A Comparison of Clinical Spinal Mobility Measures to Experimentally Derived Lumbar Spine Passive Stiffness

in Journal of Applied Biomechanics

Spinal stiffness and mobility assessments vary between clinical and research settings, potentially hindering the understanding and treatment of low back pain. A total of 71 healthy participants were evaluated using 2 clinical assessments (posteroanterior spring and passive intervertebral motion) and 2 quantitative measures: lumped mechanical stiffness of the lumbar spine and local tissue stiffness (lumbar erector spinae and supraspinous ligament) measured via myotonometry. The authors hypothesized that clinical, mechanical, and local tissue measures would be correlated, that clinical tests would not alter mechanical stiffness, and that males would demonstrate greater lumbar stiffness than females. Clinical, lumped mechanical, and tissue stiffness were not correlated; however, gradings from the posteroanterior spring and passive intervertebral motion tests were positively correlated with each other. Clinical assessments had no effect on lumped mechanical stiffness. The males had greater lumped mechanical and lumbar erector spinae stiffness compared with the females. The lack of correlation between clinical, tissue, and lumped mechanical measures of spinal stiffness indicates that the use of the term “stiffness” by clinicians may require reevaluation; clinicians should be confident that they are not altering mechanical stiffness of the spine through segmental mobility assessments; and greater resting lumbar erector stiffness in males suggests that sex should be considered in the assessment and treatment of the low back.

Spinal mobility is commonly assessed by clinicians for individuals with low back pain (LBP) and is an important factor for informing patient diagnosis, prognosis, and plan of care.14 Segmental mobility may provide insight on spine health and function, given that in vitro findings of tissue injury and degeneration have been correlated with atypical spinal stiffness or laxity.57 Spinal stiffness is frequently inferred from clinical assessments8; however, the relationship between spinal stiffness and LBP is complex and ill-defined. Disparate findings in spinal stiffness have been observed between patients with LBP and back-healthy control participants.911 As well, reduced spinal stiffness has been observed in patients reporting clinical LBP improvement following manipulation/mobilization therapies.12,13 Contributing to the complexity in interpreting findings from the literature are the variety of definitions and methods used to evaluate spinal stiffness, which are often inconsistent between clinical and research settings.

Common approaches for clinical assessment of segmental spinal mobility include the posteroanterior (PA)-spring and passive intervertebral motion (PIVM) tests. These tests are used to evaluate the quality and quantity of intervertebral joint motion, and clinicians rate mobility by classifying the joint as hypomobile, hypermobile, or normal.8,1419 Clinicians may also assess active range of motion (AROM) as a measure of overall lumbar spine mobility.20 Although these assessments are widely used, it is not always clear whether the information gained from them should be interpreted as spinal stiffness, mobility, stability, or a combination of these. For example, Landel et al15 found poor agreement between mobility assessment with the PA-spring test and segmental spine movement, defined as the angular difference between adjacent vertebral endplates between resting and end-range of motion (ROM),16,21 concurrently observed using dynamic magnetic resonance imaging. The authors concluded that clinicians using the PA-spring test may be perceiving resistance to motion, which they describe as stiffness of the specific spinal motion segment, in addition to the magnitude of motion.15,16 There is also a lack of consensus on the evaluation criteria for spinal mobility using the PIVM test22 and poor understanding of the test validity, given that no true gold standard has been established23 and only one author has attempted to quantify validity based on a radiographic reference.3,24 Because clinical assessments of spinal segmental mobility have limited reliability when used in isolation, some combination of the tests may be more useful for evaluating patients with LBP, particularly when stiffness inferences are being made.1518,2429 Although these clinical tests have been considered to measure spinal mobility, stiffness, and stability, for our purposes, they will be considered measures of spinal mobility, given the clinical grading nomenclature.

Several quantitative measurement techniques have been developed to evaluate spinal stiffness. Lumped mechanical stiffness of the lumbar spine has been measured using a passive, side-lying, nearly frictionless jig.3035 This in vivo method generates a moment–angle curve for the entire lumbar spine (hence “lumped,” as opposed to segmental stiffness), evaluating all segments together in spinal flexion. From the moment–angle curve, the slopes and breakpoints provide a quantitative, mechanical measure of stiffness for the lumbar spine according to the properties associated with a load–deformation relationship.36 The results may be confounded by stiffness contributions from nonspinal soft tissues in the trunk (ie, muscles, fascia, organs, adipose tissue), and by the method of curve-breakpoint selection. This technique has been effective in quantifying lumbar stiffness changes associated with prolonged sitting30,31 and repetitive lifting.34 While the passive jig approach is commonly used in biomechanics research,30,31,33,34,37 it is unknown whether this measure of mechanical stiffness correlates with the previously described clinical approaches. For this investigation, stiffness derived from the jig will be referred to as lumped mechanical stiffness, defined as the passive rotational resistance of the lumbar spine to a flexion moment.

