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Analysis of compensatory mechanisms in the pelvis and lower extremities in patients with pelvic incidence and lumbar lordosis mismatch
Accepted Manuscript Title: Analysis of compensatory mechanisms in the pelvis and lower extremities in patients with pelvic incidence and lumbar lordosis mismatch Authors: Xiaofei Cheng, Kai Zhang, Xiaojiang Sun, Changqing Zhao, Hua Li, Jie Zhao PII: DOI: Reference:
S0966-6362(17)30174-1 http://dx.doi.org/doi:10.1016/j.gaitpost.2017.04.041 GAIPOS 5414
To appear in:
Gait & Posture
Received date: Revised date: Accepted date:
4-8-2016 7-4-2017 30-4-2017
Please cite this article as: Cheng Xiaofei, Zhang Kai, Sun Xiaojiang, Zhao Changqing, Li Hua, Zhao Jie.Analysis of compensatory mechanisms in the pelvis and lower extremities in patients with pelvic incidence and lumbar lordosis mismatch.Gait and Posture http://dx.doi.org/10.1016/j.gaitpost.2017.04.041 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Analysis of compensatory mechanisms in the pelvis and lower extremities in patients with pelvic incidence and lumbar lordosis mismatch
Xiaofei Cheng, MD,1 Kai Zhang, MD, 1 Xiaojiang Sun, MD, 1 Changqing Zhao, MD, 1
1
Hua Li, MD, 1 Jie Zhao, MD,1* Shanghai Key Laboratory of Orthopaedic Implants, Department of Orthopaedic
Surgery, Ninth People’s Hospital, Shanghai JiaoTong University School of Medicine, Shanghai, China
* Address correspondence and reprint requests to Jie Zhao, MD, Shanghai Key Laboratory of Orthopaedic Implants, Department of Orthopaedic Surgery, Ninth People’s Hospital, Shanghai JiaoTong University School of Medicine, 639 Zhizaoju Road, Shanghai, 200011 People’s Republic of China; Phone: 8621 2327 1699; Fax: 8621 6313 6856; E-mail: [email protected]
1
Highlights
Pelvic compensation can be divided into pelvic retroversion and pelvic retroposition.
As PI-LL mismatch progress, pelvic retroposition becomes more important.
Patients with lesser PI-LL mismatch rely more on hip extension to increase pelvic retroversion.
Patients with greater PI-LL mismatch tend to add extra femoral obliquity.
Abstract The objective was to analyze the compensatory effect of the pelvis and lower extremities on sagittal spinal malalignment in patients with pelvic incidence (PI) and lumbar lordosis (LL) mismatch. A series of parameters including PI, LL, PI-LL, thoracic kyphosis (TK), pelvic tilt (PT), sacral slope (SS), knee flexion angle (KFA), tibial obliquity angle (TOA), femoral obliquity angle (FOA), femur pelvis angle (FPA) and pelvic shift (PS) were measured. Patients with PI-LL mismatch were divided into pelvic retroversion group and pelvic retroposition group based on their PT and PS, and then the parameters were compared within the two groups and with the control group. All variables were significantly different when comparing the pelvic retroversion and retroposition group with the control group except for PI, FOA and PS in the pelvic retroversion group. The pelvic retroposition group had significantly greater value of PI-LL, PI, PT, KFA, FOA and PS and contribution ratio of FOA and PS, and smaller value of LL, TK and FPA and contribution ratio of PT, TOA and FPA compared with the pelvic retroversion group. Patients 2
with lesser PI-LL mismatch rely more on hip extension to increase pelvic retroversion while those with greater PI-LL mismatch tend to add extra femoral obliquity. When compensating for larger PI-LL mismatch, the importance of hip extension is decreased and the effect of the knee and ankle joint becomes more important by providing greater femoral incline and relatively lesser ankle dorsiflexion respectively.
Key words: sagittal spinal malalignment; spinopelvic mismatch; compensatory mechanism; pelvic retroversion; pelvic retroposition; lower extremity
Introduction Lumbar degenerative changes with age could lead to a loss of lumbar lordosis (LL) and consequent sagittal spinal malalignment. Restoration of normative LL is a common method to re-establish sagittal alignment. However, an attempt to establish a definite normal value for LL is hard because LL is highly variable between individual [1, 2]. Pelvic incidence (PI) is an anatomical constant for each individual and its amount has demonstrated a good correlation with LL. Therefore, PI and LL mismatch (PI-LL) was introduced to evaluate the loss of LL and guide the correction of LL [3, 4].
Patients with sagittal spinal malalignment will adopt some compensatory postural changes starting in the flexible parts of the spine and moving distally to the pelvis and lower extremities, such as thoracic hyperextension and pelvic retroversion, to place the center of gravity above the feet, 3
maintain the trunk as upright as possible and keep a horizontal gaze [5, 6]. The compensatory mechanisms allow limiting the consequence of sagittal spinal malalignment, for which sagittal imbalance will be diminished by these mechanisms. Thus, they must be considered to detect potential spinal imbalance hidden by the compensation when assessing global sagittal balance [7]. A number of patients with PI-LL mismatch need correction surgery and several methods have been designed to preoperatively estimate the amount of correction needed. An underestimation of the compensatory mechanisms may predispose to postoperative undercorrection and residual sagittal malalignment due to the spontaneous correction of the compensatory changes after surgery [3, 8, 9]. Therefore, a comprehensive and detailed understanding and an adequate evaluation of overall compensatory mechanisms are necessary for preventing underestimation of the severity of sagittal malalignment and decreasing the risk for the insufficient correction.
Besides well-reported pelvic retroversion, several authors have proposed that pelvis translation is another compensatory mechanism in the pelvis area as important as pelvic retroversion [10, 11]. Moreover, the influence of the lower extremities on global sagittal alignment has been increasingly underlined and knee flexion has been reported to participate in compensation for sagittal spinal malalignment [11-15]. However, to our knowledge, no study has investigated the compensatory changes in the hip, knee and ankle joint by regarding them as parts of the whole lower extremities. The relationship between the positional status of these joints and compensatory pelvic retroversion and translation is still unclear. The objective of this study was thus to analyze the compensatory effect of the pelvis and lower extremities on sagittal spinal imbalance and to investigate the correlation between the pelvic compensation and the hip, knee and ankle joint in 4
patients with PI-LL mismatch.
