Gait changes after weight loss on adolescent with severe obesity after sleeve gastrectomy

Surgery for Obesity and Related Diseases 15 (2019) 374–381

Original article

Gait changes after weight loss on adolescent with severe obesity after sleeve gastrectomy Susanna Summa a, Francesco De Peppo b, Maurizio Petrarca a,∗, Romina Caccamo b, Riccardo Carbonetti a, Enrico Castelli a, Domenico Ottavio Adorisio b a MARlab,

Department of Neuroscience, Neurorehabilitation Division, “Bambino Gesù” Children’s Hospital, Rome, Italy of Pediatric Surgery, Pediatric Surgery Unit, “Bambino Gesù” Children’s Hospital, Rome, Italy

b Department

Received 30 July 2018; received in revised form 10 December 2018; accepted 10 January 2019

Abstract

Background: It has been highlighted that obesity influences the gait reducing walking velocity, stride length, ankle dorsal flexion at initial contact and ankle power generation. Meanwhile, step width, double support, hip flexion, knee extension during stance, hip moment and ankle power absorption was described increased. A tendency to the normalization of these parameters occur when subjects reduced their weight during growth. Objective: We studied the effect of fast weight loss due to Sleeve Gastrectomy on gait pattern of adolescent with severe obesity. The aim is to assess the functional benefit of the surgery. Setting: Pediatric hospital, public health, Italy. Methods: 11 patients before and after 1 year from surgery and 10 controls participated to the study. We studied the gait with an optoelectronic system and two force plates. We evaluated both kinetics and kinematics of walking. Then we looked at the differences between the pre- vs post-surgery and with the control group. Results: Step length and velocity were lower and step width was bigger in adolescent with obesity. Kinematic and kinetic parameters were altered. After surgery we observed the reduction of several gait alteration. Meanwhile, after 1 year alterations at the level of the foot, the knee and the pelvis persist. Conclusion: The sudden loss of weight highlighted the presence of long-term effects on the locomotor system. The results discourage intense walking activities before the weight loss and we suggest further studies for evaluating the necessity of a rehabilitative intervention. (Surg Obes Relat Dis 2019;15:374–381.) © 2019 American Society for Bariatric Surgery. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license. (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Key words:

Adolescent; Sleeve Gastrectomy; Gait analysis; Gait evolution

Obesity is an increasing phenomenon in adolescent and preschool children [1]. This is consistent with numerous health-related co-morbid conditions in teenagers, mainly including dyslipidemia, sleep apnea, hypertension, and joint and back pain [2]. It was also demonstrated that ∗ Correspondence: Maurizio Petrarca, Ph.D., “Bambino Gesù” Children’s Hospital, Via torre di Palidoro s.n.c. 00050, Palidoro, Rome, Italy. E-mail address: [email protected] (M. Petrarca).

principally male adolescents between 18- and 19-years old with severe obesity [3] increase the relative risk of specific cardiovascular disease risk factors. Previous authors described musculoskeletal pain and disorders [4–6], due to obesity, as risk factors in the development of knee osteoarthritis [7–9]. Consequently, it was hypothesized that people with obesity use specific strategies, which tend to minimize joint moments, especially at hip and knee level during walking [10] and to reduce walking velocities al-

https://doi.org/10.1016/j.soard.2019.01.007 1550-7289/© 2019 American Society for Bariatric Surgery. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license. (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Susanna Summa, Francesco De Peppo and Maurizio Petrarca et al. / Surgery for Obesity and Related Diseases 15 (2019) 374–381

