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Kinematic and kinetic changes in obese gait in bariatric surgery-induced weight loss
Journal of Biomechanics 45 (2012) 1769–1774
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Kinematic and kinetic changes in obese gait in bariatric surgery-induced weight loss Paavo Vartiainen a,n, Timo Bragge a, Tarja Lyytinen b, Marko Hakkarainen a, Pasi A. Karjalainen a, Jari P. Arokoski b,c a
Department of Applied Physics, University of Eastern Finland, P.O. Box 1627, FI-70211 Kuopio, Finland Department of Physical and Rehabilitation Medicine, Kuopio University Hospital, P.O. Box 1777, FI-70211 Kuopio, Finland c Institute of Clinical Medicine, University of Eastern Finland, P.O. Box 1627, FI-70211 Kuopio, Finland b
a r t i c l e i n f o
abstract
Article history: Accepted 2 May 2012
This study examines the effects of a radical bariatric surgery-induced weight loss on the gait of obese subjects. We performed a three-dimensional motion analysis of lower limbs, and collected force platform data in the gait laboratory to calculate knee and hip joint moments. Subjects (n ¼13) performed walking trials in the laboratory before and 8.8 months (SD 4.2) after the surgical procedure at two gait speeds (1.2 m/s and 1.5 m/s). The average weight loss was 26.7 kg (SD 9.2 kg), corresponding to 21.5% (SD 6.8%) of the initial weight. We observed a decrease in step width at both gait speeds, but no changes in relative double support or swing time or stride length. A significant decrease was noted in the absolute values of peak knee abductor, peak knee flexor and peak hip extensor moments. However, the moment values normalized by the body weight and height remained unchanged in most cases. Thus, we conclude that weight loss reduces hip and knee joint moments in proportion to the amount of weight lost. & 2012 Elsevier Ltd. All rights reserved.
Keywords: Biomechanics Gait Obesity Weight loss Bariatric surgery
1. Introduction Obesity is one of the most serious chronic global disorders being a strong risk factor for several diseases including knee osteoarthritis (OA) (Haslam and James, 2005). Intuitively, it seems likely that obesity can increase the biomechanical loads in knee joint load, and it is generally accepted that knee OA is driven by ¨ biomechanical loading (Andriacchi and Mundermann, 2006). It has been reported that weight loss may cause a significant risk reduction of knee OA in the general population (Muthuri et al., 2011). There are inconsistent reports of the kinematic and kinetic parameters of walking in obese individuals but otherwise healthy subjects. Several studies report that obese adults or children have a shorter step length, a wider step width and a longer double support time (Spyropoulos et al., 1991; McGraw et al., 2000; Lai et al., 2008; Browning and Kram, 2007). Furthermore, peak knee flexion angles during the stance phase have been reported as being lower (Gushue et al., 2005; DeVita and Hortoba´gyi, 2003) and a smaller range of knee and hip motion in obese people has
n
Corresponding author Tel.: þ358 40 7058 247. E-mail address: paavo.vartiainen@uef.fi (P. Vartiainen). URL: http://bsamig.uku.fi (P. Vartiainen).
0021-9290/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jbiomech.2012.05.002
been reported (Messier, 1994). However, there are studies where no differences in cadence, stride length or double support time between obese and healthy weight children have been observed (Nantel et al., 2006), and knee flexion angles have also been found to be identical in some studies (Spyropoulos et al., 1991; Browning and Kram, 2007). DeVita and Hortoba´gyi (2003) stated that obese but otherwise healthy subjects had less absolute sagittal plane knee moment at their self-selected walking speed but equal moment while walking at the same speed as lean individuals. There is only one study evaluating the effects of weight loss on the biomechanics of walking in obese, but otherwise healthy adults (Hortoba´gyi et al., 2011). In that study, gait analysis was performed before and after bariatric surgery. The average weight loss was 33.6% (42.2 kg). Weight loss increased swing time and stride length at both the self-selected and the standard speed. Weight loss also increased the self-selected speed. At the selfselected speed, normalized peak knee extensor moment increased and absolute ankle and frontal plane knee moments declined after weight loss. At a fixed speed, no significant change was observed in normalized hip, knee or ankle moments. The effects of weight loss on joint loading in obese knee OA patients have been examined in two studies (Messier et al., 2005; Aaboe et al., 2011). Messier et al. (2005) showed that a onekilogram reduction in body weight was associated with a 1.4%
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reduction in peak knee abductor moment after statistically adjusting for several variables including age, walking speed, gender and subjective scores on knee pain and function. The average weight loss in their study was only 2.6%. The subjects in the study of Aaboe et al. (2011) experienced greater weight loss, the average reduction in body mass being 13.5%. They observed a significant reduction of up to 13% in peak knee abductor moment but no significant changes in sagittal plane knee moment at the participants’ freely chosen walking speed. The aim of our study was to quantify the kinematic and kinetic changes associated with radical weight loss following bariatric surgery in obese subjects. Subjects performed walking trials in the laboratory before and on average 8.8 months after the surgery at two gait speeds (1.2 m/s and 1.5 m/s) to evaluate the possible effect of gait speed on gait kinematics and kinetics. First, we hypothesized that weight loss would reduce knee and hip joint moments. Second, we hypothesized that weight loss could change gait kinematics towards the gait pattern of normal-weight individuals, i.e. narrower step width, shorter double support time and larger hip and knee range of motion according to earlier findings (Browning and Kram, 2007; DeVita and Hortoba´gyi, 2003; Spyropoulos et al., 1991).