Methods Study participants This study included 134 adult patients with lumbar degenerative disease whose standing lateral radiograph of the spine, pelvis and lower extremities was available. We excluded patients with lumbar spondylolisthesis, spinal tumor, infection or trauma, knee flexion contracture (extension < 0°), hip flexion contracture (extension < 10°), or leg length discrepancy (>1cm). Institutional review board approval for this study and informed consent of all patients were obtained. Demographic parameters (age, gender and body mass index) were collected. Radiographic measurements All radiographs were obtained under the identical conditions. Patients were instructed to assume a comfortable standing posture. The following parameters were measured using software tools built into a picture archiving and communication system: thoracic kyphosis (TK: the angle between the upper endplate of T5 and the lower endplate of T12), LL (the angle between the upper endplate of L1 and the upper endplate of S1), PI (the angle between the perpendicular of the sacral plate and the line joining the middle of the sacral plate and the midpoint of both hip axes), pelvic tilt (PT: the angle between the vertical line and the line joining the middle of the sacral plate and the hip axis), sacral slope (SS: the angle between the sacral plate and the horizontal line), knee flexion angle (KFA: the angle between the axis of the femur and tibia), tibial obliquity angle (TOA: the angle between the tibial axis and the vertical line), femoral obliquity angle (FOA: the angle between the femoral axis and the vertical line), femur pelvis angle (FPA: the angle between the 5
femoral axis and the line joining the middle of the sacral plate and the hip axis) and pelvic shift (PS: the offset between the anterior cortex of the distal tibia and the middle of the sacral plate. According to the definitions, there are two formulas for a given subject: KFA=FOA+TOA and PT = FOA+FPA (Figure 1). Based on the values of PI-LL, patients were preliminarily divided into PI-LL match (control) group (PI-LL≤0°) and PI-LL mismatch group (PI-LL>0°). Statistical Analysis All parameters were measured twice by the same observer on two separate occasions and once by another observer to determine the intra- and inter-observer reliability, respectively. Intraclass correlation coefficients (ICCs) were used to statistically evaluate the reliability. The intra- and inter-observer reliability of these measurements had excellent agreement (ICCs between 0.81 and 0.99). Therefore, measurements taken by one observer were used in the further analyses. For subjects in the PI-LL mismatch group, a statistical software package (SPSS version 13.0, SPSS Inc., Chicago, IL) was used to produce two clusters based on their PT and PS. The K-means analysis used multiple iterations to assign these subjects to two distinct groups: pelvic retroversion group and pelvic retroposition group. All parameters were analyzed using chi-square test with Bonferroni correction, one-way ANOVA test followed by post hoc LSD test or Kruskal-Wallis H test followed by post hoc Nemenyi test. The differences between individual value of seven parameters (TK, PT, KFA, TOA, FOA, FPA and PS) in the PI-LL mismatch group and the mean of these parameters in the control group were calculated and then normalized to the value of PI-LL related to each subject as contribution ratios for these parameters. The contribution ratio was compared between the two PI-LL mismatch groups using Mann-Whitney U test. The correlation between the variables was examined using the Pearson correlation coefficient. Statistical 6
significance was defined as P value < 0.05. Statistically significant correlation coefficients were considered clinically significant only if ≥ 0.3.
Results There were 36 males and 98 females (mean age, 58.6 years; range, 40–80 years). No significant difference was noted in age, gender or body mass index among the three groups. All radiographic variables were significantly different when comparing the pelvic retroversion and retroposition group with the control group except for PI, FOA and PS in the pelvic retroversion group. The pelvic retroposition group exhibited significantly greater PI-LL, PI, PT, KFA, FOA and PS, and smaller LL, TK and FPA compared with the pelvic retroversion group. There was no significant difference in SS and TOA between the two groups (Table 1). The pelvic retroposition group had significantly greater contribution ratio of FOA and PS, and smaller contribution ratio of PT, TOA and FPA than the pelvic retroversion group. There was no significant difference in contribution ratio of TK and KFA between the two groups (Table 2). Results from the correlation analysis between the various compensatory mechanisms and PI-LL mismatch revealed that ΔTK, ΔPT, ΔKFA, ΔFOA, ΔFPA and ΔPS were significantly correlated with PI-LL in the PI-LL mismatch group (Table 3).
Discussion It is of great importance to identify and quantify the use of compensatory mechanisms when analyzing spinopelvic mismatch. Theoretically, all movable joints in the spine, pelvis and lower extremity area can participate in the compensation to some degree. The pelvis is considered to be 7
the pedestal of the spine and trunk, and plays a fundamental role as the axis of a chain consisting of the spine and lower extremities [16]. The anteroposterior tilt and displacement of the pelvis are entirely generated by the sagittal movement of the hip, knee and ankle joint, and will affect the orientation of the spine and the location of the center of gravity in the sagittal plane.
The compensatory mechanisms can be quantified by certain parameters, such as PT quantifying pelvic retroversion and PS quantifying pelvic retroposition. In the lower extremity area, FPA, KFA, FOA and TOA can quantify the amount of hip extension, knee flexion, femoral tilt and ankle dorsiflexion respectively. According to the definition, the direction of PT and PS is in accordance with FPA, KFA and FOA and opposite to TOA. We further estimated the average magnitudes of the compensatory changes by assuming the measured mean value in the control group as the ideal value, and then calculating the differences between the ideal values and the measured values of the parameters involved in compensation in the two PI-LL mismatch groups. The quotients of the differences and the value of PI-LL for each subject were regarded as contribution ratios for the compensatory mechanisms.