Another quantitative technique for measuring mechanical stiffness of specific tissues is myotonometry.38,39 A myotonometer measures the resistance of a tissue to an impulse force applied to the overlying skin and quantifies stiffness based on the damped natural oscillation response of the tissue.40,41 This technique is reliable in measuring stiffness of the lumbar erector spinae in back-healthy controls38 and has identified greater lumbar erector spinae stiffness in females with LBP compared with controls41 and older patients with LBP,42 as well as greater lumbar myofascial stiffness in patients with ankylosing spondylitis compared with age-comparable controls.43 Myotonometry is unable to determine joint stiffness; however, when used in conjunction with the previously described passive jig, it may provide powerful insight into how tissues of the low back contribute to the lumped mechanical stiffness measure. For this investigation, tissue stiffness is defined as the passive resistance of the tissue to an external, 15-millisecond impulse force applied by the myotonometer (0.18 N preload, plus 0.40 N impulse), quantified by the logarithmic decrement of the oscillation of the tissue.44 Specifically, stiffness is calculated as the multiple of the peak acceleration recorded and the mass of the device indenter, divided by the peak displacement of the tissue.44

Although all described assessments of in vivo spinal stiffness have limitations, 15,17,18,2527 a disconnect exists in how spinal stiffness and mobility are evaluated, particularly in comparing clinical and mechanical measures. This disconnect makes it difficult for translation of findings between fields, potentially hindering our understanding of spinal stiffness and mobility and how they relate to the etiology, progression, and treatment of LBP. Given this uncertainty, our main objective was to determine whether the different measurement approaches provide similar information. Specifically, we were interested in whether clinical tests of mobility at the level of L3/4 (PA-spring and PIVM) correlate with lumped lumbar mechanical stiffness evaluated on a passive flexion jig, if either clinical or lumped mechanical stiffness is correlated with lumbar tissue (muscle and ligament) stiffness measured using myotonometry (MyotonPRO(R)), and whether clinical tests are correlated with each other. In evaluating these correlations, we aimed to examine the accuracy of the terminology, as well as the outcome of the tests. Only the L3/4 motion segment was assessed because we aimed to compare clinical measures with tissue stiffness in the same spinal region. The myotonometer guidelines indicated that muscle stiffness should be measured where borders can be clearly defined,44 and the lumbar erector spinae cross-sectional area has been shown to be greatest at approximately the level of L3/4 for both males and females.4547 As well, given that stiffness in the lumbar spine will be taken up at all lumbar segments, the point of rotation of the lumbar spine for lumped mechanical stiffness was assumed to exist at the approximate midpoint (L3). As secondary objectives, we wanted to confirm whether lumped mechanical stiffness changes following clinical assessment, as well as to identify any possible sex differences in tissue stiffness. We hypothesized that clinical and lumped mechanical stiffness measures would be correlated, both clinical and lumped mechanical stiffness would be correlated with tissue stiffness, clinical tests would be correlated with each other, clinical assessments would not alter lumped mechanical stiffness, and males would demonstrate greater tissue stiffness than females.6

Methods

A total of 71 healthy adults not reporting inflammatory or infectious disease affecting the spine, osteoporosis, past spinal surgery, or current pregnancy and reporting no LBP for the last 3 months participated (see Table 1 for demographics). The participants provided informed consent, and the study was approved by the institutional review boards of both the University of Waterloo and Regis University. The study was a double-blinded, cross-sectional design. The protocol is outlined in Figure 1. Clinical assessments were performed by second-year physical therapy doctoral students with demonstrated competency in the techniques through previous coursework and supervised by a licensed physical therapist. All randomizations were determined by a coin flip. The dominant side was based on participant self-reporting of handedness for writing.

Table 1

Participant Demographics Across All Participants and Separated by Sex

Descriptive StatisticsAge, yMass, kgHeight, mBMI, kg/m2AROM, degPassive ROM, dega
Combined (N = 71)
 Mean26.270.61.7124.04543
 SD7.111.30.822.698
 Maximum64103.41.8731.96364
 Minimum2047.21.5518.52520
Males (n = 34)
 Mean25.077.41.7625.04542
 SD5.19.46.202.5108
 Maximum50103.41.8631.96355
 Minimum2159.41.6220.62520
Females (n = 37)
 Mean27.464.41.6623.24544
 SD8.49.27.222.487
 Maximum6486.21.8728.86064
 Minimum2047.21.5518.53031

Abbreviations: AROM, active ROM; BMI, body mass index; ROM, range of motion. Note: AROM refers to the lumbar active ROM measured using dual inclinometry. Passive ROM refers to the lumbar passive ROM measured in the jig.

aPassive ROM data are reported for 62 participants (30 males). See Table 3 for participant exclusion criteria.

Figure 1
Figure 1

—The experimental protocol outlining the order of lumbar AROM testing, EMG instrumentation, lumbar mechanical stiffness measurement (Jig), clinical testing (PA-spring and PIVM), and tissue stiffness testing of the supraspinous ligament and lumbar erector spinae muscle using myotonometry. Randomized steps are indicated with dashed arrows. AROM indicates active range of motion; EMG, electromyography; PA, posteroanterior; PIVM, passive intervertebral motion.