2. Methods 2.1. Subjects Participants were recruited from the clinical nutrition unit of Kuopio University Hospital, Kuopio, Finland. The recruitment period was from October 2008 to August 2010. The entry criteria consisted of patients being cleared for bariatric surgery at Kuopio University Hospital and willingness to take part in the present study. Previous knee or hip arthroplasty was an exclusion criterion. Each participant provided written consent to participate in this study after receiving detailed information about the study design. The Ethics Committee of the Kuopio University Hospital approved the study design. At baseline, 15 female and three male middle-aged obese adults aged between 30 and 63 years were recruited for this study. The baseline measurement for each subject was performed before the bariatric surgery. The follow-up measurements were performed 8.8 (SD 4.2) months after the surgery. Two subjects refused to participate in the follow-up measurements due to personal reasons. Two subjects failed to complete the tests at 1.2 m/s and 1.5 m/s walking speeds and one subject was excluded because ground reaction force data from the follow-up measurement was lost. The characteristics of the 13 participants (10 female and three male) included into the final evaluation are shown in Table 1. From these subjects, one failed to complete tests at 1.5 m/s and one subject’s camera data was lost at 1.2 m/s walking speed. At baseline all 13 subjects were severely or morbidly obese, i.e. the body mass index (BMI) was 4 35 kg=m2 (range 36.4–49.7). Average weight loss was 26.7 kg (SD 9.2 kg), corresponding to 21.5% (SD 6.8%) of the initial weight. The self-reported disease-specific joint pain was assessed using the Western Ontario and McMaster Universities (WOMAC) Osteoarthritis Index (Bellamy et al., 1988). Four subjects reported mild knee pain (Table 1). The knee and pelvis radiographs were taken and evaluated using Kellgren– Lawrence grading (Kellgren et al., 1963), in which grade Z 2 was regarded as knee or hip OA. According to the radiographic score of the subjects, none had hip OA and three subjects had mild knee OA (KL 2) and one subject had moderate knee OA (KL 3) (Table 1). 2.2. Equipment and experimental set-up We performed gait analysis in our gait laboratory (Hakkarainen et al., 2010; Liikavainio et al., 2007). We measured ground reaction forces with force platforms and recorded 3D-kinematics of lower limbs with a camera-based system. The laboratory has a ten-meter long walkway covered with a rubber mat. Threedimensional ground reaction forces (GRFs) were measured with two force platforms (Model OR6-7MA, AMTI Inc., MA, USA) embedded in the walkway. The platforms were able to measure two consecutive steps, and the walkway allowed three acceleration steps before reaching the platforms. The GRF data during the stance phase were collected and stored with AMTI software at 1000 Hz. Kinematic data were acquired using a 3D motion capture system (Hakkarainen et al., 2010). The system is based on six Basler A602f cameras at 100 frames/s. The calibration was performed based on a DLT method. The error in reconstructed 3D-coordinates was not more than a few millimeters. Walking speed was measured using a pair of photo-cells located 2.5 m apart on either side of the force platforms. The data
Table 1 Subject characteristics (n¼ 13). Values are means (SD) and knee and hip radiographic KL-gradings are number of subjects. Variables Age (years) Weight (kg) Baseline Follow-up BMI (kg/m2) Baseline Follow-up WOMACa Pain (0–100 mm) Baseline Follow-up Knee/hip KL-gradingb 0 1 2 3 4
45.5 (10.3) 123.3 (19.1) 96.6 (16.2) 42.2 (3.9) 33.1 (3.8)
15.8 (11.6) 9.1 (4.5) 5/12 4/1 3/0 1/0 0/0
a Those who reported knee pain (n¼ 4), WOMAC (Western Ontario and McMaster Universities Arthritis Index). b The more severely affected side, Kellgren–Lawrence (KL) grade.
collection was initiated when the subject passed the first photo-cell. This, along with the sufficient calibration volume of the camera system, enabled the recording of 3D-kinematics of four consecutive steps. The subjects were given enough time for warm-up and to become familiar with the experiment protocol. Subsequently, subjects walked barefoot at pre-determined gait speeds, 1.2 m/s and 1.5 m/s, along the walkway. Six trials at both speeds were recorded, with the trial order being randomized. A trial was discarded if both feet did not hit the force platforms or if purposeful targeting on the platforms was observed. Furthermore, gait speed had to be within 75% of the target speed. Subjects wore tight-fitting spandex trousers and a shirt. Retro-reflective spherical markers (diameter 18 mm) were attached on the skin of the feet and onto the spandex suit. Marker placement was based on modified Helen Hayes marker set, where three markers per segment were mounted. Marker locations were the posterior heel, first and fifth metatarsal heads, lateral malleoli, tuberositas tibiae, lateral knee joint space, gastrocnemius muscle, biceps femoris muscle, trocanter major, spina iliaca anterior superior and lumbar vertebra.
2.3. Data analysis The camera data were processed and parameters were computed using software developed in the BSAMIG research group in MATLAB R2010a environment (The MathWorks Inc., MA, USA). Forces and moments at the knee and hip joints were computed by combining ground reaction force data with position data using an inverse dynamic solution. The position and linear and angular velocities and accelerations of the segments were estimated using a Kalman filter and Kalman smoother-based method (Groote et al., 2008). Inverse dynamics computations were carried out using a seven-segment model. The segments were the pelvis, both thighs, shanks and feet. Relative segment masses were taken from the literature (Nigg and Herzog, 1999). The lengths of the model segments were based on the observed marker trajectories, i.e. the model was scaled to match the data. We analysed hip and knee moments in the sagittal plane and knee moments in the frontal plane (Fig. 1). Moments were normalized by dividing the absolute values by the product of the subject’s mass and height. Cadence parameters were calculated using kinematic data. To determine step width, we defined two lines which connected consecutive heel contact points of the same foot. The step width was determined as the distance between a line and the opposite heel contact point. Joint angle and moment graphs were calculated for all six trials. Clear outliers were removed based on visual inspection of the graphs. Parameter values were determined from the remaining trials. The value of the parameter for a subject was defined as the mean of these values. The nonparametric Wilcoxon signed rank test was used to determine the differences between the baseline and the follow-up measurements on the computed variables. The level of significance was set at p o 0:05.
3. Results No differences between the baseline and the follow-up were observed in swing time, in double support time or in stride length,
P. Vartiainen et al. / Journal of Biomechanics 45 (2012) 1769–1774
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M (Nm)
100
ext
Mhip 0 flex
Mhip −100
0
50
100
50
50
ext
M (Nm)
Mknee
Madd1 knee
0
add2 knee
M
flex knee
M −50
0
0
50
100
0
Percents of contact time
50 Percents of contact time
100
Fig. 1. Schematic illustration of kinetic parameters determined in the study. (A) Hip moment in sagittal plane: peak hip extensor moment Mext hip and peak hip flexor ext flex moment Mflex hip . (B) Knee moment in sagittal plane: peak knee extensor moment Mknee and peak knee flexor moment Mknee . (C) Knee moment in frontal plane: peak knee add2 abductor moment during early stance Madd1 knee and peak knee abductor moment during late stance Mknee .