In the present study, patients with PI-LL mismatch were subdivided into two groups based on the value of PT and PS using cluster analysis. The first group had a lower value but a higher contribution ratio of PT than the second group and thus was defined as “pelvic retroversion” group. The second group had both higher value and contribution ratio of PS than the first group and was defined as “pelvic retroposition” group. Both groups showed greater PT and the pelvic retroposition group exhibited greater PS than the control group; however, PS was not significantly 8
different between the pelvic retroversion group and the control group. The severity of PI-LL mismatch in the pelvic retroposition group was greater than that in the pelvic retroversion group. In addition, the correlation analysis demonstrated that ΔPT and ΔPS both associated with PI-LL. Together these results suggested that pelvic retroversion compensated for sagittal spinal malalignment regardless of the severity of PI-LL mismatch but its contribution to larger PI-LL mismatch was reduced in spite of having greater value of PT. In contrast, pelvic retroposition was recruited only for greater PI-LL mismatch. In a word, as PI-LL mismatch progress, the availability of pelvic retroposition as a compensatory mechanism begins to appear, whereas the contribution of pelvic retroversion is generally decreased.
For patients with sagittal spinal malalignment, pelvic retroversion allow backward rotation of the spine and head to maintain an erect position and a horizontal gaze, and backward translation of the trunk to bring the center of gravity back over the feet. Pelvic retroversion can be viewed as a combination of hip extension and femoral tilt [13]. Considering that there is a formula: PT=FOA+FPA, FPA, reflecting a mutual angular relationship between the femur and pelvis, can be used to measure hip extension [17]. In addition, the extent of femoral tilt depends on the difference between the degree of knee flexion and ankle dorsiflexion. Therefore, the hip, knee and ankle joint are all involved in pelvic retroversion. Although patients in the pelvic retroversion and retroposition group both dorsiflexed the ankles, flexed the knees and extended the hips to increase PT, the ranges of joint motion were not totally identical. Since the mean value of FOA approximated the ideal value (1.9° vs 1.5°), additional femoral tilt in the pelvic retroversion group was slight (average 0.4°). Meanwhile, the difference between the mean value of FPA and the ideal 9
value was 11.2°, suggesting that patients had almost completely extended the hips (hip extension reserve usually equals 10°) [18]. On the contrary, the mean excess of FOA was higher than that of FPA (8.2° vs 6.0°) in the pelvic retroposition group. The current results implied that, to retrovert the pelvis, patients with lesser PI-LL mismatch (the pelvic retroversion group) relied more on hip extension while those with greater PI-LL mismatch (the pelvic retroposition group) tended to add extra femoral obliquity by further knee flexion. Typical patients in the pelvic retroversion and retroposition group exhibited two different postures during standing observed from the lateral view. The former had an erect trunk, hyperextended hips and nearly vertical femurs formed by mild knee flexion and ankle dorsiflexion. By contrast, although the latter also extended the hip joint itself, they seemed to be in a crouch posture owing to a forward inclination of the trunk and obvious femoral tilt (Figure 2).
Unlike pelvic retroversion allowing simultaneous backward rotation and translation of the spine, pelvic retroposition only lead to a backward displacement of the axis of gravity. In this way, the trunk still leans forward and the patients cannot restore an erect position and horizontal gaze, which are important for daily functions and social activities. This limitation reduces the efficacy of pelvic retroposition and makes the patients with minor PI-LL mismatch give priority to pelvic retroversion. PS account for the offset of the pelvis related to the feet and is simultaneously modulated by the hip, knee and ankle joint as well as PT. The pelvic offset depends not only on the magnitude of joint motion, but also on the length of the lever arm. Under the condition of equal range of joint motion, the more distal the joint is, the larger offset it produces. Since the two PI-LL mismatch groups did not differ significantly in TOA, the difference in PS between the two 10
groups should be attributed to the different posture of the knee and hip joint. Knee flexion has a greater impact on PS than hip extension because its range of motion is larger than that of hip extension and, more importantly, the knees are more distal than the hips. Therefore, the pelvic retroposition group with greater KFA had larger PS than the pelvic retroversion group.
When humans with normal sagittal alignment keep a standing position, the hip joint is placed in a neutral position with FPA approximately equal to PT as the femurs are almost vertical. The value of FPA in the two PI-LL mismatch groups was both significantly greater than that in the control group, implying the recruitment of hip extension as a compensatory mechanism. The larger value and contribution ratio of FPA in the pelvic retroversion group compared to those in the pelvic retroposition group showed that, with the progression of PI-LL mismatch, the amount of hip extension would decrease and the contribution of the hip joint to compensation would decline accordingly. Knee flexion has been proven to associate with PI-LL mismatch and effectively decrease sagittal spinal imbalance [11-15]. The value of KFA was significantly greater in the pelvic retroposition group than in the pelvic retroversion group. Nevertheless, there was no significant difference in the contribution ratio of KFA between the two groups, indicating that knee flexion provided a relatively constant compensation for sagittal imbalance regardless of its amount. However, the pelvic retroposition group had significantly greater value and contribution ratio of FOA than the pelvic retroversion group, which might suggest that knee flexion became more efficient when compensating for larger PI-LL mismatch by providing greater proportional femoral incline. Larger knee flexion needs more muscle strength and energy consumption. Moreover, it will lead to longer duration of the knee pain, a decrease in walking velocity and 11
stride length, and rapid muscle fatigue, and thus reduce the overall knee function and the ability to stand and walk [15]. It could also explain why the patients with minor PI-LL mismatch did not adopt pelvic retroposition to compensate.
Our data revealed that the value of TOA was not significantly different between the two PI-LL mismatch groups and had no significant correlation with the value of PI-LL, indicating that the degree of ankle dorsiflexion would not change with the aggravation of PI-LL mismatch. However, considering the opposite direction of motion between ankle dorsiflexion and pelvic retroversion and retroposition, the lower contribution ratio of TOA in the pelvic retroposition group could be favorable for the pelvic compensation to counter greater PI-LL mismatch. A previous study has proved that the gravity line is relatively fixed referring to the position of the feet wherever the pelvis is [10]. So pelvic retroposition would keep the pelvis away from the gravity line. The present results showed that the displacement of the pelvis was generated by the cooperation of knee flexion and ankle dorsiflexion.