lowing the decrease of vertical loads. Furthermore, an increased stress at midfoot [11], the pediatric pes planus [12], and an increased stress at the heel at the second through fifth metatarsal were observed as well as the tendency to develop flat feet during life span [13]. Despite the above-reported alterations, gait is commonly encouraged [3,14,15]. Muscle contractile dysfunction were observed as a consequence of muscle structure modification and of altered recruitment patterns and contractile function [16]. Muscle structure differs both in myofiber size and architecture, in lipid accumulation and in fiber type. The consequences are an increased volitional fatigue and the decrease of the relative strength and power [16] that can be associated with a decrease of walking velocity, stride length, ankle dorsiflexion at initial contact, and ankle power generation [17]. It was also described an increase of the step width, the double support duration, the hip flexion, the knee extension during stance, the hip moment, and ankle power absorption [17,18]. A tendency to the normalization of these parameters occurs when patients reduced their weight [19]. Therefore, it is commonly accepted that obesity results in aberrant mechanics, which can potentially induce musculoskeletal injuries in adults [20]. Standing postural control is also affected as revealed by a greater displacement of the center of pressure [21]. It has been suggested that these alterations were related more to the increase in body fat percentage rather than in body mass index (BMI) [22]. A fast weight loss is an interesting circumstance to investigate the possible influence of obesity on gait maturation. The aim of this paper was to discuss, in a population of adolescent with severe obesity, the effect of surgical intervention (laparoscopic sleeve gastrectomy; LSG) on the gait pattern. LSG results in a sudden reduction of weight and fat mass [23] better maintained over time when associated with a nutritional program [24]. We want to test if the altered gait pattern, due to the obesity condition, recoveries toward the normal pattern after sudden weight loss. This observation could give indirect information about the long-term effects of obesity on the locomotor system. Further aims were to assess the functional benefit of the surgery and to enhance the understanding on the gait dynamics. Deepening the knowledge about these aspects will help us to better define an activity plan for teenagers with obesity.

375

and thigh restrained fat masses to avoid marker fluctuations. We asked the participants to walk barefoot at their self-selected speed along a 12-m walkway containing the force platforms at the midpoint. We modified the position of 2 markers of the PiG protocol, to reduce artifacts due to fat mass fluctuation at the baseline assessment before the surgery. They were positioned laterally on the iliac crest instead on the anterior superior iliac spine; meanwhile, we accurately measured the interasis distance and the anterior superior iliac spine–trocanter distance. The equivalence of the results was tested on 3 healthy patients applying the following 2 markers protocols: the standard PiG and the modified PiG. After surgery, the standard PiG protocol became applicable. Participants Eleven participants classified on the basis of BMI as patients at high risk (3 in Class II Obesity) and at very high risk (8 in Class III Obesity [25]; 2 females and 9 males; age 14.8 ± 1.3; weight presurgery 122.3 ± 20.0 kg; BMI presurgery 42.9 ± 5.0 kg/m2 ) and 10 teenagers with normal weight (7 female and 3 males; age 18.7 ± 4.9; weight 57.3 ± 11.5 kg; BMI 21.7 ± 2.0 kg/m2 ) participated in the study. The small differences in age between the participants are negligible during gait analysis comparison considering that the gait pattern is known to be stable from 11-years old to elderly, regarding spatiotemporal parameters, kinematics, and kinetics [26–28]. The control group was introduced as a benchmark of “normal gait” and considering the gait stability above mentioned a reassessment of “normal gait” was not conducted. Exclusion criteria were the presence of concomitant pathologies and specifically, diabetes, cardiovascular, neurologic, orthopedic, metabolic, or genetic diseases. We evaluated the group with obesity before (baseline) and 1 year after surgery. The study was conducted in accordance with the Helsinki Declaration on human rights and was approved by the Ethical Committee of the “Bambino Gesù” Children’s Hospital. All the participants and their parents signed an informed consent. Surgical procedure

Methods Experimental set-up We performed 3-dimensional gait analysis on 11 participants before and after SG. Data were collected with an optoelectronic system with 8 cameras (Vicon MX, Oxford, UK) at 200 Hz using the PlugInGait (PiG) protocol, and with 2 force plates (AMTI Or6-6, Watertown, MA, USA) at 1000 Hz. Nonelastic dressing on abdomen

LSG was performed using a 5-trocar laparoscopic technique. The great curvature of the stomach is freed from the omentum attachment starting approximately 6 to 7 cm from the pylorus until the cardias. The stomach is then resected longitudinally starting 6 to 7 cm from the pylorus, to avoid the dumping syndrome, until the gastroesophageal junction, under the guidance of a 40-Fr boogie. The transected gastric specimen is retrieved via a port site. This port site is then closed with an absorbable mul-