Citation: Journal of Applied Biomechanics 36, 6; 10.1123/jab.2020-0030

Active ROM

Lumbar flexion AROM was assessed in standing using dual inclinometry.48 Inclinometers were positioned over the T12 and S2 spinous processes in upright stance. The participants were instructed to bend forward as far as they could with knees extended, and the angular difference between the device readings was recorded. This measurement approach isolates the lumbar ROM from hip and pelvis contributions.49

Electromyography

Electrical activity of the lumbar erector spinae (L3 level) on the participants’ nondominant side was monitored with surface electromyography to ensure flexion motion was passive during the jig trials (MyoTrac2; Thought Technology Ltd, Montreal, CA).30,32 Standard procedures were used for skin preparation and electrode (EMG Triode Electrode T3402M; Thought Technology Ltd) placement.32 The participants performed 2 submaximal reference contractions in the prone position, knees flexed 90°, and hands placed behind the head, while lifting their thighs off the table for 3 seconds.50 Passivity was assumed if muscle activation was <2% of the peak of 2 trials.

Kinematics and Lumped Mechanical Stiffness Assessment

Two reflective markers were placed over the S2 and T12 spinous processes to define the lumbar flexion angle in the jig (Figure 2A). The jig was used to quantify lumped mechanical stiffness, and the design was based on systems used in previous studies.30,31,3335 The jig provides a nearly frictionless surface, with a plexiglass-lined upper-body cradle, floating on Hudson bearings (Figure 2A). A digital camera (PowerShot G7 X Mark II; Canon Inc, Ōta, Tokyo, Japan) was used to capture kinematic data at 30 Hz for digitization in MaxTRAQ (MaxTRAQ Standard V2.8.4.4; Innovision Systems Inc., Columbiaville,  MI). The participants were positioned side-lying, with the lower body/pelvis constrained on an immobile platform and the torso resting on a mobile upper body cradle. The participants’ torso and pelvis were braced anteriorly to isolate lumbar flexion motion. The starting position for the flexion trial was a neutral spine alignment in both the frontal and sagittal plane, where sagittal neutral was defined as the point where the participant naturally came to rest on the bearing surface with muscles inactive.

Figure 2
Figure 2

—(A) The side-lying jig used to evaluate lumped mechanical stiffness of the lumbar spine. (B) A representative example of the moment-angle curve derived from the passive jig to evaluate lumped mechanical stiffness of the lumbar spine. Slope zones are labeled according to “low,” “transition,” and “high” stiffness zones. Slope breakpoint locations are indicated with an arrow.

Citation: Journal of Applied Biomechanics 36, 6; 10.1123/jab.2020-0030

When relaxed, the participants were drawn into maximum lumbar flexion via a rigid bar, with the speed guided by a 60-beats-per-minute metronome. Maximum flexion was defined as the point at which the investigator could not pull the participant into greater flexion or when the participant verbally indicated that they were at their end ROM. Applied force was measured by a uniaxial load cell at 1200 Hz (MLP-300-CO; Transducer Techniques, Temecula, CA) attached to the bar. To avoid inducing viscoelastic changes associated with prolonged time spent in full lumbar flexion,51 one familiarization trial was performed, followed by the recorded test trial.

Kinematic and force data were filtered using a dual-pass low-pass second-order Butterworth filter (effective cutoff frequency of 3 Hz).32 The flexion moment was calculated by multiplying the time-varying moment arm (L3 to the point of force application) by the perpendicular pull force. The lumbar flexion angle was calculated based on vectors derived from S2 and T12 markers, normalized to the initial neutral position.

Moment–angle curves were constructed based on the flexion motion to determine passive lumbar spinal stiffness. The motion window of interest was defined as the region between where both the flexion moment and angle exceeded 1 N·m and 1°, respectively, and the peak flexion moment. An algorithm was used to fit the moment–angle data to give the least sum of squares with a piecewise linear curve with 2 breakpoints.52 Given the set of ordered pairs (lumbar flexion moment and angle) and specifying that 2 breakpoints should be found, the algorithm determines 2 breakpoint locations within the range of the measured angles, which minimized the squared error between the linear fit and the original data. The 2 breakpoints (low/high) effectively divide the curve into 3 segments representing low, transition, and high stiffness zones (Figure 2B). Steeper slopes and shifts of the breakpoints to the right compared with the baseline indicate higher stiffness.33

Clinical Measures of Stiffness and Mobility

Following the jig trial, clinical tests and myotonometry were performed in randomized order. PA-spring was assessed with the participant prone while the examiner manually applied a posterior-to-anterior force over the L3 spinous process during the participant’s natural exhale. Force was applied and released over 1 to 2 seconds to move the segment through its complete and available ROM.13,19,53 PIVM testing was performed in a side-lying position with the palpation of the L3/4 interspinous space while passively flexing the lumbar spine by moving the knees toward the torso.19 L3/4 motion segments were assessed as hypermobile, hypomobile, or normal for both the PA-spring and PIVM tests, based on previously established criteria.19,54 Each test was performed by 2 examiners, blinded to each other’s assessment. If the rating for a single test differed between the examiners, a third examiner was used as a tie breaker. If all 3 examiners disagreed, that measure was removed from the analysis. Interrater testing suggested excellent reliability (intraclass correlation coefficient > .95) for the 6 examiners for the PIVM and PA-spring tests on a single participant prior to the data collections for this work.