Table 2 Cadence parameters (means (SD)) at gait speeds 1.2 m/s and 1.5 m/s. Significant p-values in bold. Parameter
Step width (m) Double support time (% gait cycle) Swing time (% gait cycle) Stride length (m) a
1.2 m/s
1.5 m/s
Baseline
Follow-up
p-Valuea
Baseline
Follow-up
p-Value
0.12 14.6 37.6 1.29
0.09 14.1 37.8 1.30
0.001 0.570 0.470 0.850
0.13 13.2 40.0 1.42
0.09 12.9 40.1 1.42
o 0:001 0.420 0.970 0.850
(0.03) (1.8) (1.3) (0.09)
(0.03) (0.9) (1.3) (0.10)
(0.02) (1.3) (1.0) (0.09)
(0.02) (1.3) (1.8) (0.08)
Wilcoxon signed-rank test.
whereas a significant decrease in step width was observed (Table 2). The hip flexion angle at initial contact decreased significantly at both gait speeds, but no significant changes were observed in knee joint angles (Table 3). Individual changes in absolute values of moment parameters are presented in Figs. 2 and 3. A significant decrease in absolute values were observed in peak knee abductor moments, peak hip extensor moment and in peak knee flexor moment (Table 4). The only significant difference in normalized moments was the increase in peak knee abductor moment during the early stance at a gait speed of 1.5 m/s.
4. Discussion The main finding of the present study is that the absolute values of peak hip extensor and knee abductor and flexor joint moments decreased significantly following weight loss, while most normalized values of moments showed no significant
changes. Weight loss also changed gait kinematics; i.e. there were significant decreases in step width and hip flexion angle at initial contact. Absolute values of joint moments decreased as the weight declined, as was hypothesized. The change in peak knee abductor moment was 18.6% in early stance and 15.6% in late stance at the gait speed of 1.2 m/s following 21.5% weight loss. At the gait speed of 1.5 m/s, the changes were 12.7% and 13.1%, respectively. These decreases were smaller than those previously reported when amount of weight lost is taken into account; Hortoba´gyi et al. (2011) described a 27.0% change in peak knee abductor moment in early stance with the weight loss of 33.6% in otherwise healthy subjects and Aaboe et al. (2011) reported up to 13% in the peak knee abductor moment with a weight loss of 13.6% in knee OA subjects. Normalized values of sagittal plane moments revealed no significant changes, which means that absolute values of moments decreased in proportion to the weight loss. Most normalized peak knee abductor moments also remained
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Table 3 Hip and knee angles (means (SD)) at gait speeds 1.2 m/s and 1.5 m/s. Significant p-values in bold. Parameter
1.2 m/s
Hip flexion angle at initial contact (1) Peak knee flexion angle during early stance (1) Knee flexion angle at initial contact (1) Knee minimum flexion angle during stance (1) Knee flexion angle at toe off (1) a
1.5 m/s
Baseline
Follow-up
p-Valuea
Baseline
Follow-up
p-Value
32 (6) 22 (5) 13 (6) 1 (9) 38 (1)
26 (4) 19 (5) 10 (7) 0 (7) 38 (1)
0.010 0.090 0.150 0.380 0.470
32 (7) 24 (7) 14 (8) 5 (9) 40 (1)
27 (5) 22 (6) 14 (7) 2 (7) 40 (2)
0.020 0.730 0.790 0.300 0.970
Wilcoxon signed-rank test.
PEAK KNEE ABDUCTOR MOMENT DURING LATE STANCE
Speed: 1.5 m/s Nm
Speed: 1.2 m/s Nm
PEAK KNEE ABDUCTOR MOMENT DURING EARLY STANCE
100
100
50
50
0
0
100
100
50
50
0
0
Fig. 2. Individual changes in the absolute knee abductor moment parameters at two gait speeds, 1.2 m/s (top) and 1.5 m/s (bottom). The left end of the line points to the value of the parameter at the baseline and the right end at the follow-up measurement. The thick dashed line represents the mean change and thick vertical lines show the standard deviations.