376

Susanna Summa, Francesco De Peppo and Maurizio Petrarca et al. / Surgery for Obesity and Related Diseases 15 (2019) 374–381

tifilament suture. A drainage tube is placed into the abdominal cavity. Surgical procedures were performed by the same surgeon in the operating setting of our hospital. The participants had, in the postoperative period, a balanced diet of 1100 to 1500 Kcal with a protein intake of 25 to 30 g/serving. Furthermore, in the postoperative period, all patients started with a program of physical exercises, at least 30 minutes 3 times a week, depending on their attitude, without specific gait training. Data analysis We looked at the joint rotation of the following body parts: upper limbs, lower limbs, the foot progression angle, which is the angle of the foot with respect to the direction of progression, and at the pelvis orientation. In addition, we computed spatiotemporal and kinetic gait parameters. Kinetic data were normalized for individual weight. We also normalized the time series as a percentage of the gait cycle (0–100). For each participant, we extracted 3 representative gait cycles. We identified and calculated some parameters (range of motion [RoM] and peaks values of angle joint, moments, and powers). Statistical analysis Because of the reduced number of participants in each group, we applied the Shapiro–Wilk test for studying the normality distribution of the data. As a consequence of the unequal variances among patients and controls, we computed a Welch t test statistic. When the Shapiro–Wilk test failed, we computed the Mann-Whitney U test. We looked at the surgery effect comparing pre- and postsurgery parameters. We used paired sample t test and when data violated the normality assumption, we used Wilcoxon signed-rank test. We investigated the effect size following Cohen guidelines [27,29] and Volker suggestions [28,30]. Effect size (d) is considered to be “no effect” for d < .20, “small” for .20 < d < .50, ‘‘moderate” for .50 < d < .80, and “large” for d > .80. For the indicators that exhibited a significant variation, we additionally looked at their correlations with the weight loss and BMI variation between pre- and postsurgery. P values was set at .05. Results After the surgery the patients decreased weight and BMI. One year after the surgery the averaged weight of the patients was 81.5 ± 13.9 kg and the averaged BMI was 28.7 ± 4.6 kg/m2 . Therefore, the averaged total weight loss was 40.8 ± 15 kg, the averaged percent change in

BMI was 32.7 ± 9.9%, and averaged percentage of excess of weight loss was 81.07 ± 28. Spatiotemporal parameters The presurgery group statistically differed from control group in step width, step length, double support, and percent stance. We found a reduction in the step width and a moderate increase of the step length after the surgery. The stance duration improved as well, and the swing time increased after the surgery. No significant differences arose between controls and the patients 1 year after the surgery. All the spatiotemporal parameters results are summarized in Table 1. Kinematics All the kinematic results are summarized in Table 1. Pre versus control Looking at the upper body, we observed increased head obliquity and rotation RoM (Fig. 1A), increased shoulder mean abduction and mean external rotation (Fig. 1B), increased elbow mean flexion (Fig. 1C), and increased RoM of the pelvis tilt but with a decrease of the pelvis obliquity RoM (Fig. 1D). Looking at the lower body, we observed reduced hip flexion/extension RoM (Fig. 1E), increased percentage of the peak of maximal hip extension (Fig. 1E), reduced knee flexion/extension mean and RoM with increased extension at Initial Contact (IC) with a reduced maximal flexion in stance and swing (Fig. 1F), increased knee extension in stance (Fig. 1F), reduced ankle flexion/extension RoM and dorsiflexion at IC (Fig. 1G), a reduction of the maximum plantar flexion (Fig. 1G), and a decreased foot progression angle in the external rotation of the foot (Fig. 1H). Post versus control After weight reduction, some parameters did not regain values comparable with the control group. After surgery the head obliquity and rotation RoM was reduced (Fig. 1A) but it was still bigger with respect to the control group. We observed the same behavior for the mean abduction and mean external rotation of the shoulder (Fig. 1B) and the increased elbow mean flexion (Fig. 1C). Looking at differences before versus after surgery, we also observed for the lower body, the increased RoM of the pelvis tilt and the decreased pelvis obliquity RoM (Fig. 1D), the increased knee mean and RoM flexion/extension with the decreased extension at IC and the reduced maximal flexion in stance and swing with the increased extension in stance (Fig. 1F),