Lumbar Erector Spinae and Supraspinous Ligament Stiffness

Tissue stiffness was measured for the supraspinous ligament and lumbar erector spinae muscle in randomized order (MyotonPRO®; Myoton AS, Tallinn, Estonia). Supraspinous ligament stiffness was measured in the interspinous space between L3/4 while the participant lay prone over a bolster in slight lumbar flexion. Lumbar erector spinae muscle stiffness was measured over the dominant side while the participant lay prone in a neutral spine position.40 Ten repeated impulses were applied with the myotonometer, and the values were deemed acceptable if the coefficient of variation was ≤3%.55,56 Finally, the participants returned to the jig for a repeated measure of lumped mechanical stiffness.

Statistics

Correlations between clinical mobility and lumped mechanical and tissue stiffness were evaluated using Pearson or Kendall tau correlations, as appropriate (Table 2) (SAS® Studio version 3.6; SAS Institute Inc, Cary, NC). Certain characteristics of the moment–angle curve were included in correlations with clinical and myotonometer measures because of expected relationships and to reduce type II error.57 PA-spring grading was compared with stiffness in the “high” zone (slope) because the PA-spring is thought to evaluate the linear elastic region of segmental motion, which is observed at the end range,58 and therefore may be congruent with the stiffest zone of the moment–angle curve. PIVM-grading was compared with the second breakpoint of lumped mechanical stiffness because clinicians evaluated the initiation of motion of L3 on L4 and the amount of motion occurring before the adjacent motion segment begins to move; because both the PIVM and second breakpoint assess or indicate a marked change in stiffness, both may be measuring the same spinal property. Stiffness in the “low” zone (slope) was compared with tissue stiffness because both ligament59 and passive muscle60,61 stiffness differ depending on tissue length, and both tests evaluated stiffness at or near resting length.

Table 2

Statistical Methods and Dependent Variables Applied for Relevant Comparisons With Regard to the Proposed Questions

Dependent variablesStatistical testComparisonsNumberb
Are clinical tests for stiffness at L3/4 correlated with lumped mechanical stiffness?
 Lumped mechanical stiffness—high zone

 PIVM

 PA-spring
Kendall τHigh slopea vs PA-spring

Second breakpointa vs PIVM
2
Are clinical tests correlated with tissue stiffness measured by the MyotonPRO®?
 PIVM

 PA-spring

 Tissue stiffness
Kendall τPIVM vs lumbar erector spinae

PIVM vs supraspinous ligament

PA-spring vs lumbar erector spinae

PA-spring vs supraspinous ligament
4
Is lumped mechanical stiffness correlated with tissue stiffness measured by the MyotonPRO®?
 Lumped mechanical stiffness—low zone

 Tissue stiffness
Spearman RLow slopea vs lumbar erector spinae

Low slopea vs supraspinous ligament
2
Are clinical tests of spine stiffness at L3/4 correlated with each other?
 PIVM

 PA-spring

 AROM
Kendall τPIVM vs PA-spring vs AROM3
Is LMS altered by clinical assessment of stiffness? Does sex affect this relationship?
 Stiffness zones

 Time (baseline/post)

 Sex
Mixed general linear model

(3 × 2 × 2)
Low/transition/high slope

vs

Baseline/postclinical

vs

Male/female
 Breakpoints

 Time (baseline/post)

 Sex
Mixed general linear model

(2 × 2 × 2)
First/second breakpoint

vs

Baseline/postclinical

vs

Male/female
Are there sex differences in stiffness measured by the MyotonPRO®?
 Tissue

 Sex
t TestMale vs female (lumbar erector spinae)

Male vs female (supraspinous ligament)

Abbreviations: AROM, lumbar active range of motion; PA-spring, posteroanterior spring test at L3; PIVM, passive intervertebral motion test at L3/4.

aAll lumped mechanical stiffness data used in the correlations are from the baseline (ie, preclinical) trial. bIndicates the number of correlations performed.

Mixed general linear models were used to evaluate whether application of the clinical tests altered lumped mechanical stiffness (moment–angle slopes) and whether sex differences exist in lumped stiffness (Table 2). Where appropriate, the Mauchly test was used to evaluate sphericity and Greenhouse–Geisser-corrected P values were used when assumptions were violated. t tests were used to investigate sex differences in tissue stiffness (Table 2). For descriptive purposes, a dependent t test was used to evaluate differences in lumbar ROM between active and passive tests, and independent t tests were used to evaluate sex differences in lumbar ROM. For all analyses, the alpha level for significance was set a priori at .05 and Bonferroni adjustments were made to account for multiple comparisons. No effect of clinical assessment was found for lumped mechanical stiffness; therefore, correlations involving these measures were made using the preclinical (baseline) values.