statistically unchanged, the only exception being in the peak abductor moment during early stance at gait speed 1.5 m/s, which increased significantly. This would counteract the beneficial effects of weight loss on compressive loads being transmitted to the medial compartment of the knee. However, the importance of our finding is uncertain, because we detected no effect on that moment at the gait speed of 1.2 m/s. Thus, our results are rather consistent with those of Hortoba´gyi et al. (2011), who observed
no significant changes in normalized peak knee extensor or peak knee abductor moments in otherwise healthy subjects. There is also evidence that in knee OA subjects extensive weight loss does not modify knee moments (Messier et al., 2011). Hortoba´gyi et al. (2011) demonstrated that weight loss produced a substantial decrease in the absolute ankle plantar flexion moment at a standard walking speed (1.51 m/s), but the normalized ankle moments did not change after weight loss. We did not report ankle joint parameters in our study, since the markers on the forefoot could not be identified reliably in some situations. However, markers on the lateral malleoli were successfully tracked and thus we were able to determine the position of the ankle joint. We also accurately determined GRF application point and thus we were able to complete calculations in inverse dynamics chain. Figs. 2 and 3 together with the large standard deviation values show that variations in the changes of moments are remarkable. In some subjects, moment values increased, even though the mean value decreased significantly. This suggests that in the presurgery state, some individuals had gait adaptations which lowered the joint moments at the baseline measurement due to neuromuscular adaptation (DeVita and Hortoba´gyi, 2003). The average decreases in step width were remarkable, 3 cm at gait speed 1.2 m/s and 4 cm at gait speed 1.5 m/s. It is possible that when individuals have more mass they have to place their feet wider apart to maintain their dynamic stability. The decrease in this value may also be explained by the reduced girth of the thighs. There are no earlier reports on the effects of weight loss on the step width. Browning and Kram (2007) observed a greater step width in the obese than in the normal-weight group. Thus, the association of larger weight and wider step width found in the present study is consistent with the findings of Browning and Kram. We observed no changes in relative double support time or swing time. These results are inconsistent with those of Browning and Kram (2007), who found a greater relative stance time and swing time in the obese group compared to normal-weight group. In addition, we observed no change in stride length. However, an increase in stride length related to weight loss has been reported previously, even at a fixed gait speed (Hortoba´gyi et al., 2011). We cannot find any single explanation for this inconsistency. The significant decrease we observed in hip flexion angle at initial contact is contrary to our initial hypothesis and also is inconsistent with the findings of Hortoba´gyi et al. (2011), who reported increased hip range of motion at a self-selected speed after weight loss. In our study, stride length did not change although after surgery the hip was less flexed at initial contact. This might be partly due to the fact that the knee was simultaneously less flexed and there may also be changes in pelvis rotation. We used fixed gait speeds to prevent speed affecting the gait parameters. If we had used a self-selected speed, the speed might well have increased following the weight loss, as shown earlier by Aaboe et al. (2011) and Hortoba´gyi et al. (2011). A higher speed would probably have increased the joint moments and thus
P. Vartiainen et al. / Journal of Biomechanics 45 (2012) 1769–1774
PEAK HIP EXTENSOR MOMENT
0
PEAK HIP FLEXOR MOMENT
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PEAK KNEE EXTENSOR MOMENT
PEAK KNEE FLEXOR MOMENT
200 0
−50
100
Speed: 1.2 m/s Nm
150 −100
100
50
−150
−50
−200 50 0
−250
−100
0 0 200
0
−50
100
Speed: 1.5 m/s Nm
150 −100
100
50
−150
−50
−200 50 0
−250 0
−100
Fig. 3. Individual changes in the absolute sagittal plane moment parameters at two gait speeds, 1.2 m/s (top) and 1.5 m/s (bottom). The left end of the line points to the value of the parameter at the baseline and the right end at the follow-up measurement. The thick dashed line represents the mean change and thick vertical lines show the standard deviations.
Table 4 Knee and hip joint absolute and normalized moments (means (SD)) at gait speeds 1.2 m/s and 1.5 m/s. Significant p-values in bold. Parameter
1.2 m/s Baseline
Peak knee abductor moment during early stance Absolute (N m) 70 (22) Normalized (N m/kg m) 0.32 (0.07) Peak knee abductor moment during late stance Absolute (N m) 64 (22) Normalized (N m/kg m) 0.29 (0.09) Peak knee extensor moment Absolute (N m) 44 (33) Normalized (N m/kg m) 0.19 (0.13) Peak knee flexor moment Absolute (N m) 50 (26) Normalized (N m/kg m) 0.24 (0.14) Peak hip extensor moment Absolute (N m) 119 (27) Normalized (N m/kg m) 0.57 (0.15) Peak hip flexor moment Absolute (N m) 93 (27) Normalized (N m/kg m) 0.43 (0.13) a
1.5 m/s a
Baseline
Follow-up
p-Value
0.016 0.791
71 (27) 0.32 (0.08)
62 (19) 0.36 (0.07)
0.043 0.007
54 (16) 0.31 (0.07)
0.016 0.204
61 (20) 0.28 (0.08)
53 (16) 0.30 (0.08)
0.092 0.110
33 (22) 0.18 (0.10)
0.204 0.970
53 (37) 0.23 (0.15)
44 (29) 0.25 (0.15)
0.424 0.733
39 (19) 0.23 (0.12)
0.043 0.424
61 (21) 0.29 (0.12)
43 (20) 0.26 (0.13)
0.003 0.339
89 (20) 0.54 (0.10)
o 0:001 1.000
162 (34) 0.76 (0.15)
123 (32) 0.75 (0.18)
0.016 1.000
86 (55) 0.48 (0.18)
0.233 0.791
105 (28) 0.48 (0.10)
100 (63) 0.55 (0.21)
0.424 0.622
Follow-up
p-Value
57 (19) 0.32 (0.07)
Wilcoxon signed-rank test.
counteracted the effects of the weight loss. We used slower (1.2 m/s) and faster (1.5 m/s) speeds, which are estimates of normal gait speed for healthy individuals (Bohannon and Andrews, 2011). We presumed
that the changes in gait parameters would have been clearer when subjects were performing a more demanding walking task, but no clear differences were observed.
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In our study, the nine participants were obese without musculoskeletal pathology in their lower extremities and four subjects had knee OA. Due to the small sample size and the fact that the knee OA subjects mainly suffered from mild radiographic disease with minor knee pain, we did not perform comparison between these two subgroups. In our knee OA subjects the knee pain was comparable to those of Hortoba´gyi et al. (2011) who had obese, but otherwise healthy adults in their study. It is not possible resolve which of the other possible confounding factors, i.e. subjective knee pain, gender or age had any direct effects on the measured parameters. We recognize some limitations in the study. First, the validity of marker-based motion analysis is limited by the difficulties in marker placement especially in obese subjects, who have thick layers of soft tissue on most anatomic landmarks. Second, during weight loss, the thickness of soft tissue may decrease, and thus it is impossible to achieve identical marker placements at the follow-up measurements as used at the baseline. Our modelbased method allows for variations in marker placement, as the marker locations in the model can be modified. However, it is challenging to determine the marker locations in the model so that they would precisely represent the sites of the bony structures of the lower limbs. Third, soft tissue and the spandex suit may cause movement artifacts. Finally, the joint angle values are error-prone, because we did not perform calibration measurements to determine zero angles for the knee and hip. The present study shows that hip and knee moments are reduced in proportion to the weight loss following extensive weight loss, and that step width is reduced. Larger, prospective studies are needed to evaluate, if these gait changes reduce emergence of new knee OA cases.
Conflict of interest statement The authors declare no conflict of interest.
Acknowledgments This study has been supported by the strategic funding of the University of Eastern Finland and by a grant (5960431) from Kuopio University Hospital. References Aaboe, J., Bliddal, H., Messier, S., Alkjar, T., Henriksen, M., 2011. Effects of an intensive weight loss program on knee joint loading in obese adults with knee osteoarthritis. Osteoarthritis and Cartilage 19 (7), 822–828.