Table 1 Spatiotemporal kinematic and kinetic parameters. Pre

Post

Control

Pre versus control P

Pre versus control (effect size)

Pre versus Post P

Pre versus post (effect size)

Post versus control P

Post versus control (effect size)

Corr. Delta Weight P

%Stance Step width Step length Double support Head obliquity RoM Head rotation RoM Shoulder mean abduction Shoulder mean external rotation Elbow mean flexion Pelvis tilt RoM Pelvis obliquity RoM Hip flexion/extension RoM %Max hip extension Knee flexion/extension mean Knee flexion/extension RoM Knee IC extension Knee max flexion in stance Knee max flexion in swing Knee max extension in stance Ankle flexion/extension RoM Ankle IC dorsiflexion Ankle max plantar flexion FPA mean Hip max extension moment Hip max flexion moment Hip max abduction moment Hip negative work Knee max extension moment Knee max flexion moment Knee positive work Ankle max plantarflexion moment Ankle max dorsiflexion moment Ankle positive work

63 (1.47) .27 (.03) .58 (.05) .15 (.03) 8.21 (4.37) 9.86 (3.29) 29.63 (5.38) 31.14 (8.24)

61 (1.73) .19 (.02) .61 (.05) .13 (.03) 6.58 (2.49) 7.43 (2.71) 17.48 (5.35) 18.37 (11.16)

60 (1.29) .18 (.02) .62 (.03) .12 (.02) 3.38 (1.03) 5.57 (2.41) 8.78 (3.49) −3.21 (12.41)

.015 .001 ns .03 .001 .006 .0001 .0001

1.40 2.48 −1.02 1.01 1.50 1.56 4.59 3.27

.005 .001 .018 ns ns ns .001 .005

−.88 −2.45 .63 −.40 −.45 −.86 −2.26 −1.30

ns ns ns ns .002 ns .002 .003

.35 .20 −.24 .50 1.68 .73 1.92 1.83

ns ns ns ns ns ns ns ns

ns ns ns .039 ns ns ns ns

46.21 (5.70) 5.45 (1.53) 6.31 (.91) 40.56 (4.21) 55.77 (1.01) 12.21 (3.99) 51.67 (4.23) −.08 (4.13) 8.42 (4.80) 47.82 (4.64) −2.56 (4.16)

39.12 (4.41) 4.45 (1.64) 7.39 (2.94) 43.90 (4.14) 53.32 (1.34) 15.89 (3.91) 56.17 (3.84) 3.78 (4.22) 10.41 (6.39) 54.59 (5.13) −1.21 (3.25)

34.99 (3.75) 3.19 (.91) 10.93 (2.49) 45.03 (4.10) 52.14 (1.33) 21.99 (3.61) 61.09 (3.99) 7.86 (4.40) 16.26 (4.93) 64.26 (4.36) 3.60 (3.40)

.0003 .002 .0002 .03 .0002 .0002 .0006 .002 .005 .0001 .003

2.33 1.83 −2.53 −1.06 3.06 −2.56 −2.32 −1.86 −1.60 −3.65 −1.61

.001 ns ns .009 .003 .014 .002 ns ns .002 ns

−1.39 −.55 .59 .80 −2.04 .92 1.14 .92 .35 1.38 .34

.037 .043 .007 ns ns .005 .010 .045 .027 .002 .007

1.01 .95 −1.30 −.27 .89 −1.62 −1.26 −0.94 −1.03 −2.03 −1.45

.028 .038 ns ns ns .048 ns ns ns .027 ns

.022 ns ns ns ns ns ns ns ns .023 ns

26.91 (4.31)

28.37 (4.34)

33.01 (5.29)

.015

−1.27

ns

.34

.045

−.96

ns

ns

−2.92 (3.03) −14.62 (5.11) −16.85 (6.41) −.53 (.26) .75 (.37) 1.10 (.38) .08 (.05) −.47 (.22) .22 (.12) .11 (.05) −.12 (.09)

