc, Chicago, Ill) was used to analyze PA responses. The effect of 2 within-subjects factors (ribcage condition and vertebral level) and 1 between-subjects factor (sex) was examined. The Pearson correlation coefficient was also used to investigate whether PA stiffness in the unconstrained condition was related to skinfold thickness and BMI. We compared the lower thoracic regional stiffness in the unconstrained and constrained conditions, together with analysis of the effect of sex, using ANOVA. Test-retest reliability in measurement of lower thoracic regional stiffness was expressed as an intraclass correlation coefficient (ICC [2,1]). A significance level of P ⬍ .05 was used for all statistical tests.
RESULTS Figure 3 shows the mean PA stiffness at 5 vertebral levels for both conditions of ribcage constraint. The average PA stiffness was lowest at L3 in both conditions (12.8 N/mm unconstrained, 13.4 N/mm constrained). The mean PA stiffness was greatest at T12 in the unconstrained ribcage con-
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Fig 3. PA stiffness at T12-L4 for the unconstrained and constrained ribcage conditions. Error bars represent standard deviations. Table 2. Pearson correlation coefficient values for correlation between PA stiffness* and BMI and skinfold thickness†
PA PA PA PA PA
stiffness stiffness stiffness stiffness stiffness
T12 L1 L2 L3 L4
BMI
Skinfold
0.05 0.28 0.27 0.13 ⫺0.09
⫺0.29 ⫺0.09 ⫺0.14 ⫺0.25 ⫺0.29
*PA stiffness corresponds to the unconstrained condition when loads were applied to T12, L1, L2, L3 and L4. † Skinfold was measured at the level of the xiphisternal junction in the midaxillary line.
dition (14.4 N/mm) and at L4 in the constrained condition (15.2 N/mm). The ANOVA showed a significant difference in the PA stiffness between ribcage conditions (F1,40 ⫽ 14.03), with the mean PA stiffness in the constrained condition being 0.9 N/mm higher than in the unconstrained condition. There was also a significant quadratic trend (F1,40 ⫽ 13.22); that is, as shown in Figure 3, there were high values at both the cephalad and caudad ends of the region tested, and lower values in the middle. Pairwise comparisons indicated that the mean PA stiffness at L3 was lower than the stiffness at T12 and L4. There was no significant interaction between the 2 experimental ribcage conditions and vertebral level of load location. There was no significant variation of PA stiffness due to sex (14.8 N/mm for men, 13.1 N/mm for women). The ANOVA showed that the mean lower thoracic regional stiffness in the constrained condition (12.9 N/mm) was significantly greater than that in the unconstrained
condition (12.0 N/mm) (F1,40 ⫽ 16.16). This indicated that the ribcage constraint device was effective in decreasing thoracic deformation. There was no significant variation in the lower thoracic regional stiffness due to sex. The results of the correlations between PA stiffness and measures of body type are listed in Table 2. For the lower thoracic regional stiffness, the test-retest reliability, ICC (2,1), was 0.82, with a 95% CI of 0.68-0.90.
DISCUSSION Our intent in this study was to examine the effect of ribcage constraint on thoracolumbar PA stiffness and also whether this effect varied in relation to the vertebral level where the PA force was applied. Our results show that ribcage movement does alter thoracolumbar PA stiffness, but for PA forces applied at T12 to L4, the effect does not depend on the location of the applied force. We used a ribcage constraint device to reduce the movement of the posterior ribcage in the sagittal plane and investigate whether that movement was a determinant of thoracolumbar PA stiffness. Effectiveness of the constraint device was shown by a significant increase in the lower thoracic regional stiffness in the constrained compared to the unconstrained ribcage condition. The lower thoracic regional stiffness in the constrained condition was approximately 7% greater than that in the unconstrained condition, corresponding to 0.38 mm (5.57 mm vs 5.96 mm) less displacement of the indenter over the 70 N range of forces considered. Even though this change in stiffness is too small to be clinically detectable,23 it demonstrates the mechanism involved. Despite the fact that the ribcage deformation and displacement were only partially restrained, this amount of