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Kinematic and kinetic changes in obese gait in bariatric surgery-induced weight loss Paavo Vartiainen a,n, Timo Bragge a, Tarja Lyytinen b, Marko Hakkarainen a, Pasi A. Karjalainen a, Jari P. Arokoski b,c a
Department of Applied Physics, University of Eastern Finland, P.O. Box 1627, FI-70211 Kuopio, Finland Department of Physical and Rehabilitation Medicine, Kuopio University Hospital, P.O. Box 1777, FI-70211 Kuopio, Finland c Institute of Clinical Medicine, University of Eastern Finland, P.O. Box 1627, FI-70211 Kuopio, Finland b
a r t i c l e i n f o
abstract
Article history: Accepted 2 May 2012
This study examines the effects of a radical bariatric surgery-induced weight loss on the gait of obese subjects. We performed a three-dimensional motion analysis of lower limbs, and collected force platform data in the gait laboratory to calculate knee and hip joint moments. Subjects (n ¼13) performed walking trials in the laboratory before and 8.8 months (SD 4.2) after the surgical procedure at two gait speeds (1.2 m/s and 1.5 m/s). The average weight loss was 26.7 kg (SD 9.2 kg), corresponding to 21.5% (SD 6.8%) of the initial weight. We observed a decrease in step width at both gait speeds, but no changes in relative double support or swing time or stride length. A significant decrease was noted in the absolute values of peak knee abductor, peak knee flexor and peak hip extensor moments. However, the moment values normalized by the body weight and height remained unchanged in most cases. Thus, we conclude that weight loss reduces hip and knee joint moments in proportion to the amount of weight lost. & 2012 Elsevier Ltd. All rights reserved.
Keywords: Biomechanics Gait Obesity Weight loss Bariatric surgery
1. Introduction Obesity is one of the most serious chronic global disorders being a strong risk factor for several diseases including knee osteoarthritis (OA) (Haslam and James, 2005). Intuitively, it seems likely that obesity can increase the biomechanical loads in knee joint load, and it is generally accepted that knee OA is driven by ¨ biomechanical loading (Andriacchi and Mundermann, 2006). It has been reported that weight loss may cause a significant risk reduction of knee OA in the general population (Muthuri et al., 2011). There are inconsistent reports of the kinematic and kinetic parameters of walking in obese individuals but otherwise healthy subjects. Several studies report that obese adults or children have a shorter step length, a wider step width and a longer double support time (Spyropoulos et al., 1991; McGraw et al., 2000; Lai et al., 2008; Browning and Kram, 2007). Furthermore, peak knee flexion angles during the stance phase have been reported as being lower (Gushue et al., 2005; DeVita and Hortoba´gyi, 2003) and a smaller range of knee and hip motion in obese people has
n
Corresponding author Tel.: þ358 40 7058 247. E-mail address: paavo.vartiainen@uef.fi (P. Vartiainen). URL: http://bsamig.uku.fi (P. Vartiainen).
0021-9290/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jbiomech.2012.05.002
been reported (Messier, 1994). However, there are studies where no differences in cadence, stride length or double support time between obese and healthy weight children have been observed (Nantel et al., 2006), and knee flexion angles have also been found to be identical in some studies (Spyropoulos et al., 1991; Browning and Kram, 2007). DeVita and Hortoba´gyi (2003) stated that obese but otherwise healthy subjects had less absolute sagittal plane knee moment at their self-selected walking speed but equal moment while walking at the same speed as lean individuals. There is only one study evaluating the effects of weight loss on the biomechanics of walking in obese, but otherwise healthy adults (Hortoba´gyi et al., 2011). In that study, gait analysis was performed before and after bariatric surgery. The average weight loss was 33.6% (42.2 kg). Weight loss increased swing time and stride length at both the self-selected and the standard speed. Weight loss also increased the self-selected speed. At the selfselected speed, normalized peak knee extensor moment increased and absolute ankle and frontal plane knee moments declined after weight loss. At a fixed speed, no significant change was observed in normalized hip, knee or ankle moments. The effects of weight loss on joint loading in obese knee OA patients have been examined in two studies (Messier et al., 2005; Aaboe et al., 2011). Messier et al. (2005) showed that a onekilogram reduction in body weight was associated with a 1.4%
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reduction in peak knee abductor moment after statistically adjusting for several variables including age, walking speed, gender and subjective scores on knee pain and function. The average weight loss in their study was only 2.6%. The subjects in the study of Aaboe et al. (2011) experienced greater weight loss, the average reduction in body mass being 13.5%. They observed a significant reduction of up to 13% in peak knee abductor moment but no significant changes in sagittal plane knee moment at the participants’ freely chosen walking speed. The aim of our study was to quantify the kinematic and kinetic changes associated with radical weight loss following bariatric surgery in obese subjects. Subjects performed walking trials in the laboratory before and on average 8.8 months after the surgery at two gait speeds (1.2 m/s and 1.5 m/s) to evaluate the possible effect of gait speed on gait kinematics and kinetics. First, we hypothesized that weight loss would reduce knee and hip joint moments. Second, we hypothesized that weight loss could change gait kinematics towards the gait pattern of normal-weight individuals, i.e. narrower step width, shorter double support time and larger hip and knee range of motion according to earlier findings (Browning and Kram, 2007; DeVita and Hortoba´gyi, 2003; Spyropoulos et al., 1991).