Results

A total of 71 participants completed the protocol. The average lumbar AROM for all participants was 45° (9°) (Table 1). Comparing lumbar AROM with passive ROM in the jig, there was no difference in average ROM between the methods (t = .73, P = .465) (Table 1). No sex difference in lumbar ROM was observed using either method (AROM: t = .34, P = .794; passive ROM: t = .56, P = .184). The aggregate descriptive summary of the clinical findings and the number of participants assessed and retained for each test is summarized in Table 3, with the statistical results relating to the hypotheses in Table 4 (correlations) and Table 5 (analysis of variances and t tests).

Table 3

Summary Description of the Data Set, Clinical Classifications, and Exclusion Factors

AssessmentNumber of participants assessedNumber of participants retainedClinical classificationReasons for exclusion
AROM7171
Lumped mechanical stiffness (correlations)7162In the baseline evaluation:

–Participants were unable to remain passive

–Technical errors
Lumped mechanical stiffness (ANOVA)7153In either the baseline or the postclinical evaluations:

–Participants were unable to remain passive

–Technical errors
PA-spring7166Hypomobile: 22

Normal: 37

Hypermobile: 7
–All 3 examiners disagreed with the grading
PIVM7168Hypomobile: 12

Normal: 42

Hypermobile: 14
 –All 3 examiners disagreed with the grading
Tissue tests (Myoton)6767

Abbreviations: ANOVA, analysis of variance; AROM, lumbar active range of motion; PA-spring, posteroanterior spring test at L3; PIVM, passive intervertebral motion test at L3/4.

Table 4

Summary of the Data and Statistical Findings for Tests of Correlation

Dependent variablesStatistics
Are clinical tests for stiffness at L3/4 correlated with lumped mechanical stiffness?
 PA-springHigh slope, N·m/degτP#
 19 – 31 – 72.26 (1.25)−.060.57357
 PIVMSecond breakpoint, deg   
 12 – 35 – 1237.1 (8.5)−.067.52259
Are clinical tests correlated with tissue stiffness measured by the MyotonPRO®?
 PA-springLumbar erector spinae stiffness, N/mτP#
 21 – 35 – 6247.1 (63.6)−.023.820 
 Supraspinous ligament stiffness, N/m  62
 387.6 (134.2)−.145.155 
 PIVMLumbar erector spinae stiffness, N/mτP#
 11 – 41 – 12242.8 (64.5).031.754 
 Supraspinous ligament stiffness, N/m  64
 374.2 (134.7).118.235 
Is lumped mechanical stiffness correlated with tissue stiffness measured by the MyotonPRO®?
 Low slope, N·m/degLumbar erector spinae stiffness, N/mrP#
 0.2 (0.1)246.2 (64.2)−.024.856 
 Supraspinous ligament stiffness, N/m  60
 383.7 (136.1)−.209.109 
Are clinical tests of spine stiffness at L3/4 correlated with each other? 
 PA-springPIVMτP#
 22 – 34 – 710 – 39 – 14.540<.00163
 PA-springAROM, deg   
 22 – 37 – 744.8 (9.1).159.11466
 PIVMAROM, deg   
 12 – 42 – 1444.7 (9.2).092.35368

Abbreviations: #, the total number of participants included in the statistical test; τ, Kendall Tau correlation coefficient; r, Pearson correlation coefficient; PA-spring, posteroanterior spring test at L3; PIVM, passive intervertebral motion test at L3/4. Note: For clinical tests (PA-spring/PIVM), # – # – # refers to the number of participants included in the correlation who were characterized as hypomobile-normal-hypermobile. Values are reported as mean (SD). Bold values indicate statistical significance.

Table 5

Summary of the Data and Statistical Findings for ANOVAs and t Tests

Dependent variablesStatistics
Is lumped mechanical stiffness altered by clinical assessment of stiffness? Does sex affect this relationship?
 Lumped mechanical stiffness slope, N·m/degFP#
  Sex main effect
  ♀   
  0.91 (1.1)1.16 (1.2)4.31.043 
  Time main effect
  Pre (Baseline)Post   
  1.0 (1.2)0.99 (1.1)0.97.329 
  Time × sex interaction effect
  Pre ♀Post ♀Pre ♂Post ♂   
  0.94 (1.1)0.89 (1.1)1.19 (1.31)1.14 (1.11)0.00.969 
 Breakpoints, deg  53
  Sex main effect
  ♀   
  29.7 (11.6)28.4 (11.2)0.17.681 
  Time main effect
  Pre (Baseline)Post   
  29.6 (10.5)28.7 (12.3)0.01.908 
  Time × sex interaction effect
  Pre ♀Post ♀Pre ♂Post ♂   
  29.7 (10.8)29.6 (12.5)29.4 (10.3)27.3 (12.2)0.25.619 
Are there sex differences in stiffness measured by the MyotonPRO®?
 Lumbar erector spinae tissue stiffness, N/mtP#
  ♀   
  227.2 (65.6)262.0 (57.1)−2.32.02467
 Supraspinous ligament tissue stiffness, N/m
  ♀  
  358.7 (150.7)398.8 (112.9)−1.23.223

Abbreviations: ♂, male; ♀, female; ANOVAs, analysis of variances; #, heading refers to the total number of participants included in the statistical test. Values are reported as mean (SD). Bold values indicate statistical significance.