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change was sufficient to show the contribution of the ribcage to the thoracolumbar PA stiffness. The 0.38-mm reduction in posterior ribcage movement produced a mean 0.24-mm decrease in thoracolumbar PA displacement over the same force range; that is, the percentage of reduction in the thoracolumbar PA displacement was 63% of the reduction in posterior ribcage movement. This ratio suggests a high sensitivity of thoracolumbar PA stiffness to posterior ribcage movements. We could therefore speculate that complete prevention of posterior ribcage movement would be likely to result in substantially greater increases in PA thoracolumbar stiffness. In this study, the PA stiffness values corresponding to unconstrained ribcage movement are similar to those in previous studies. The PA stiffness values at L1-L4 reported in previous studies, using the same frequency of loading, ranged between 14.1 N/mm and 17.5 N/mm in asymptomatic subjects.8,9,14 The slightly lower PA stiffness at L1-L4 in our study (12.8-14.0 N/mm) compared to previous studies could be due to the difference in subject characteristics and directions of applied load. In addition, the PA stiffness value at T10 reported in previous studies, using a slower frequency (0.05 Hz), was 10.4 N/mm.7,11 The higher PA stiffness at T12 in our study (14.4 N/mm) compared to previous studies could be due to the differences in frequency of applied force13 and vertebral level. The effect of sex on thoracolumbar PA stiffness of subjects without low back pain in the unconstrained ribcage condition has been previously studied, with different outcomes.7,24,25 Lee et al7 found no effect of sex on PA stiffness at T4, T7, T10, L1, and L4, whereas Allison et al25 reported a 24% greater PA stiffness at L1 and L3 in men compared with women. When considering the material properties of the ribcage related to sex, Lee et al17 found that the mean AP ribcage stiffness, in response to AP load over the sternum, was 8.4 N/mm in women and 10.5 N/mm in men. In our study, we examined the effect of sex on both lower thoracic regional stiffness and thoracolumbar PA stiffness. The mean lower thoracic regional stiffness values in women and men were both 12.0 N/mm. The mean thoracolumbar PA stiffness values in women and men were 12.7 N/mm and 14.3 N/mm, respectively. There were no significant differences between sexes for lower thoracic regional stiffness and thoracolumbar PA stiffness. Previous studies have measured AP ribcage stiffness as 7.6-9.4 N/mm.11,17 We observed lower thoracic regional stiffness of approximately 12 N/mm, which is higher. Lower stiffness might have been expected in the lower thoracic region as a result of the presence of floating ribs in this region and of relatively longer costal cartilages, which have lower stiffness than ribs.26 This apparent paradox may be related to the way the structure stiffness (the ribcage stiffness) has been tested (ie, AP vs PA load, indenter size difference, force direction, and frequency) or the smaller AP diameter in the lower thoracic region. Further investigation
Chansirinukor, Lee, and Latimer Ribcage Movement
of the variation of regional stiffness would be required to resolve this issue. Skinfold thickness and BMI have been previously shown to influence lower lumbar PA stiffness. Viner et al9 found that suprailiac skinfold thickness was a significant determinant of PA stiffness in the low lumbar region (r2 ⫽ .28-.50 at L3-L5). Lee et al7 also found that suprailiac skinfold thickness was significantly correlated (r2 ⫽ .18) with PA stiffness at L4. It has been reported that midaxillary and suprailiac skinfold thickness are highly correlated (r ⫽ .83).7 Therefore, we would expect that the use of midaxillary skinfold thickness would yield a similar outcome to the use of suprailiac skinfold. However, the PA stiffness values in our study showed only weak correlations with midaxillary skinfold thickness (Table 2). This suggests that the amount of subcutaneous fat may not be an important determinant of variation in thoracolumbar PA stiffness. A plausible reason why our results did not show the same relationship between BMI and PA stiffness observed by Viner et al9 is that their subjects showed a larger range of BMI values. Among their subjects were 3 overweight subjects, whose BMIs were more than 30 kg/m2, and 5 underweight subjects, whose BMIs were less than 20 kg/m2. In contrast, the subjects in our study showed more uniform BMIs, with the maximum BMI being 28.07 kg/m2. Interestingly, we found a low correlation between BMI and skinfold thickness (r ⫽ .45, P ⫽ .003), and there was a negative correlation between BMI and skinfold except at the L4 level. This result suggests that the midaxillary skinfold thickness may not correlate well with the subjects’ overall fatness. The model of Lee et al7 suggests that PA stiffness