2. Methods 2.1. Subjects Participants were recruited from the clinical nutrition unit of Kuopio University Hospital, Kuopio, Finland. The recruitment period was from October 2008 to August 2010. The entry criteria consisted of patients being cleared for bariatric surgery at Kuopio University Hospital and willingness to take part in the present study. Previous knee or hip arthroplasty was an exclusion criterion. Each participant provided written consent to participate in this study after receiving detailed information about the study design. The Ethics Committee of the Kuopio University Hospital approved the study design. At baseline, 15 female and three male middle-aged obese adults aged between 30 and 63 years were recruited for this study. The baseline measurement for each subject was performed before the bariatric surgery. The follow-up measurements were performed 8.8 (SD 4.2) months after the surgery. Two subjects refused to participate in the follow-up measurements due to personal reasons. Two subjects failed to complete the tests at 1.2 m/s and 1.5 m/s walking speeds and one subject was excluded because ground reaction force data from the follow-up measurement was lost. The characteristics of the 13 participants (10 female and three male) included into the final evaluation are shown in Table 1. From these subjects, one failed to complete tests at 1.5 m/s and one subject’s camera data was lost at 1.2 m/s walking speed. At baseline all 13 subjects were severely or morbidly obese, i.e. the body mass index (BMI) was 4 35 kg=m2 (range 36.4–49.7). Average weight loss was 26.7 kg (SD 9.2 kg), corresponding to 21.5% (SD 6.8%) of the initial weight. The self-reported disease-specific joint pain was assessed using the Western Ontario and McMaster Universities (WOMAC) Osteoarthritis Index (Bellamy et al., 1988). Four subjects reported mild knee pain (Table 1). The knee and pelvis radiographs were taken and evaluated using Kellgren– Lawrence grading (Kellgren et al., 1963), in which grade Z 2 was regarded as knee or hip OA. According to the radiographic score of the subjects, none had hip OA and three subjects had mild knee OA (KL 2) and one subject had moderate knee OA (KL 3) (Table 1). 2.2. Equipment and experimental set-up We performed gait analysis in our gait laboratory (Hakkarainen et al., 2010; Liikavainio et al., 2007). We measured ground reaction forces with force platforms and recorded 3D-kinematics of lower limbs with a camera-based system. The laboratory has a ten-meter long walkway covered with a rubber mat. Threedimensional ground reaction forces (GRFs) were measured with two force platforms (Model OR6-7MA, AMTI Inc., MA, USA) embedded in the walkway. The platforms were able to measure two consecutive steps, and the walkway allowed three acceleration steps before reaching the platforms. The GRF data during the stance phase were collected and stored with AMTI software at 1000 Hz. Kinematic data were acquired using a 3D motion capture system (Hakkarainen et al., 2010). The system is based on six Basler A602f cameras at 100 frames/s. The calibration was performed based on a DLT method. The error in reconstructed 3D-coordinates was not more than a few millimeters. Walking speed was measured using a pair of photo-cells located 2.5 m apart on either side of the force platforms. The data
Table 1 Subject characteristics (n¼ 13). Values are means (SD) and knee and hip radiographic KL-gradings are number of subjects. Variables Age (years) Weight (kg) Baseline Follow-up BMI (kg/m2) Baseline Follow-up WOMACa Pain (0–100 mm) Baseline Follow-up Knee/hip KL-gradingb 0 1 2 3 4
45.5 (10.3) 123.3 (19.1) 96.6 (16.2) 42.2 (3.9) 33.1 (3.8)
15.8 (11.6) 9.1 (4.5) 5/12 4/1 3/0 1/0 0/0
a Those who reported knee pain (n¼ 4), WOMAC (Western Ontario and McMaster Universities Arthritis Index). b The more severely affected side, Kellgren–Lawrence (KL) grade.
collection was initiated when the subject passed the first photo-cell. This, along with the sufficient calibration volume of the camera system, enabled the recording of 3D-kinematics of four consecutive steps. The subjects were given enough time for warm-up and to become familiar with the experiment protocol. Subsequently, subjects walked barefoot at pre-determined gait speeds, 1.2 m/s and 1.5 m/s, along the walkway. Six trials at both speeds were recorded, with the trial order being randomized. A trial was discarded if both feet did not hit the force platforms or if purposeful targeting on the platforms was observed. Furthermore, gait speed had to be within 75% of the target speed. Subjects wore tight-fitting spandex trousers and a shirt. Retro-reflective spherical markers (diameter 18 mm) were attached on the skin of the feet and onto the spandex suit. Marker placement was based on modified Helen Hayes marker set, where three markers per segment were mounted. Marker locations were the posterior heel, first and fifth metatarsal heads, lateral malleoli, tuberositas tibiae, lateral knee joint space, gastrocnemius muscle, biceps femoris muscle, trocanter major, spina iliaca anterior superior and lumbar vertebra.
2.3. Data analysis The camera data were processed and parameters were computed using software developed in the BSAMIG research group in MATLAB R2010a environment (The MathWorks Inc., MA, USA). Forces and moments at the knee and hip joints were computed by combining ground reaction force data with position data using an inverse dynamic solution. The position and linear and angular velocities and accelerations of the segments were estimated using a Kalman filter and Kalman smoother-based method (Groote et al., 2008). Inverse dynamics computations were carried out using a seven-segment model. The segments were the pelvis, both thighs, shanks and feet. Relative segment masses were taken from the literature (Nigg and Herzog, 1999). The lengths of the model segments were based on the observed marker trajectories, i.e. the model was scaled to match the data. We analysed hip and knee moments in the sagittal plane and knee moments in the frontal plane (Fig. 1). Moments were normalized by dividing the absolute values by the product of the subject’s mass and height. Cadence parameters were calculated using kinematic data. To determine step width, we defined two lines which connected consecutive heel contact points of the same foot. The step width was determined as the distance between a line and the opposite heel contact point. Joint angle and moment graphs were calculated for all six trials. Clear outliers were removed based on visual inspection of the graphs. Parameter values were determined from the remaining trials. The value of the parameter for a subject was defined as the mean of these values. The nonparametric Wilcoxon signed rank test was used to determine the differences between the baseline and the follow-up measurements on the computed variables. The level of significance was set at p o 0:05.
3. Results No differences between the baseline and the follow-up were observed in swing time, in double support time or in stride length,
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M (Nm)
100
ext
Mhip 0 flex
Mhip −100
0
50
100
50
50
ext
M (Nm)
Mknee
Madd1 knee
0
add2 knee
M
flex knee
M −50
0
0
50
100
0
Percents of contact time
50 Percents of contact time
100
Fig. 1. Schematic illustration of kinetic parameters determined in the study. (A) Hip moment in sagittal plane: peak hip extensor moment Mext hip and peak hip flexor ext flex moment Mflex hip . (B) Knee moment in sagittal plane: peak knee extensor moment Mknee and peak knee flexor moment Mknee . (C) Knee moment in frontal plane: peak knee add2 abductor moment during early stance Madd1 knee and peak knee abductor moment during late stance Mknee .