−2.21 (2.74) −16.20 (5.11) −12.78 (5.14) −.72 (.22) .52 (.28) .90 (.19) .12 (.07) −.35 (.15) .27 (.15) .06 (.04) −.14 (.04)

−.10 (4.40) −20.03 (6.30) 7.27 (2.91) −.72 (.09) .39 (.13) .76 (.14) .06 (.03) −.27 (.14) .37 (.18) .05 (.02) .13 (.05)

.044 .04 .002 .0006 .001 ns .027 .038 .036 .012 ns

−.76 .94 −1.86 .95 1.31 1.19 .47 −1.07 −1.01 1.61 .10

ns ns .007 ns ns .041 ns ns ns .018 ns

.27 −.31 .67 −.77 −.71 −.67 .73 .64 .38 −1.06 −.31

ns ns .02 ns ns ns .02 ns ns ns ns

−.57 .67 −1.32 .01 .62 .84 1.20 .52 .62 .38 .30

ns ns ns ns ns ns ns ns ns ns ns

ns ns .046 ns ns ns ns ns ns ns ns

1.24 (.14)

1.41 (.18)

1.47 (.18)

.008

−1.39

.009

1.06

ns

.32

ns

ns

.21 (.03)

.25 (.05)

.28 (.05)

.005

−1.51

.018

.95

ns

.57

ns

ns

Corr = correlation; BMI = body mass index; ns = not significant; RoM = range of motion; IC = Initial Contact; max = maximum; FPA = foot progression angle. Values are averaged (standard deviation) per group. ∗ : p-value < 0,05.

Corr. Delta BMI P

Susanna Summa, Francesco De Peppo and Maurizio Petrarca et al. / Surgery for Obesity and Related Diseases 15 (2019) 374–381

Gait parameters

377

378

Susanna Summa, Francesco De Peppo and Maurizio Petrarca et al. / Surgery for Obesity and Related Diseases 15 (2019) 374–381

Fig. 1. Left panel upper body. (A) Head angle on the frontal (left) and the transversal (right) plane. (B) Shoulder angle on the frontal (left) and the transversal (right) plane. (C) Elbow angle on the sagittal plane. (D) Pelvis angle on the sagittal (left) and the frontal (right) plane. Right panel lower body. (E) Hip angle on the sagittal plane. (F) Knee angle on the sagittal plane. (G) Ankle angle on the sagittal plane. (H) Foot progression angle on the transversal plane. Solid lines denote averaged group value. Dashed areas denote the standard error. Black, red, and green colors stand, respectively, for teenagers with normal weight, the group with obesity before (baseline), and the group 1 year after surgery.

the increased ankle RoM (Fig. 1G), and the decrease foot progression angle in the external direction of the foot (Fig. 1H). However, all these parameters maintained a significant difference compared with the control group. Kinetics All the kinetic results are summarized in Table 1. Pre versus control The participants with obesity showed an increased hip flexor moment during load response and a decreased extensor moment (Fig. 2A), an increased hip adductor moment (Fig. 2B), a decreased knee flexor moment during load response, an increased knee extensor moment during the support phase (Fig. 2C), and a decreased ankle dorsal moment in stance (Fig. 2D). When we analyzed powers,

we found an increase of the hip negative work (Fig. 2E), an increase of knee positive work (Fig. 2F), and a reduced ankle positive work (Fig. 2G).

Post versus control After surgery, all the moments at hip, knee, and ankle level regained values close to that of the control group. Only the hip negative work showed increased values with respect to the control group after surgery (Fig. 2E).