Clinical mobility tests at L3/4 were not correlated with lumped mechanical stiffness evaluated in the passive jig. Specifically, stiffness in the high stiffness zone did not correlate with the results of the PA-spring test, nor was the second breakpoint location related to stiffness assessed by the PIVM. Clinical mobility tests were not correlated with supraspinous ligament or erector spinae muscle stiffness. Lumped mechanical stiffness in the low stiffness zone was not correlated with either tissue stiffness. The PA-spring and PIVM test findings were significantly positively correlated. There were no correlations between lumbar AROM and the PA-spring or PIVM tests.

A main effect of sex on lumped mechanical stiffness was identified. The males had greater lumbar stiffness compared with the females by ∼0.25 N·m per degree, measured across the entire flexion moment–angle curve. There was no time × sex interaction, nor were there any other interaction effects (zone × sex: F = 2.17, P = .147; time × zone: F = 1.70, P = .198; time × zone × sex: F = 0.79, P = .390). There was no difference between males and females in lumped mechanical stiffness when evaluated by breakpoint location. Lumped mechanical stiffness based on curve breakpoint did not change following the clinical test application, nor was there a significant interaction effect with participants’ sex, nor were there any other interaction effects (breakpoint × sex: F = 0.39, P = .534; time × breakpoint: F = 0.35, P = .559; time × breakpoint × sex: F = 0.21, P = .648). Sex differences in tissue stiffness were found; specifically, the males had significantly greater erector spinae stiffness by ∼35 N/m compared with the females. There were no sex differences for supraspinous ligament stiffness.

Discussion

The primary objective of this study was to determine if in vivo mechanical testing of spinal stiffness and clinical segmental mobility assessments provide similar information in the lumbar spine. Contrary to our hypothesis, the only significant correlation was between the results of the PA-spring and PIVM tests. As expected, the clinical assessments did not change lumped lumbar stiffness. In partial support of the hypothesis, the males demonstrated greater lumbar erector spinae stiffness and greater lumped mechanical stiffness in lumbar flexion when evaluated across all 3 zones; however, supraspinous ligament stiffness did not differ between the sexes. To the authors’ knowledge, this study is the first work to compare clinical measures of lumbar spine mobility with mechanical and tissue stiffness measures.

Because the clinical tests are thought to provide information similar to stiffness16,22 and the PIVM is assessed with similar body-positioning, we expected that mechanical stiffness from the passive jig would correlate positively with the gradings from the PA-spring and, particularly, the PIVM. Contrary to our hypothesis, there were no significant correlations between the clinical measures and lumped mechanical stiffness. Although all measures were taken at the end ROM, it is possible that no associations were found because the passive jig evaluates the spine in flexion, whereas PA-spring testing evaluates in extension.16 Thus, the joint and tissues were challenged differently. In addition, the lumped mechanical assessment provides a measure of the entire lumbar region, whereas the PA-spring and PIVM assess a single-motion segment. To reconcile localized and regional assessments, correlations between the “high” zone slope of the moment–angle curve and PA-spring findings were performed because both evaluate the linear elastic stiffness region through the end ROM.58 Similarly, PIVM testing assesses segmental mobility during flexion in a side-lying position, which is analogous to the flexion motion in the passive jig. Also, during the PIVM, clinicians assessed motion initiation and the amount of motion occurring before the next motion segment begins to move; therefore, to reconcile localized and regional assessments, PIVM grading and the second breakpoint from the moment–angle curve, where stiffness properties demonstrate a marked change, were compared. Given these considerations, this leads us to conclude that the clinically applied mobility tests do not provide information about the lumped mechanical stiffness of the lumbar spine.

There is conflicting evidence from in vitro studies regarding the correlation in stiffness between adjacent lumbar spine segments in humans to explain why segmental mobility measures did not correlate with lumped mechanical stiffness in the current study. van Engelen et al62 report that neighboring lumbar spine segments can have significantly different mechanical properties; however, this was not the case when stiffness was evaluated about the flexion/extension axis, which was the primary axis assessed in the current study. Similarly, Zirbel et al63 showed no effect of segment level on in vitro flexion/extension stiffness of the lumbar spine, although hysteresis, another viscoelastic property, was affected. In contrast, Panjabi et al64 assessed segmental motion (as compared with stiffness) in vitro and reported greater motion moving caudally through the lumbar intervertebral segments. When measured in vivo, there is a lack of consensus on how lumbar segment level affects stiffness.14 While some evidence suggests that stiffness at a single lumbar segment may relate to properties of the entire lumbar spine, the findings in the current study were unable to demonstrate such a correlation.