Table 2 Cadence parameters (means (SD)) at gait speeds 1.2 m/s and 1.5 m/s. Significant p-values in bold. Parameter
Step width (m) Double support time (% gait cycle) Swing time (% gait cycle) Stride length (m) a
1.2 m/s
1.5 m/s
Baseline
Follow-up
p-Valuea
Baseline
Follow-up
p-Value
0.12 14.6 37.6 1.29
0.09 14.1 37.8 1.30
0.001 0.570 0.470 0.850
0.13 13.2 40.0 1.42
0.09 12.9 40.1 1.42
o 0:001 0.420 0.970 0.850
(0.03) (1.8) (1.3) (0.09)
(0.03) (0.9) (1.3) (0.10)
(0.02) (1.3) (1.0) (0.09)
(0.02) (1.3) (1.8) (0.08)
Wilcoxon signed-rank test.
whereas a significant decrease in step width was observed (Table 2). The hip flexion angle at initial contact decreased significantly at both gait speeds, but no significant changes were observed in knee joint angles (Table 3). Individual changes in absolute values of moment parameters are presented in Figs. 2 and 3. A significant decrease in absolute values were observed in peak knee abductor moments, peak hip extensor moment and in peak knee flexor moment (Table 4). The only significant difference in normalized moments was the increase in peak knee abductor moment during the early stance at a gait speed of 1.5 m/s.
4. Discussion The main finding of the present study is that the absolute values of peak hip extensor and knee abductor and flexor joint moments decreased significantly following weight loss, while most normalized values of moments showed no significant
changes. Weight loss also changed gait kinematics; i.e. there were significant decreases in step width and hip flexion angle at initial contact. Absolute values of joint moments decreased as the weight declined, as was hypothesized. The change in peak knee abductor moment was 18.6% in early stance and 15.6% in late stance at the gait speed of 1.2 m/s following 21.5% weight loss. At the gait speed of 1.5 m/s, the changes were 12.7% and 13.1%, respectively. These decreases were smaller than those previously reported when amount of weight lost is taken into account; Hortoba´gyi et al. (2011) described a 27.0% change in peak knee abductor moment in early stance with the weight loss of 33.6% in otherwise healthy subjects and Aaboe et al. (2011) reported up to 13% in the peak knee abductor moment with a weight loss of 13.6% in knee OA subjects. Normalized values of sagittal plane moments revealed no significant changes, which means that absolute values of moments decreased in proportion to the weight loss. Most normalized peak knee abductor moments also remained
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Table 3 Hip and knee angles (means (SD)) at gait speeds 1.2 m/s and 1.5 m/s. Significant p-values in bold. Parameter
1.2 m/s
Hip flexion angle at initial contact (1) Peak knee flexion angle during early stance (1) Knee flexion angle at initial contact (1) Knee minimum flexion angle during stance (1) Knee flexion angle at toe off (1) a
1.5 m/s
Baseline
Follow-up
p-Valuea
Baseline
Follow-up
p-Value
32 (6) 22 (5) 13 (6) 1 (9) 38 (1)
26 (4) 19 (5) 10 (7) 0 (7) 38 (1)
0.010 0.090 0.150 0.380 0.470
32 (7) 24 (7) 14 (8) 5 (9) 40 (1)
27 (5) 22 (6) 14 (7) 2 (7) 40 (2)
0.020 0.730 0.790 0.300 0.970
Wilcoxon signed-rank test.
PEAK KNEE ABDUCTOR MOMENT DURING LATE STANCE
Speed: 1.5 m/s Nm
Speed: 1.2 m/s Nm
PEAK KNEE ABDUCTOR MOMENT DURING EARLY STANCE
100
100
50
50
0
0
100
100
50
50
0
0
Fig. 2. Individual changes in the absolute knee abductor moment parameters at two gait speeds, 1.2 m/s (top) and 1.5 m/s (bottom). The left end of the line points to the value of the parameter at the baseline and the right end at the follow-up measurement. The thick dashed line represents the mean change and thick vertical lines show the standard deviations.
statistically unchanged, the only exception being in the peak abductor moment during early stance at gait speed 1.5 m/s, which increased significantly. This would counteract the beneficial effects of weight loss on compressive loads being transmitted to the medial compartment of the knee. However, the importance of our finding is uncertain, because we detected no effect on that moment at the gait speed of 1.2 m/s. Thus, our results are rather consistent with those of Hortoba´gyi et al. (2011), who observed
no significant changes in normalized peak knee extensor or peak knee abductor moments in otherwise healthy subjects. There is also evidence that in knee OA subjects extensive weight loss does not modify knee moments (Messier et al., 2011). Hortoba´gyi et al. (2011) demonstrated that weight loss produced a substantial decrease in the absolute ankle plantar flexion moment at a standard walking speed (1.51 m/s), but the normalized ankle moments did not change after weight loss. We did not report ankle joint parameters in our study, since the markers on the forefoot could not be identified reliably in some situations. However, markers on the lateral malleoli were successfully tracked and thus we were able to determine the position of the ankle joint. We also accurately determined GRF application point and thus we were able to complete calculations in inverse dynamics chain. Figs. 2 and 3 together with the large standard deviation values show that variations in the changes of moments are remarkable. In some subjects, moment values increased, even though the mean value decreased significantly. This suggests that in the presurgery state, some individuals had gait adaptations which lowered the joint moments at the baseline measurement due to neuromuscular adaptation (DeVita and Hortoba´gyi, 2003). The average decreases in step width were remarkable, 3 cm at gait speed 1.2 m/s and 4 cm at gait speed 1.5 m/s. It is possible that when individuals have more mass they have to place their feet wider apart to maintain their dynamic stability. The decrease in this value may also be explained by the reduced girth of the thighs. There are no earlier reports on the effects of weight loss on the step width. Browning and Kram (2007) observed a greater step width in the obese than in the normal-weight group. Thus, the association of larger weight and wider step width found in the present study is consistent with the findings of Browning and Kram. We observed