The main limitation of this study is a relatively small sample size of patients with PI-LL mismatch. Although these cases have provided enough evidence to support the conclusions, a larger sample size is likely to reveal more information about the compensatory mechanisms in the pelvis and lower extremities. Additionally, this study only analyzed static posture of patients with sagittal spinal malalignment. The importance of dynamic aspects in spinal misalignment and/or spinopelvic mismatch has been reviewed recently [19]. The dynamic analysis may provide more 12
valuable results for these patients and would be performed in further studies.
Conclusions The pelvic compensation for PI-LL mismatch can be divided into pelvic retroversion and pelvic retroposition, which are measured by PT and PS respectively. Patients with lesser PI-LL mismatch rely more on hip extension to increase pelvic retroversion while those with greater PI-LL mismatch tend to add extra femoral obliquity. When compensating for larger PI-LL mismatch, the importance of hip extension is decreased and the effect of the knee and ankle joint becomes more important by providing greater femoral incline and relatively lesser ankle dorsiflexion respectively.
Conflict of interest statement All authors: none.
Acknowledgements This study was supported by the grant of The National Natural Science Foundation of China (81572168), Fund for Key Disciplines of Shanghai Municipal Education Commission (J50206) and The Important Disease Joint Research Project of Shanghai Health System (2013ZYJB0502).
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Figure Legends Figure 1 Illustration of radiographic measurements. (FOA, femoral obliquity angle; FPA, femur pelvis angle; KFA, knee flexion angle; LL, lumbar lordosis; PI, pelvic incidence; PS, pelvic shift; PT, pelvic tilt; SS, sacral slope; TK, thoracic kyphosis; TOA, tibial obliquity angle )
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Figure 2 Lateral radiographs depicting two different standing postures. A: patients in the pelvic retroversion group have an erect trunk, hyperextended hips and nearly vertical femurs formed by mild knee flexion and ankle dorsiflexion; B: patients in the pelvic retroposition group seem to be in a crouch posture owing to a forward inclination of the trunk and obvious femoral tilt in spite of extension of the hip joint itself.
17
Table 1 Demographic and radiographic parameters for patients with lumbar degenerative diseases PI-LL
PI-LL mismatch group
match group Pelvic
P
Pelvic
P
P
retroversion
value1
retroposition
value1
value2
group
group 39
n
40
55
Gender (male/female)
11/29
15/40
0.580
10/29
0.527
0.527
Age (yrs)
56.1±7.7
59.7±7.9
0.052
59.7±11.0
0.078
0.974
Body mass index
22.4±3.7
0.780
0.548
0.365 21.6±4.1
22.1±4.2
2
(kg/m ) LL (°)
53.1±9.1
33.8±10.8 *
<0.001
27.8±15.3 *#
<0.001
0.017
Thoracic kyphosis (°)
42.6±6.7
34.6±11.7 *
0.001
29.1±14.1 *#
<0.001
0.022
PI (°)
47.4±8.8
47.6±10.2
0.900
55.1±11.0 *#
0.001
0.001
Sacral slope (°)
35.0±6.5
24.6±8.4 *
<0.001
28.0±10.2 *
<0.001
0.055
Pelvic tilt (°)
12.3±5.9
23.1±5.7 *
<0.001
26.9±5.5 *#
<0.001
0.002
PI-LL (°)
-5.8±2.5
13.0±7.5 *
<0.001
28.6±11.1 *#
<0.001
<0.001
Knee flexion angle (°)
3.4±2.3
7.5±3.4 *
<0.001
14.4±5.9 *#
<0.001
<0.001
Tibial obliquity angle
1.9±2.2
<0.001
0.080
<0.001 5.7±2.8
*
(°) 18
4.7±2.6
*
Femoral obliquity
1.5±2.8
0.693 1.9±3.4
9.7±6.1
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
*#
angle (°) Femur pelvis angle
10.8±6.9
<0.001 22.0±6.2
*
16.8±6.7
*#
(°) Pelvic shift (mm)
23.8±34.6
35.0±32.4
0.131
134.8±40.3 *#
Patients with PI-LL mismatch were subdivided into pelvic retroversion and retroposition group based on the value of pelvic tilt and pelvic shift using cluster analysis. Data were expressed as mean ± standard deviation; PI, pelvic incidence; LL, lumbar lordosis. 1
Compared with the PI-LL match group.
2
Compared with the pelvic retroversion group.
*
P<0.05 Compared with the PI-LL match group
#
P<0.05 Compared with the pelvic retroversion group
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Table 2 Comparison of contribution ratio of compensatory mechanisms between the pelvic retroversion and retroposition group Pelvic Pelvic retroversion group
retroposition
P value
group ΔThoracic kyphosis/PI-LL
0.78(0.93)
0.59(0.72)
0.070
ΔPelvic tilt/PI-LL
0.86(0.70)
0.63(0.59)
<0.001
ΔKnee flexion angle/PI-LL
0.29(0.37)
0.33(0.30)
0.064
ΔTibial obliquity angle/PI-LL
0.26(0.37)
0.18(0.28)
<0.001
ΔFemoral obliquity angle/PI-LL
0.03(0.34)
0.14(0.37)
<0.001
ΔFemur pelvis angle/PI-LL
0.83(1.12)
0.49(0.76)
<0.001
ΔPelvic shift/PI-LL
1.08(2.60)
2.59(3.24)
<0.001
We assumed the measured mean value in the control group as the ideal value and then calculated the differences between the ideal values and the measured values of the parameters involved in compensation in the two PI-LL mismatch groups. The quotients of the differences and the value of PI-LL for each subject were regarded as contribution ratios for the compensatory mechanisms. Data were expressed as median (interquartile range); PI, pelvic incidence; LL, lumbar lordosis.
20
Table 3 Correlations between compensatory mechanisms and PI-LL mismatch for patients with PI-LL mismatch PI-LL r
P value
ΔThoracic kyphosis
0.353
<0.001
ΔPelvic tilt
0.517
<0.001
ΔKnee flexion angle
0.713
<0.001
ΔTibial obliquity angle
-0.113
0.272
ΔFemoral obliquity angle
0.719
<0.001
ΔFemur pelvis angle
-0.255
0.013
ΔPelvic shift
0.728
<0.001
Results indicated that the compensatory mechanisms in the pelvis and lower extremities, except for ankle rotation, were significantly correlated with PI-LL mismatch in the PI-LL mismatch group. PI, pelvic incidence; LL, lumbar lordosis.