would reflect the stiffness of elements supporting the spine. They hypothesized that PA stiffness would be highest near the pelvis and lower in the midlumbar region (because there is a lack of supporting structures), and increasing in the thorax but lower than near the pelvis (because the ribcage has lower stiffness than the pelvis). In our study, the PA stiffness value at L3 was lower than those values at T12 and L4, and there was a significant quadratic trend of PA stiffness values (Fig 3). This pattern of PA stiffness variation is consistent with the model proposed by Lee et al.7 Our results support the concept behind this model: The deformation and displacement of the structures that support the spine are major contributors to PA displacement. In unconstrained ribcage movement, a thoracolumbar PA force applied to a spinous process may produce a number of responses: intervertebral displacements at many thoracic and lumbar levels, compression of soft tissues on the anterior body surface and overlying the loaded vertebra, deformation and rigid-body displacement of the ribcage, and compression of the abdomen and pelvic rotation.7,13,27,28 There are many possible explanations by which the ribcage constraint could bring about increased thoracolumbar PA stiffness, most of which would be expected also to affect the lower thoracic regional stiffness. When the anterolateral
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clamping of the ribcage was applied, there could have been less movement at the costovertebral and costotransverse joints, less rigid-body motion of the lower thorax, smaller rib and costal cartilage deformations, and less compression of anterior soft tissues. Any of these effects could produce less movement of the vertebral column as a whole. Because we did not measure movements of the individual vertebrae, the extent of contribution of interverebral joints to the reduction in PA movement (and hence increased PA stiffness) is not known. In relation to our experiment, the structures contributing to PA displacement can be hypothesized as originating from 2 major groups—ribcage and nonribcage components (the nonribcage component includes intervertebral joints). Our study showed that the increase in PA stiffness, and hence the reduction in PA displacement due to ribcage constraint, did not significantly differ between vertebral levels, whereas the unconstrained PA stiffness did show significant variations. The findings suggest that although the PA displacement includes substantial contributions from nonspinal structures, the level-to-level variations in PA displacement may be indicative of behavior of the spine. Therefore, the clinical practice of comparing responses between vertebral levels29 may have some validity. We need to remember, however, that these findings cannot necessarily be directly applied to patients with low back pain. The presence of low back pain may be associated with involuntary hyperactivity of the paraspinal muscles. Changes in lumbar extensor muscle activity have been previously shown to increase lumbar PA stiffness.12 Hence, it is possible that the muscle activity of patients with low back pain may also contribute to variations in PA stiffness, and therefore alter the relative importance of the contributions of ribcage and nonribcage components. In the context of decreasing emphasis on the PA stiffness response as a clinically useful sign of spinal disorders,4-6 our results provide a mixed message to clinicians. On one hand, the finding that the thoracolumbar PA stiffness is sensitive to ribcage movements confirms the role of another nonspinal variable as a determinant of the PA response. On the other hand, the relative consistency of the ribcage contribution across a range of vertebral locations allows the possibility that the observed level-to-level variations in PA stiffness may be attributable to spinal tissues, and hence may be of clinical value.
CONCLUSIONS The contribution of the ribcage movement as one part of the mechanism determining the thoracolumbar PA stiffness has been demonstrated. The role of ribcage movement appears uniform across a range of vertebral locations (T12-L4) of the applied force. This finding suggests that although the PA stiffness values along the thoracolumbar spine reflect the properties of nonspinal structures associated with the
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ribcage, these structures may have a similar influence at many locations, and intersegmental variations in PA stiffness might be more indicative of the properties of other tissues, such as intervertebral joints.