no changes in relative double support time or swing time. These results are inconsistent with those of Browning and Kram (2007), who found a greater relative stance time and swing time in the obese group compared to normal-weight group. In addition, we observed no change in stride length. However, an increase in stride length related to weight loss has been reported previously, even at a fixed gait speed (Hortoba´gyi et al., 2011). We cannot find any single explanation for this inconsistency. The significant decrease we observed in hip flexion angle at initial contact is contrary to our initial hypothesis and also is inconsistent with the findings of Hortoba´gyi et al. (2011), who reported increased hip range of motion at a self-selected speed after weight loss. In our study, stride length did not change although after surgery the hip was less flexed at initial contact. This might be partly due to the fact that the knee was simultaneously less flexed and there may also be changes in pelvis rotation. We used fixed gait speeds to prevent speed affecting the gait parameters. If we had used a self-selected speed, the speed might well have increased following the weight loss, as shown earlier by Aaboe et al. (2011) and Hortoba´gyi et al. (2011). A higher speed would probably have increased the joint moments and thus
P. Vartiainen et al. / Journal of Biomechanics 45 (2012) 1769–1774
PEAK HIP EXTENSOR MOMENT
0
PEAK HIP FLEXOR MOMENT
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PEAK KNEE EXTENSOR MOMENT
PEAK KNEE FLEXOR MOMENT
200 0
−50
100
Speed: 1.2 m/s Nm
150 −100
100
50
−150
−50
−200 50 0
−250
−100
0 0 200
0
−50
100
Speed: 1.5 m/s Nm
150 −100
100
50
−150
−50
−200 50 0
−250 0
−100
Fig. 3. Individual changes in the absolute sagittal plane moment parameters at two gait speeds, 1.2 m/s (top) and 1.5 m/s (bottom). The left end of the line points to the value of the parameter at the baseline and the right end at the follow-up measurement. The thick dashed line represents the mean change and thick vertical lines show the standard deviations.
Table 4 Knee and hip joint absolute and normalized moments (means (SD)) at gait speeds 1.2 m/s and 1.5 m/s. Significant p-values in bold. Parameter
1.2 m/s Baseline
Peak knee abductor moment during early stance Absolute (N m) 70 (22) Normalized (N m/kg m) 0.32 (0.07) Peak knee abductor moment during late stance Absolute (N m) 64 (22) Normalized (N m/kg m) 0.29 (0.09) Peak knee extensor moment Absolute (N m) 44 (33) Normalized (N m/kg m) 0.19 (0.13) Peak knee flexor moment Absolute (N m) 50 (26) Normalized (N m/kg m) 0.24 (0.14) Peak hip extensor moment Absolute (N m) 119 (27) Normalized (N m/kg m) 0.57 (0.15) Peak hip flexor moment Absolute (N m) 93 (27) Normalized (N m/kg m) 0.43 (0.13) a
1.5 m/s a
Baseline
Follow-up
p-Value
0.016 0.791
71 (27) 0.32 (0.08)
62 (19) 0.36 (0.07)
0.043 0.007
54 (16) 0.31 (0.07)
0.016 0.204
61 (20) 0.28 (0.08)
53 (16) 0.30 (0.08)
0.092 0.110
33 (22) 0.18 (0.10)
0.204 0.970
53 (37) 0.23 (0.15)
44 (29) 0.25 (0.15)
0.424 0.733
39 (19) 0.23 (0.12)
0.043 0.424
61 (21) 0.29 (0.12)
43 (20) 0.26 (0.13)
0.003 0.339
89 (20) 0.54 (0.10)
o 0:001 1.000
162 (34) 0.76 (0.15)
123 (32) 0.75 (0.18)
0.016 1.000
86 (55) 0.48 (0.18)
0.233 0.791
105 (28) 0.48 (0.10)
100 (63) 0.55 (0.21)
0.424 0.622
Follow-up
p-Value
57 (19) 0.32 (0.07)
Wilcoxon signed-rank test.
counteracted the effects of the weight loss. We used slower (1.2 m/s) and faster (1.5 m/s) speeds, which are estimates of normal gait speed for healthy individuals (Bohannon and Andrews, 2011). We presumed
that the changes in gait parameters would have been clearer when subjects were performing a more demanding walking task, but no clear differences were observed.
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In our study, the nine participants were obese without musculoskeletal pathology in their lower extremities and four subjects had knee OA. Due to the small sample size and the fact that the knee OA subjects mainly suffered from mild radiographic disease with minor knee pain, we did not perform comparison between these two subgroups. In our knee OA subjects the knee pain was comparable to those of Hortoba´gyi et al. (2011) who had obese, but otherwise healthy adults in their study. It is not possible resolve which of the other possible confounding factors, i.e. subjective knee pain, gender or age had any direct effects on the measured parameters. We recognize some limitations in the study. First, the validity of marker-based motion analysis is limited by the difficulties in marker placement especially in obese subjects, who have thick layers of soft tissue on most anatomic landmarks. Second, during weight loss, the thickness of soft tissue may decrease, and thus it is impossible to achieve identical marker placements at the follow-up measurements as used at the baseline. Our modelbased method allows for variations in marker placement, as the marker locations in the model can be modified. However, it is challenging to determine the marker locations in the model so that they would precisely represent the sites of the bony structures of the lower limbs. Third, soft tissue and the spandex suit may cause movement artifacts. Finally, the joint angle values are error-prone, because we did not perform calibration measurements to determine zero angles for the knee and hip. The present study shows that hip and knee moments are reduced in proportion to the weight loss following extensive weight loss, and that step width is reduced. Larger, prospective studies are needed to evaluate, if these gait changes reduce emergence of new knee OA cases.
Conflict of interest statement The authors declare no conflict of interest.
Acknowledgments This study has been supported by the strategic funding of the University of Eastern Finland and by a grant (5960431) from Kuopio University Hospital. References Aaboe, J., Bliddal, H., Messier, S., Alkjar, T., Henriksen, M., 2011. Effects of an intensive weight loss program on knee joint loading in obese adults with knee osteoarthritis. Osteoarthritis and Cartilage 19 (7), 822–828.
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