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S0966-6362(17)30174-1 http://dx.doi.org/doi:10.1016/j.gaitpost.2017.04.041 GAIPOS 5414
To appear in:
Gait & Posture
Received date: Revised date: Accepted date:
4-8-2016 7-4-2017 30-4-2017
Please cite this article as: Cheng Xiaofei, Zhang Kai, Sun Xiaojiang, Zhao Changqing, Li Hua, Zhao Jie.Analysis of compensatory mechanisms in the pelvis and lower extremities in patients with pelvic incidence and lumbar lordosis mismatch.Gait and Posture http://dx.doi.org/10.1016/j.gaitpost.2017.04.041 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Analysis of compensatory mechanisms in the pelvis and lower extremities in patients with pelvic incidence and lumbar lordosis mismatch
Xiaofei Cheng, MD,1 Kai Zhang, MD, 1 Xiaojiang Sun, MD, 1 Changqing Zhao, MD, 1
1
Hua Li, MD, 1 Jie Zhao, MD,1* Shanghai Key Laboratory of Orthopaedic Implants, Department of Orthopaedic
Surgery, Ninth People’s Hospital, Shanghai JiaoTong University School of Medicine, Shanghai, China
* Address correspondence and reprint requests to Jie Zhao, MD, Shanghai Key Laboratory of Orthopaedic Implants, Department of Orthopaedic Surgery, Ninth People’s Hospital, Shanghai JiaoTong University School of Medicine, 639 Zhizaoju Road, Shanghai, 200011 People’s Republic of China; Phone: 8621 2327 1699; Fax: 8621 6313 6856; E-mail: [email protected]
1
Highlights
Pelvic compensation can be divided into pelvic retroversion and pelvic retroposition.
As PI-LL mismatch progress, pelvic retroposition becomes more important.
Patients with lesser PI-LL mismatch rely more on hip extension to increase pelvic retroversion.
Patients with greater PI-LL mismatch tend to add extra femoral obliquity.
Abstract The objective was to analyze the compensatory effect of the pelvis and lower extremities on sagittal spinal malalignment in patients with pelvic incidence (PI) and lumbar lordosis (LL) mismatch. A series of parameters including PI, LL, PI-LL, thoracic kyphosis (TK), pelvic tilt (PT), sacral slope (SS), knee flexion angle (KFA), tibial obliquity angle (TOA), femoral obliquity angle (FOA), femur pelvis angle (FPA) and pelvic shift (PS) were measured. Patients with PI-LL mismatch were divided into pelvic retroversion group and pelvic retroposition group based on their PT and PS, and then the parameters were compared within the two groups and with the control group. All variables were significantly different when comparing the pelvic retroversion and retroposition group with the control group except for PI, FOA and PS in the pelvic retroversion group. The pelvic retroposition group had significantly greater value of PI-LL, PI, PT, KFA, FOA and PS and contribution ratio of FOA and PS, and smaller value of LL, TK and FPA and contribution ratio of PT, TOA and FPA compared with the pelvic retroversion group. Patients 2
with lesser PI-LL mismatch rely more on hip extension to increase pelvic retroversion while those with greater PI-LL mismatch tend to add extra femoral obliquity. When compensating for larger PI-LL mismatch, the importance of hip extension is decreased and the effect of the knee and ankle joint becomes more important by providing greater femoral incline and relatively lesser ankle dorsiflexion respectively.
Key words: sagittal spinal malalignment; spinopelvic mismatch; compensatory mechanism; pelvic retroversion; pelvic retroposition; lower extremity
Introduction Lumbar degenerative changes with age could lead to a loss of lumbar lordosis (LL) and consequent sagittal spinal malalignment. Restoration of normative LL is a common method to re-establish sagittal alignment. However, an attempt to establish a definite normal value for LL is hard because LL is highly variable between individual [1, 2]. Pelvic incidence (PI) is an anatomical constant for each individual and its amount has demonstrated a good correlation with LL. Therefore, PI and LL mismatch (PI-LL) was introduced to evaluate the loss of LL and guide the correction of LL [3, 4].
Patients with sagittal spinal malalignment will adopt some compensatory postural changes starting in the flexible parts of the spine and moving distally to the pelvis and lower extremities, such as thoracic hyperextension and pelvic retroversion, to place the center of gravity above the feet, 3
maintain the trunk as upright as possible and keep a horizontal gaze [5, 6]. The compensatory mechanisms allow limiting the consequence of sagittal spinal malalignment, for which sagittal imbalance will be diminished by these mechanisms. Thus, they must be considered to detect potential spinal imbalance hidden by the compensation when assessing global sagittal balance [7]. A number of patients with PI-LL mismatch need correction surgery and several methods have been designed to preoperatively estimate the amount of correction needed. An underestimation of the compensatory mechanisms may predispose to postoperative undercorrection and residual sagittal malalignment due to the spontaneous correction of the compensatory changes after surgery [3, 8, 9]. Therefore, a comprehensive and detailed understanding and an adequate evaluation of overall compensatory mechanisms are necessary for preventing underestimation of the severity of sagittal malalignment and decreasing the risk for the insufficient correction.
Besides well-reported pelvic retroversion, several authors have proposed that pelvis translation is another compensatory mechanism in the pelvis area as important as pelvic retroversion [10, 11]. Moreover, the influence of the lower extremities on global sagittal alignment has been increasingly underlined and knee flexion has been reported to participate in compensation for sagittal spinal malalignment [11-15]. However, to our knowledge, no study has investigated the compensatory changes in the hip, knee and ankle joint by regarding them as parts of the whole lower extremities. The relationship between the positional status of these joints and compensatory pelvic retroversion and translation is still unclear. The objective of this study was thus to analyze the compensatory effect of the pelvis and lower extremities on sagittal spinal imbalance and to investigate the correlation between the pelvic compensation and the hip, knee and ankle joint in 4
patients with PI-LL mismatch.