The lack of correlation between erector spinae muscle and supraspinous ligament stiffness with lumped mechanical stiffness and with the clinical tests provides evidence that there are multiple contributors to passive mechanical stiffness and segmental mobility in the lumbar spine, apart from the measured superficial passive tissue constraints. That lumped mechanical stiffness did not correlate with tissue stiffness may be because many passive tissues contribute to the measure. This rationale is supported by models of load sharing in the lumbar spine, which, although analyzed in simulated standing lumbar flexion, imply that many passive tissues, particularly the intervertebral disc and capsular ligaments, provide significant contribution to resisting an anterior flexion moment.6567 As well, methodological differences may explain why the lumped mechanical stiffness and myotonometry findings were not coincident. Myotonometer measures of muscle and ligament stiffness provide tissue properties from force applied perpendicular to the primary line of action of the tissue, which is important because the muscle and ligament are anisotropic.6870 Therefore, we would not necessarily expect tissue stiffness from the myotonometer to correlate with either lumped mechanical stiffness or PIVM gradings, due to differences in force application directionality. Given that both the PA-spring and myotonometry challenge the tissue in a similar direction, we expected a positive correlation between these measures, although none was found. While this may be due to different tissues being assessed in each approach (ie, the PA-spring evaluates many soft and spinal tissues resisting an applied force at a single segment, as opposed to individual tissues), these findings, combined with the understanding that the PA-spring was not correlated with lumped mechanical stiffness, provide support for the PA-spring test being primarily a measure of segmental mobility, rather than stiffness. This is in contrast to previous work that concluded that the PA-spring does not agree with segmental or total lumbar motion in the sagittal-plane and that, perhaps, the PA-spring grading is influenced by the clinician’s perception of joint stiffness.15 Together, these findings lead us to conclude that tissues other than the erector spinae muscle and supraspinous ligament are contributing to segmental mobility characteristics in the PA direction, and much remains to be learned about what specifically is being assessed during segmental mobility testing.

We expected the PA-spring and PIVM gradings to be associated with each other, and this hypothesis was supported. Therefore, clinical mobility testing of spinal segments may yield similar information, even when one is performed in a primarily extension direction (PA-spring)16 compared with a primarily flexion direction (PIVM). Therefore, although clinicians frequently use multiple approaches to assess gross and segmental mobility of the spine, these tests may not provide discretely different information for the clinician. If spinal segmental mobility assessment is the primary goal, it may not be necessary for clinicians to perform both tests to gain the necessary insight for diagnosis and plan of care.

Because clinicians may perform multiple segmental mobility assessments over the course of a single session,25,53,58 it was important to determine whether the process of assessing spinal mobility alters the mechanical stiffness of the spine. To address this question, we compared lumped mechanical stiffness before and after application of the clinical mobility assessments. We did not expect mechanical stiffness to change following the clinical assessment because the tests were applied as a single motion, rather than in multiple repetitions, as would be performed to mobilize the spine.71 This hypothesis was supported, and these results provide confidence to clinicians that they are not changing the lumped mechanical stiffness of the lumbar spine through segmental mobility assessment when it is performed with a limited number of tests (PA-spring and PIVM) and with limited test repetition (1–2 repetitive motions).

Based on previous work reporting sex differences in thoracolumbar fascial shear strain72 and stress-relaxation of the lumbar erector spinae,73 we expected males would have greater spinal stiffness than females. We found greater overall lumped mechanical stiffness of the lumbar spine in flexion for males when evaluated across all stiffness zones of the moment–angle curve, as well as greater erector spinae stiffness, which was consistent with previous findings.40 However, there were no sex differences in stiffness of the supraspinous ligament, nor in gross mobility assessed as standing AROM. Therefore, the greater stiffness observed in the males did not translate to limitations in overall ROM, gross mobility, in this sample. Because the supraspinous ligament would not be expected to have a significant contribution to passive stiffness until the end range of flexion motion, we suggest that the greater resting lumbar erector spinae stiffness observed in males may contribute to the greater lumped mechanical stiffness observed in the passive jig. This is done with the understanding that the jig was not completely frictionless and the males generally had greater mass than the females. Although sex differences in baseline mechanical stiffness have not been previously reported in studies using a similar lumped method, sex-specific responses to prolonged sitting or driving have been found, with males tending to show a stiffening response to exposure, whereas females were either unchanged or variable.30,31 When lumbar stiffness is measured using an indentation device in patients with LBP, males have been found to demonstrate greater joint stiffness at all lumbar levels.74 Pagé et al75 also found that females had less spine stiffness compared with males, using a slightly different indentation method, although the differences were only significant at L3 and L5. Given the significant sex-specific differences, as well as the growing evidence for sex-specific lumbar tissue characteristics in the literature, sex should be considered in the assessment and treatment of the low back. This is especially critical because manual therapy treatments have been shown to reduce muscle stiffness76; therefore, when tissue stiffness reduction is the therapeutic goal, differential tissues may be indicated for treatment according to the patient’s sex.