REFERENCES 1. Maitland GD, Banks K, English K, Hengeveld E, editors. Maitland’s vertebral manipulation. 6th ed. Oxford, UK: Butterworth-Heinemann; 2001. p. 351-3. 2. Kawchuk G, Herzog W. A new technique of tissue stiffness (compliance) assessment: its reliability, accuracy and comparison with an existing method. J Manipulative Physiol Ther 1996;19:13-8. 3. Edwards BC. Examination. In: Maitland GD, Banks K, English K, Hengeveld E, editors. Maitland’s vertebral manipulation. 6th ed. Oxford, UK: Butterworth-Heinemann; 2001. p. 146-58. 4. Maher C, Latimer J. Pain or resistance—the manual therapists’ dilemma. Aust J Physiother 1992;38:257-60. 5. Lee M, Latimer J, Maher C. Manipulation: investigation of a proposed mechanism. Clin Biomech 1993;8:302-6. 6. Maher C, Adams R. Reliability of pain and stiffness assessments in clinical manual lumbar spine examination. Phys Ther 1994;74:801-11. 7. Lee M, Steven GP, Crosbie J, Higgs R. Variations in posteroanterior stiffness in the thoracolumbar spine: preliminary observations and proposed mechanisms. Phys Ther 1998;78: 1277-87. 8. Lee M, Liversidge K. Posteroanterior stiffness at three locations in the lumbar spine. J Manipulative Physiol Ther 1994; 17:511-6. 9. Viner A, Lee M, Adams R. Posteroanterior stiffness in the lumbosacral spine: the correlation between adjacent vertebral levels. Spine 1997;22:2724-30. 10. Caling B, Lee M. Effect of direction of applied mobilization force on the posteroanterior response in the lumbar spine. J Manipulative Physiol Ther 2001;24:71-8. 11. Edmondston SJ, Allison GT, Gregg CD, Purden SM, Svansson GR, Watson AE. Effect of position on the posteroanterior stiffness of the lumbar spine. Man Ther 1998;3:21-6. 12. Lee M, Esler M-A, Mildren J, Herbert R. Effect of extensor muscle activation on the response to lumbar posteroanterior forces. Clin Biomech 1993;8:115-9. 13. Lee M, Svensson NL. Effect of loading frequency on response of the spine to lumbar posteroanterior forces. J Manipulative Physiol Ther 1993;16:439-46. 14. Latimer J, Holland M, Lee M, Adams R. Plinth padding and measures of posteroanterior lumbar spine. J Manipulative Physiol Ther 1997;20:315-9. 15. Maher CG, Latimer J, Holland MJ. Plinth padding confounds measures of posteroanterior spinal stiffness. Man Ther 1999; 4:145-50. 16. Chansirinukor W, Lee M, Latimer J. Contribution of pelvic rotation to lumbar posteroanterior movement. Man Ther 2001; 6:242-9. 17. Lee M, Hill S, Scullin J. Ribcage compressibility in living subjects. Clin Biomech 1994;9:379-80. 18. Brewerton DA. The doctor’s role in diagnosis and prescribing vertebral manipulation. In: Maitland GD, Banks K, English K, Hengeveld E, editors. Maitland’s vertebral manipulation. 6th ed. Oxford, UK: Butterworth-Heinemann; 2001. p. 17-9. 19. Lee M, Svensson NL. Measurement of stiffness during simulated spinal physiotherapy. Clin Phys Physiol Meas 1990;11: 201-7.
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20. Reynolds HM, Rechtien JJ, Marshall GW, Marshall S. Spinal curvature of young adult females. Hum Biol 1986;58:88391. 21. Viner A, Lee M. Direction of manual force applied during assessment of stiffness in the lumbosacral spine. J Manipulative Physiol Ther 1995;18:441-7. 22. Beaumont A, McCrum C, Lee M. The effects of tidal breathing and breath-holding on the postero-anterior stiffness of the lumbar spine. Proceedings of the 7th Biennial Conference of the Manipulative Physiotherapists Association of Australia; 1991 Nov 27-30; Leura, NSW, Australia. Victoria, Australia: Manipulative Physiotherapists Assoc of Australia; 1991. 23. Nicholson L, Adams R, Maher C. Reliability of a discriminant measure for judgements of non-biological stiffness. Man Ther 1997;2:150-6. 24. Lee M, Steven GP. Modelling the trunk responses to lumbar manipulative forces. In: Middleton J, Jones ML, Pande GN, editors. Computer methods in biomechanics and biomedical
Chansirinukor, Lee, and Latimer Ribcage Movement
25.
26. 27. 28. 29.
engineering—2. Amsterdam: Gordon and Breach Science Pub; 1998. p. 371-8. Allison GT, Edmondston SJ, Roe CP, Reid SE, Toy DA, Lundgren HE. Influence of load orientation on the posteroanterior stiffness of the lumbar spine. J Manipulative Physiol Ther 1998;21:1-5. Roberts SB, Chen PH. Elastostatic analysis of the human thoracic skeleton. J Biomech 1970;9:185-92. Lee M, Lau H, Lau T. Sagittal plane rotation of the pelvis during lumbar posteroanterior loading. J Manipulative Physiol Ther 1994;17:149-55. Lee M, Kelly DW, Steven GP. A model of spine, ribcage and pelvic responses to a specific lumbar manipulative force in relaxed subjects. J Biomech 1995;28:1403-8. Jull G. Examination of the articular system. In: Boyling J, Palastanga N, editors. Grieve’s modern manual therapy: the vertebral column. Edinburgh, Scotland: Churchill Livingstone; 1994. p. 520-2.
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