Methods Study participants This study included 134 adult patients with lumbar degenerative disease whose standing lateral radiograph of the spine, pelvis and lower extremities was available. We excluded patients with lumbar spondylolisthesis, spinal tumor, infection or trauma, knee flexion contracture (extension < 0°), hip flexion contracture (extension < 10°), or leg length discrepancy (>1cm). Institutional review board approval for this study and informed consent of all patients were obtained. Demographic parameters (age, gender and body mass index) were collected. Radiographic measurements All radiographs were obtained under the identical conditions. Patients were instructed to assume a comfortable standing posture. The following parameters were measured using software tools built into a picture archiving and communication system: thoracic kyphosis (TK: the angle between the upper endplate of T5 and the lower endplate of T12), LL (the angle between the upper endplate of L1 and the upper endplate of S1), PI (the angle between the perpendicular of the sacral plate and the line joining the middle of the sacral plate and the midpoint of both hip axes), pelvic tilt (PT: the angle between the vertical line and the line joining the middle of the sacral plate and the hip axis), sacral slope (SS: the angle between the sacral plate and the horizontal line), knee flexion angle (KFA: the angle between the axis of the femur and tibia), tibial obliquity angle (TOA: the angle between the tibial axis and the vertical line), femoral obliquity angle (FOA: the angle between the femoral axis and the vertical line), femur pelvis angle (FPA: the angle between the 5
femoral axis and the line joining the middle of the sacral plate and the hip axis) and pelvic shift (PS: the offset between the anterior cortex of the distal tibia and the middle of the sacral plate. According to the definitions, there are two formulas for a given subject: KFA=FOA+TOA and PT = FOA+FPA (Figure 1). Based on the values of PI-LL, patients were preliminarily divided into PI-LL match (control) group (PI-LL≤0°) and PI-LL mismatch group (PI-LL>0°). Statistical Analysis All parameters were measured twice by the same observer on two separate occasions and once by another observer to determine the intra- and inter-observer reliability, respectively. Intraclass correlation coefficients (ICCs) were used to statistically evaluate the reliability. The intra- and inter-observer reliability of these measurements had excellent agreement (ICCs between 0.81 and 0.99). Therefore, measurements taken by one observer were used in the further analyses. For subjects in the PI-LL mismatch group, a statistical software package (SPSS version 13.0, SPSS Inc., Chicago, IL) was used to produce two clusters based on their PT and PS. The K-means analysis used multiple iterations to assign these subjects to two distinct groups: pelvic retroversion group and pelvic retroposition group. All parameters were analyzed using chi-square test with Bonferroni correction, one-way ANOVA test followed by post hoc LSD test or Kruskal-Wallis H test followed by post hoc Nemenyi test. The differences between individual value of seven parameters (TK, PT, KFA, TOA, FOA, FPA and PS) in the PI-LL mismatch group and the mean of these parameters in the control group were calculated and then normalized to the value of PI-LL related to each subject as contribution ratios for these parameters. The contribution ratio was compared between the two PI-LL mismatch groups using Mann-Whitney U test. The correlation between the variables was examined using the Pearson correlation coefficient. Statistical 6
significance was defined as P value < 0.05. Statistically significant correlation coefficients were considered clinically significant only if ≥ 0.3.
Results There were 36 males and 98 females (mean age, 58.6 years; range, 40–80 years). No significant difference was noted in age, gender or body mass index among the three groups. All radiographic variables were significantly different when comparing the pelvic retroversion and retroposition group with the control group except for PI, FOA and PS in the pelvic retroversion group. The pelvic retroposition group exhibited significantly greater PI-LL, PI, PT, KFA, FOA and PS, and smaller LL, TK and FPA compared with the pelvic retroversion group. There was no significant difference in SS and TOA between the two groups (Table 1). The pelvic retroposition group had significantly greater contribution ratio of FOA and PS, and smaller contribution ratio of PT, TOA and FPA than the pelvic retroversion group. There was no significant difference in contribution ratio of TK and KFA between the two groups (Table 2). Results from the correlation analysis between the various compensatory mechanisms and PI-LL mismatch revealed that ΔTK, ΔPT, ΔKFA, ΔFOA, ΔFPA and ΔPS were significantly correlated with PI-LL in the PI-LL mismatch group (Table 3).
Discussion It is of great importance to identify and quantify the use of compensatory mechanisms when analyzing spinopelvic mismatch. Theoretically, all movable joints in the spine, pelvis and lower extremity area can participate in the compensation to some degree. The pelvis is considered to be 7
the pedestal of the spine and trunk, and plays a fundamental role as the axis of a chain consisting of the spine and lower extremities [16]. The anteroposterior tilt and displacement of the pelvis are entirely generated by the sagittal movement of the hip, knee and ankle joint, and will affect the orientation of the spine and the location of the center of gravity in the sagittal plane.
The compensatory mechanisms can be quantified by certain parameters, such as PT quantifying pelvic retroversion and PS quantifying pelvic retroposition. In the lower extremity area, FPA, KFA, FOA and TOA can quantify the amount of hip extension, knee flexion, femoral tilt and ankle dorsiflexion respectively. According to the definition, the direction of PT and PS is in accordance with FPA, KFA and FOA and opposite to TOA. We further estimated the average magnitudes of the compensatory changes by assuming the measured mean value in the control group as the ideal value, and then calculating the differences between the ideal values and the measured values of the parameters involved in compensation in the two PI-LL mismatch groups. The quotients of the differences and the value of PI-LL for each subject were regarded as contribution ratios for the compensatory mechanisms.
In the present study, patients with PI-LL mismatch were subdivided into two groups based on the value of PT and PS using cluster analysis. The first group had a lower value but a higher contribution ratio of PT than the second group and thus was defined as “pelvic retroversion” group. The second group had both higher value and contribution ratio of PS than the first group and was defined as “pelvic retroposition” group. Both groups showed greater PT and the pelvic retroposition group exhibited greater PS than the control group; however, PS was not significantly 8
different between the pelvic retroversion group and the control group. The severity of PI-LL mismatch in the pelvic retroposition group was greater than that in the pelvic retroversion group. In addition, the correlation analysis demonstrated that ΔPT and ΔPS both associated with PI-LL. Together these results suggested that pelvic retroversion compensated for sagittal spinal malalignment regardless of the severity of PI-LL mismatch but its contribution to larger PI-LL mismatch was reduced in spite of having greater value of PT. In contrast, pelvic retroposition was recruited only for greater PI-LL mismatch. In a word, as PI-LL mismatch progress, the availability of pelvic retroposition as a compensatory mechanism begins to appear, whereas the contribution of pelvic retroversion is generally decreased.