Correlation analysis The correlation between the significant variables and the weight and BMI variation was significant for the following: double support duration, elbow flexion, pelvis tilt RoM, knee flexion extension mean value, knee maximum

Susanna Summa, Francesco De Peppo and Maurizio Petrarca et al. / Surgery for Obesity and Related Diseases 15 (2019) 374–381

379

Fig. 2. Left panel joints moment. (A) Hip joint moment on the sagittal plane. (B) Hip joint moment on the frontal plane. (C) Knee joint moment on the sagittal plane. (D) Ankle joint moment on the sagittal plane. Right panel joints power. (E) Hip joint power. (F) Knee joint power. (G) Ankle joint power. Solid lines denote averaged group value. Dashed areas denote the standard error. Black, red, and green colors stand respectively for teenagers with normal weight, the group with obesity before (baseline), and the group 1 year after surgery.

flexion in swing, and mean angle of the foot progression. Discussion In this paper we analyzed the gait of adolescent with obesity before and after LSG. Differences between presurgery and standard gait As reported in literature, teenagers with obesity suffer from gait alteration [17,18] mainly correlated with the decrease of walking velocity. Conversely, our study highlights no previously described gait alterations: a decreased ankle power generation during late stance, increased knee power generation and positive work during stance, increased hip powers during stance, decreased power generation in swing and increased negative work, an increased external rotation of the foot progression angle, an increased RoM of the pelvic tilt, an increased RoM of the pelvic rotation, and a decreased RoM of the pelvic obliquity. The differences with the literature could be explained by the severity of obesity, and by the fact that we resolved the full body model. All the kinetic and kinematic alterations can be explained by the increased mass and volumes and the augmented step width by the enlarged volume of the thighs. The increased external rotation of the foot can be due to the bigger displacement of the center of pressure [21].

The reduction of the ankle dorsiflexion at initial contact and power generation can be related to the reduced velocity, which is a reduction of the dynamic component with reduced ankle power generation in late stance. Reduced knee flexion and reduced hip extension during stance favor the reduction of moments and load forces on these articulations [8,9]. The pelvis, which represent the junction and a frame of reference between upper and lower body coordination [29,31] increases the RoM, affecting the increased head mobility. The forward bending of the head could be supported by the following 2 different hypotheses: the unbalance, that is, the participants look at the path where they are moving to, and the depression [30–33]. It is known that the depression elicits slow gaits [32–35] similarly to our results. Looking at the upper limb our results showed an increased flexion of the elbow: this behavior can be ascribed to the unbalance, with the upper limb raising to minimize the moment in torsion of the upper body. Differences between pre- and postsurgery After surgery, gait parameters tend to normalize as observed in literature [16], but with some exceptions previously unreported. A reduction of the external rotation of the foot progression angle, the increase of the maximum plantar flexion of the ankle during the swing, the increase of both RoM and extension of the knee during stance, and

380

Susanna Summa, Francesco De Peppo and Maurizio Petrarca et al. / Surgery for Obesity and Related Diseases 15 (2019) 374–381

the decrease of the RoM of the pelvis tilt and obliquity persist. The residual increase of the foot progression angle influences the reduced ankle plantar flexion, the residual reduction of ankle RoM, and the kinetics at the end of the support phase that influence also the knee. The action of the foot lever in inducing knee passive flexion in initial swing is reduced by the increase of the foot progression angle. Furthermore, the increased mass of the lower limb before surgery partially breaks the rising of the shank and necessitate of the increase of knee power generation. After surgery, this knee power generation was not observed while a relative external rotation of the foot remains with the consequent reduction of knee flexion in swing. Summarizing, we observed clear gait alterations concomitant with the obese condition, which are reported to be associated with back and joint pain that can lead to knee osteoarthritis over time. In that perspective, it is difficult to distinguish between the mere effect of the increased load from the effect of kinetic and kinematic alterations on the gait function. It seems that there is a mutual interaction that has a different solution for each subject. The fact that the reduction of the weight provides only a partial restoration of the gait pattern reinforces this interpretation. Consequently, the residual increase of pelvic, foot, and knee mobility after weight loss can be considered residual risk factors over time for pain and osteoarthritis occurrence. The main strengths of the present work were represented by the fact that we conducted a full body gait assessment on a cohort of homogeneous teenagers with severe obesity without co-morbid conditions that can alter the gait. The main limitations were that we studied a small cohort size and we did not measure the contribution of the lean mass modification. As minor limitations, we did not reassess the control group and there is a little mean age difference between controls and participants with obesity. Conclusions We explored the functional benefit of LSG on teenagers with severe obesity and we conducted a deep analysis aiming at understanding gait dynamic characteristics and changes. The sudden loss of weight highlighted the presence of long-term effects on the locomotor system. Both intense walking activities before the weight loss and a specific rehabilitative intervention for restoring dynamic gait components should be evaluated after a patient specific assessment; during which a patient-centered evaluation of load effects on joints and gait pattern alteration is conducted. Author contributions O.D.A., F.D.P., M.P., and R. Caccamo conceived the study. S.S. and M.P. reviewed the literature. R. Carbonetti