This study has some limitations. First, we selected a participant group that identified as being free from LBP for the past 3 months to ensure that the participants were not experiencing an acute episode of LBP. Although 3 months of persistent or recurring LBP has been used as inclusion criteria in studies examining LBP,3,41,77,78 at least 1 year pain free has been suggested as an appropriate cutoff to ensure no LBP pain-related changes in motor control.79 We do not believe that the 3-month cutoff used in the current study affects the conclusions made, given that no participants reported LBP during the testing procedures and the study did not directly investigate motor control. In addition, we were only able to monitor 1 lumbar erector muscle while the participants were in the passive jig, with the assumption that the trunk flexors were also passive.

As well, although mechanical stiffness and clinical mobility findings were not correlated, there might be some interplay between joint/tissue stiffness and joint mobility. A stiffer spine may be more likely to demonstrate reduced mobility, whereas a less stiff joint may demonstrate greater mobility. We were unable to demonstrate that relationship in the current study. The lack of correlation between clinical, mechanical, and tissue stiffness in this study speaks to the difficulty in manually assessing mechanical properties of the spine. Even though each clinical test is intended to evaluate a slightly different aspect of spine mechanics, both the PIVM and PA-spring tended to give the same results. The similarity in gradings seems reasonable, as it is understood that physiological limits of palpation likely limit clinicians’ ability to identify small differences in spine mobility.80

It is also important to note that flexion induced by the passive jig is trunk-on-pelvis motion, while PIVM induces a pelvis-on-trunk motion, and this could be a confounder when comparing the 2 approaches. The lack of correlation between mechanical stiffness and clinical mobility testing could be due to methodological differences described or could indicate that the methods assess distinctly different characteristics. We believe these findings provide insight into what information is being gathered from different testing approaches, as well as the language that is used to describe such findings.

We have demonstrated that, except for the association between the PA-spring and PIVM, there is little correlation between clinical, tissue, and lumped mechanical measures of spinal stiffness. This finding has important implications. The language used regarding mobility and stiffness is inconsistent among clinicians and between disciplines. It is often unclear, even within the clinical literature, whether it is indeed mobility or stiffness that is being considered. Hypomobility and stiffness are often used interchangeably, and the findings from this study suggest that these are not the same characteristic, although they likely are related. It is possible that clinical assessments using the conceptual framework of “stiffness” do not actually correspond to mechanical stiffness in the lumbar spine and it may be time to reevaluate the use of this terminology.

Another important finding in this study was that the males and females demonstrated different lumbar stiffness with the mechanical testing measures. This implies that consideration for the patient’s sex should be incorporated into the clinical decision-making process. The participants in this study were healthy and not experiencing any low back dysfunction or pain at the time of testing. Males may be expected to have naturally greater tissue stiffness than females in the lumbar spine, and the judgment of what is considered atypical may differ between males and females. This finding also has the potential to impact treatment, as there may be sex-based differences in which tissues are most appropriate to target for intervention.

Acknowledgments

Funding was provided by the National Sciences and Engineering Council of Canada (NSERC). L.M.T. was supported by an NSERC CGS and NSERC CGS-MSFSS award, J.M.B. was supported by an NSERC CGS, and J.P.C. is supported by a Canada Research Chair in Spine Biomechanics and Injury Prevention. The authors have no conflict of interest to disclose.

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If the inline PDF is not rendering correctly, you can download the PDF file here.

Tennant, Barrett, and Callaghan are with the Department of Kinesiology, University of Waterloo, Waterloo, ON, Canada. Nelson-Wong, Kuest, Lawrence, Levesque, Owens, Prisby, Spivey, Albin, and Jagger are with the School of Physical Therapy, Regis University, Denver, CO, USA. Wong is with the Department of Mechanical Engineering, Colorado School of Mines, Golden, CO, USA.

Callaghan (jack.callaghan@uwaterloo.ca) is corresponding author.
  • View in gallery

    —The experimental protocol outlining the order of lumbar AROM testing, EMG instrumentation, lumbar mechanical stiffness measurement (Jig), clinical testing (PA-spring and PIVM), and tissue stiffness testing of the supraspinous ligament and lumbar erector spinae muscle using myotonometry. Randomized steps are indicated with dashed arrows. AROM indicates active range of motion; EMG, electromyography; PA, posteroanterior; PIVM, passive intervertebral motion.

  • View in gallery

    —(A) The side-lying jig used to evaluate lumped mechanical stiffness of the lumbar spine. (B) A representative example of the moment-angle curve derived from the passive jig to evaluate lumped mechanical stiffness of the lumbar spine. Slope zones are labeled according to “low,” “transition,” and “high” stiffness zones. Slope breakpoint locations are indicated with an arrow.

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