For patients with sagittal spinal malalignment, pelvic retroversion allow backward rotation of the spine and head to maintain an erect position and a horizontal gaze, and backward translation of the trunk to bring the center of gravity back over the feet. Pelvic retroversion can be viewed as a combination of hip extension and femoral tilt [13]. Considering that there is a formula: PT=FOA+FPA, FPA, reflecting a mutual angular relationship between the femur and pelvis, can be used to measure hip extension [17]. In addition, the extent of femoral tilt depends on the difference between the degree of knee flexion and ankle dorsiflexion. Therefore, the hip, knee and ankle joint are all involved in pelvic retroversion. Although patients in the pelvic retroversion and retroposition group both dorsiflexed the ankles, flexed the knees and extended the hips to increase PT, the ranges of joint motion were not totally identical. Since the mean value of FOA approximated the ideal value (1.9° vs 1.5°), additional femoral tilt in the pelvic retroversion group was slight (average 0.4°). Meanwhile, the difference between the mean value of FPA and the ideal 9
value was 11.2°, suggesting that patients had almost completely extended the hips (hip extension reserve usually equals 10°) [18]. On the contrary, the mean excess of FOA was higher than that of FPA (8.2° vs 6.0°) in the pelvic retroposition group. The current results implied that, to retrovert the pelvis, patients with lesser PI-LL mismatch (the pelvic retroversion group) relied more on hip extension while those with greater PI-LL mismatch (the pelvic retroposition group) tended to add extra femoral obliquity by further knee flexion. Typical patients in the pelvic retroversion and retroposition group exhibited two different postures during standing observed from the lateral view. The former had an erect trunk, hyperextended hips and nearly vertical femurs formed by mild knee flexion and ankle dorsiflexion. By contrast, although the latter also extended the hip joint itself, they seemed to be in a crouch posture owing to a forward inclination of the trunk and obvious femoral tilt (Figure 2).
Unlike pelvic retroversion allowing simultaneous backward rotation and translation of the spine, pelvic retroposition only lead to a backward displacement of the axis of gravity. In this way, the trunk still leans forward and the patients cannot restore an erect position and horizontal gaze, which are important for daily functions and social activities. This limitation reduces the efficacy of pelvic retroposition and makes the patients with minor PI-LL mismatch give priority to pelvic retroversion. PS account for the offset of the pelvis related to the feet and is simultaneously modulated by the hip, knee and ankle joint as well as PT. The pelvic offset depends not only on the magnitude of joint motion, but also on the length of the lever arm. Under the condition of equal range of joint motion, the more distal the joint is, the larger offset it produces. Since the two PI-LL mismatch groups did not differ significantly in TOA, the difference in PS between the two 10
groups should be attributed to the different posture of the knee and hip joint. Knee flexion has a greater impact on PS than hip extension because its range of motion is larger than that of hip extension and, more importantly, the knees are more distal than the hips. Therefore, the pelvic retroposition group with greater KFA had larger PS than the pelvic retroversion group.
When humans with normal sagittal alignment keep a standing position, the hip joint is placed in a neutral position with FPA approximately equal to PT as the femurs are almost vertical. The value of FPA in the two PI-LL mismatch groups was both significantly greater than that in the control group, implying the recruitment of hip extension as a compensatory mechanism. The larger value and contribution ratio of FPA in the pelvic retroversion group compared to those in the pelvic retroposition group showed that, with the progression of PI-LL mismatch, the amount of hip extension would decrease and the contribution of the hip joint to compensation would decline accordingly. Knee flexion has been proven to associate with PI-LL mismatch and effectively decrease sagittal spinal imbalance [11-15]. The value of KFA was significantly greater in the pelvic retroposition group than in the pelvic retroversion group. Nevertheless, there was no significant difference in the contribution ratio of KFA between the two groups, indicating that knee flexion provided a relatively constant compensation for sagittal imbalance regardless of its amount. However, the pelvic retroposition group had significantly greater value and contribution ratio of FOA than the pelvic retroversion group, which might suggest that knee flexion became more efficient when compensating for larger PI-LL mismatch by providing greater proportional femoral incline. Larger knee flexion needs more muscle strength and energy consumption. Moreover, it will lead to longer duration of the knee pain, a decrease in walking velocity and 11
stride length, and rapid muscle fatigue, and thus reduce the overall knee function and the ability to stand and walk [15]. It could also explain why the patients with minor PI-LL mismatch did not adopt pelvic retroposition to compensate.
Our data revealed that the value of TOA was not significantly different between the two PI-LL mismatch groups and had no significant correlation with the value of PI-LL, indicating that the degree of ankle dorsiflexion would not change with the aggravation of PI-LL mismatch. However, considering the opposite direction of motion between ankle dorsiflexion and pelvic retroversion and retroposition, the lower contribution ratio of TOA in the pelvic retroposition group could be favorable for the pelvic compensation to counter greater PI-LL mismatch. A previous study has proved that the gravity line is relatively fixed referring to the position of the feet wherever the pelvis is [10]. So pelvic retroposition would keep the pelvis away from the gravity line. The present results showed that the displacement of the pelvis was generated by the cooperation of knee flexion and ankle dorsiflexion.
The main limitation of this study is a relatively small sample size of patients with PI-LL mismatch. Although these cases have provided enough evidence to support the conclusions, a larger sample size is likely to reveal more information about the compensatory mechanisms in the pelvis and lower extremities. Additionally, this study only analyzed static posture of patients with sagittal spinal malalignment. The importance of dynamic aspects in spinal misalignment and/or spinopelvic mismatch has been reviewed recently [19]. The dynamic analysis may provide more 12
valuable results for these patients and would be performed in further studies.