and M.P. collected gait data. S.S., R. Carbonetti, and M.P. analyzed the data. All authors interpreted the data and wrote the manuscript. All authors read and approved the final manuscript. Funding This study was partially supported by Pegaso Onlus (Grant numbers: opbg-201603x003858) and by the Italian Ministry of Health within the Research program Ricerca Finalizzata (Grant numbers: CO-2011-02351627). Disclosures The authors have no commercial associations that might be a conflict of interest in relation to this article. Supplementary material Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.soard. 2019.01.007. References [1] de Onis M, Blössner M, Borghi E. Global prevalence and trends of overweight and obesity among preschool children. Am J Clin Nutr 2010;92(5):1257–64. [2] Inge TH, Zeller MH, Jenkins TM, et al. Perioperative outcomes of adolescents undergoing bariatric surgery: the Teen-Longitudinal Assessment of Bariatric Surgery (Teen-LABS) study. JAMA Pediatr 2014;168(1):47–53. [3] Michalsky MP, Inge TH, Simmons M, et al. Cardiovascular risk factors in severely obese adolescents: the Teen Longitudinal Assessment of Bariatric Surgery (Teen-LABS) Study. JAMA Pediatr 2015;169(5):438–44. [4] Shultz SP, Anner J, Hills AP. Pediatric obesity, physical activity and the musculoskeletal system. Obes Rev 2009;10(5):576–82. [5] Wearing SC, HennigEM Byrne NM, Steele JR, Hills AP. Musculoskeletal disorders associated with obesity: a biomechanical perspective. Obes Rev 2006;7(3):239–50. [6] Bout-Tabaku S, Michalsky MP, Jenkins TM, et al. Musculoskeletal pain, self-reported physical function, and quality of life in the Teen–Longitudinal Assessment of Bariatric Surgery (Teen-LABS) Cohort. JAMA Pediatr 2015;169(6):552–9. [7] Runhaar J, Koes BW, Clockaerts S, Bierma-Zeinstra SMA. A systematic review on changed biomechanics of lower extremities in obese individuals: a possible role in development of osteoarthritis. Obes Rev 2011;12(12):1071–82. [8] Amiri P, Hubley-Kozey CL, Landry SC, Stanish WD, Wilson JLA. Obesity is associated with prolonged activity of the quadriceps and gastrocnemii during gait. J Electromyogr Kinesiol 2015; 25(6):951–8. [9] Pamukoff DN, Lewek MD, Blackburn JT. Greater vertical loading rate in obese compared to normal weight young adults. Clin Biomech 2016;33:61–5. [10] McMillan AG, Pulver AME, Collier DN, Williams DSB. Sagittal and frontal plane joint mechanics throughout the stance phase of walking in adolescents who are obese. Gait Posture 2010; 32(2):263–8. [11] Mickle KJ, Steele JR, Munro BJ. Does excess mass affect plantar pressure in young children? Int J Pediatr Obes 2006;1(3):183–8.

Susanna Summa, Francesco De Peppo and Maurizio Petrarca et al. / Surgery for Obesity and Related Diseases 15 (2019) 374–381 [12] Mahaffey R, Morrison SC, Bassett P, Drechsler WI, Cramp MC. The impact of body fat on 3 dimensional motion of the pediatric foot during walking. Gait Posture 2016;44:155–60. [13] Mueller S, Carlsohn A, Mueller J, Baur H, Mayer F. Influence of obesity on foot loading characteristics in gait for children aged 1 to 12 years. PLoS One 2016;11(2):e0149924. [14] Shultz SP, Sitler MR, Tierney RT, Hillstrom HJ, Song J. Effects of pediatric obesity on joint kinematics and kinetics during 2 walking cadences. Arch Phys Med Rehabil 2009;90(12):2146–54. [15] Shultz SP, Browning RC, Schutz Y, Maffeis C, Hills AP. Childhood obesity and walking: guidelines and challenges. Int J Pediatr Obes 2011;6(5-6):332–41. [16] Bollinger LM. Potential contributions of skeletal muscle contractile dysfunction to altered biomechanics in obesity. Gait Posture 2017;56:100–7. [17] Cimolin V, Galli M, Vismara L, Albertini G, Sartorio A, Capodaglio P. Gait pattern in lean and obese adolescents. Int J Rehabil Res 2015;38(1):40–8. [18] Hills AP, Parker AW. Gait characteristics of obese children. Arch Phys Med Rehabil 1991;72(6):403–7. [19] Cimolin V, Vismara L, Galli M, Grugni G, Cau N, Capodaglio P. Gait strategy in genetically obese patients: a 7-year follow up. Res Dev Disabil 2014;35(7):1501–6. [20] Wearing SC, Hennig EM, Byrne NM, Steele JR, Hills AP. The biomechanics of restricted movement in adult obesity. Obes Rev 2006;7(1):13–24. [21] Villarrasa-Sapiña I, García-Massó X, Serra-Añó P, Garcia-Lucerga C, Gonzalez LM, Lurbe E. Differences in intermittent postural control between normal-weight and obese children. Gait Posture 2016;49:1–6. [22] Meng H, O’Connor DP, Lee BC, Charles S, Layne CS, Gorniak SL. Effects of adiposity on postural control and cognition. Gait Posture 2016;43:31–7. [23] Noel P, Nedelcu M, Eddbali I, Manos T, Gagner M. Long term results (8 years) after sleeve gastrectomy? Surg Obes Relat Dis 2017;13(7):1115–16.

381

[24] Caron M, Hould FS, Lescelleur O, et al. Long-term nutritional impact of sleeve gastrectomy. Surg Obes Relat Dis 2017; 13(10):1664–73. [25] NIH classification of overweight and obesity, US [https://www. nhlbi.nih.gov/]. Bethesda: National Institutes of Health; cyr [updated 2019/01/29; cited 2018/02/08]. Available from: https://www.nhlbi. nih.gov/ health/ educational/ lose_wt/ BMI/ bmi_dis.htm. [26] Sutherland DH, Olshen R, Cooper L, Woo SL. The development of mature gait. J Bone Joint Surg Am 1980;62(3):336–53. [27] Wu Y 1, Zhong Z, Lu M, He J. Statistical analysis of gait maturation in children based on probability density functions. In: Conf Proc IEEE Eng Med Biol Soc; 2011. p. 1652–5. [28] Kraan CM, Tan AHJ, Cornish KM. The developmental dynamics of gait maturation with a focus on spatiotemporal measures. Gait Posture 2017;51:208–17. [29] Cohen J. Statistical power analysis for the behavioral sciences. Newbury Park: Sage; 1988. p. 8–17. [30] Volker MA. Reporting effect size estimates in school psychology research. Psychol Schools 2006;43(6):653–72. [31] Amori V, Petrarca M, Patané F, Castelli E, Cappa P. Upper body balance control strategy during continuous 3D postural perturbation in young adults. Gait Posture 2015;41:19–25. [32] Luppino FS, de Wit LM, Bouvy PF, et al. Overweight, obesity, and depression. A Systematic review and meta-analysis of longitudinal studies. Arch Gen Psychiatry 2010;67(3):220–9. [33] Nemiary D, Shim R, Mattox G, Holden K. The relationship between obesity and depression among adolescents. Psychiatr Ann 2012;42(8):305–8. [34] Barliya A, Omlor L, Giese MA, Berthoz A, Flash T. Expression of emotion in the kinematics of locomotion. Exp Brain Res 2013;225(2):159–76. [35] Brandler TC, Wang C, Oh-Park M, Holtzer R, Verghese J. Depressive symptoms and gait dysfunction in the elderly. Am J Geriatr Psychiatry 2012;20(5):425–32.