Conclusions The pelvic compensation for PI-LL mismatch can be divided into pelvic retroversion and pelvic retroposition, which are measured by PT and PS respectively. Patients with lesser PI-LL mismatch rely more on hip extension to increase pelvic retroversion while those with greater PI-LL mismatch tend to add extra femoral obliquity. When compensating for larger PI-LL mismatch, the importance of hip extension is decreased and the effect of the knee and ankle joint becomes more important by providing greater femoral incline and relatively lesser ankle dorsiflexion respectively.
Conflict of interest statement All authors: none.
Acknowledgements This study was supported by the grant of The National Natural Science Foundation of China (81572168), Fund for Key Disciplines of Shanghai Municipal Education Commission (J50206) and The Important Disease Joint Research Project of Shanghai Health System (2013ZYJB0502).
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Figure Legends Figure 1 Illustration of radiographic measurements. (FOA, femoral obliquity angle; FPA, femur pelvis angle; KFA, knee flexion angle; LL, lumbar lordosis; PI, pelvic incidence; PS, pelvic shift; PT, pelvic tilt; SS, sacral slope; TK, thoracic kyphosis; TOA, tibial obliquity angle )
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Figure 2 Lateral radiographs depicting two different standing postures. A: patients in the pelvic retroversion group have an erect trunk, hyperextended hips and nearly vertical femurs formed by mild knee flexion and ankle dorsiflexion; B: patients in the pelvic retroposition group seem to be in a crouch posture owing to a forward inclination of the trunk and obvious femoral tilt in spite of extension of the hip joint itself.
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Table 1 Demographic and radiographic parameters for patients with lumbar degenerative diseases PI-LL
PI-LL mismatch group
match group Pelvic
P
Pelvic
P
P
retroversion
value1
retroposition
value1
value2
group
group 39
n
40
55
Gender (male/female)
11/29
15/40
0.580
10/29
0.527
0.527
Age (yrs)
56.1±7.7
59.7±7.9
0.052
59.7±11.0
0.078
0.974
Body mass index
22.4±3.7
0.780
0.548
0.365 21.6±4.1
22.1±4.2
2
(kg/m ) LL (°)
53.1±9.1
33.8±10.8 *
<0.001
27.8±15.3 *#
<0.001
0.017
Thoracic kyphosis (°)
42.6±6.7
34.6±11.7 *
0.001
29.1±14.1 *#
<0.001
0.022
PI (°)
47.4±8.8
47.6±10.2
0.900
55.1±11.0 *#
0.001
0.001
Sacral slope (°)
35.0±6.5
24.6±8.4 *
<0.001
28.0±10.2 *
<0.001
0.055
Pelvic tilt (°)
12.3±5.9
23.1±5.7 *
<0.001
26.9±5.5 *#
<0.001
0.002
PI-LL (°)
-5.8±2.5
13.0±7.5 *
<0.001
28.6±11.1 *#
<0.001
<0.001
Knee flexion angle (°)
3.4±2.3
7.5±3.4 *
<0.001
14.4±5.9 *#
<0.001
<0.001
Tibial obliquity angle
1.9±2.2
<0.001
0.080
<0.001 5.7±2.8
*
(°) 18
4.7±2.6
*
Femoral obliquity
1.5±2.8
0.693 1.9±3.4
9.7±6.1
<0.001
<0.001
<0.001
<0.001
<0.001
<0.001
*#
angle (°) Femur pelvis angle
10.8±6.9
<0.001 22.0±6.2
*
16.8±6.7
*#
(°) Pelvic shift (mm)
23.8±34.6
35.0±32.4
0.131
134.8±40.3 *#
Patients with PI-LL mismatch were subdivided into pelvic retroversion and retroposition group based on the value of pelvic tilt and pelvic shift using cluster analysis. Data were expressed as mean ± standard deviation; PI, pelvic incidence; LL, lumbar lordosis. 1
Compared with the PI-LL match group.
2
Compared with the pelvic retroversion group.
*
P<0.05 Compared with the PI-LL match group
#
P<0.05 Compared with the pelvic retroversion group
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Table 2 Comparison of contribution ratio of compensatory mechanisms between the pelvic retroversion and retroposition group Pelvic Pelvic retroversion group
retroposition
P value
group ΔThoracic kyphosis/PI-LL
0.78(0.93)
0.59(0.72)
0.070
ΔPelvic tilt/PI-LL
0.86(0.70)
0.63(0.59)
<0.001
ΔKnee flexion angle/PI-LL
0.29(0.37)
0.33(0.30)
0.064
ΔTibial obliquity angle/PI-LL
0.26(0.37)
0.18(0.28)
<0.001
ΔFemoral obliquity angle/PI-LL
0.03(0.34)
0.14(0.37)
<0.001
ΔFemur pelvis angle/PI-LL
0.83(1.12)
0.49(0.76)
<0.001
ΔPelvic shift/PI-LL
1.08(2.60)
2.59(3.24)
<0.001
We assumed the measured mean value in the control group as the ideal value and then calculated the differences between the ideal values and the measured values of the parameters involved in compensation in the two PI-LL mismatch groups. The quotients of the differences and the value of PI-LL for each subject were regarded as contribution ratios for the compensatory mechanisms. Data were expressed as median (interquartile range); PI, pelvic incidence; LL, lumbar lordosis.
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Table 3 Correlations between compensatory mechanisms and PI-LL mismatch for patients with PI-LL mismatch PI-LL r
P value
ΔThoracic kyphosis
0.353
<0.001
ΔPelvic tilt
0.517
<0.001
ΔKnee flexion angle
0.713
<0.001
ΔTibial obliquity angle
-0.113
0.272
ΔFemoral obliquity angle
0.719
<0.001
ΔFemur pelvis angle
-0.255
0.013
ΔPelvic shift
0.728
<0.001
Results indicated that the compensatory mechanisms in the pelvis and lower extremities, except for ankle rotation, were significantly correlated with PI-LL mismatch in the PI-LL mismatch group. PI, pelvic incidence; LL, lumbar lordosis.
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