Changes in Functional Mobility and Musculoskeletal Pain After Bariatric Surgery in Teens With Severe Obesity: Teen–Longitudinal Assessment of Bariatric Surgery (LABS) Study | Adolescent Medicine | JAMA Pediatrics | JAMA Network
[Skip to Navigation]
Sign In
Figure 1.  Changes in Time to Completion for the 400-m Walk Test and Resting Heart Rate Prior to Testing From Baseline to 6 Months, 12 Months, and 24 Months
Changes in Time to Completion for the 400-m Walk Test and Resting Heart Rate Prior to Testing From Baseline to 6 Months, 12 Months, and 24 Months

Data are adjusted for age, sex, race/ethnicity, baseline body mass index, and surgical center. The error bars represent 95% CIs. bpm indicates beats per minute.

aP < .01 from baseline.

Figure 2.  Changes in Posttest Heart Rate, Heart Rate Difference, and 2-Minute Heart Rate Recovery From Baseline to 6 Months, 12 Months, and 24 Months
Changes in Posttest Heart Rate, Heart Rate Difference, and 2-Minute Heart Rate Recovery From Baseline to 6 Months, 12 Months, and 24 Months

Data are adjusted for age, sex, race/ethnicity, baseline body mass index, surgical center, and change in time to completion. The 2-minute heart rate recovery is calculated by posttest heart rate minus 2-minute postcompletion heart rate. The error bars represent 95% CIs. bpm indicates beats per minute.

aP < .01 from baseline.

bP = .01 from 6 months.

Figure 3.  Patients With and Without Musculoskeletal Pain Concerns During or After the 400-m Walk Test at Baseline (Preoperative) and 6-Month, 12-Month, and 24-Month Follow-up
Patients With and Without Musculoskeletal Pain Concerns During or After the 400-m Walk Test at Baseline (Preoperative) and 6-Month, 12-Month, and 24-Month Follow-up

Relative risk (RR) of having musculoskeletal pain concerns from baseline, with 95% CIs listed below. The P values indicate the difference from baseline.

Table.  Preoperative (Baseline) Demographic, Anthropometric, and Surgical Type for the Teen-LABS Cohort (N = 206)
Preoperative (Baseline) Demographic, Anthropometric, and Surgical Type for the Teen-LABS Cohort (N = 206)
1.
Gidding  SS, Nehgme  R, Heise  C, Muscar  C, Linton  A, Hassink  S.  Severe obesity associated with cardiovascular deconditioning, high prevalence of cardiovascular risk factors, diabetes mellitus/hyperinsulinemia, and respiratory compromise.  J Pediatr. 2004;144(6):766-769.PubMedGoogle ScholarCrossref
2.
Stovitz  SD, Pardee  PE, Vazquez  G, Duval  S, Schwimmer  JB.  Musculoskeletal pain in obese children and adolescents.  Acta Paediatr. 2008;97(4):489-493.PubMedGoogle ScholarCrossref
3.
Taylor  ED, Theim  KR, Mirch  MC,  et al.  Orthopedic complications of overweight in children and adolescents.  Pediatrics. 2006;117(6):2167-2174.PubMedGoogle ScholarCrossref
4.
Krul  M, van der Wouden  JC, Schellevis  FG, van Suijlekom-Smit  LWA, Koes  BW.  Musculoskeletal problems in overweight and obese children.  Ann Fam Med. 2009;7(4):352-356.PubMedGoogle ScholarCrossref
5.
Wearing  SC, Hennig  EM, Byrne  NM, Steele  JR, Hills  AP.  The impact of childhood obesity on musculoskeletal form.  Obes Rev. 2006;7(2):209-218.PubMedGoogle ScholarCrossref
6.
Kelly  AS, Barlow  SE, Rao  G,  et al; American Heart Association Atherosclerosis, Hypertension, and Obesity in the Young Committee of the Council on Cardiovascular Disease in the Young, Council on Nutrition, Physical Activity and Metabolism, and Council on Clinical Cardiology.  Severe obesity in children and adolescents: identification, associated health risks, and treatment approaches: a scientific statement from the American Heart Association.  Circulation. 2013;128(15):1689-1712.PubMedGoogle ScholarCrossref
7.
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):552-559.PubMedGoogle ScholarCrossref
8.
Forhan  M, Gill  SV.  Obesity, functional mobility and quality of life.  Best Pract Res Clin Endocrinol Metab. 2013;27(2):129-137.PubMedGoogle ScholarCrossref
9.
Okifuji  A, Hare  BD.  The association between chronic pain and obesity.  J Pain Res. 2015;8:399-408.PubMedGoogle ScholarCrossref
10.
Vestergaard  S, Patel  KV, Bandinelli  S, Ferrucci  L, Guralnik  JM.  Characteristics of 400-meter walk test performance and subsequent mortality in older adults.  Rejuvenation Res. 2009;12(3):177-184.PubMedGoogle ScholarCrossref
11.
Newman  AB, Simonsick  EM, Naydeck  BL,  et al.  Association of long-distance corridor walk performance with mortality, cardiovascular disease, mobility limitation, and disability.  JAMA. 2006;295(17):2018-2026.PubMedGoogle ScholarCrossref
12.
Correia de Faria Santarém  G, de Cleva  R, Santo  MA,  et al.  Correlation between body composition and walking capacity in severe obesity.  PLoS One. 2015;10(6):e0130268.PubMedGoogle ScholarCrossref
13.
Hergenroeder  AL, Brach  JS, Otto  AD, Sparto  PJ, Jakicic  JM.  The influence of body mass index on self-report and performance-based measures of physical function in adult women.  Cardiopulm Phys Ther J. 2011;22(3):11-20.PubMedGoogle Scholar
14.
King  WC, Engel  SG, Elder  KA,  et al.  Walking capacity of bariatric surgery candidates.  Surg Obes Relat Dis. 2012;8(1):48-59.PubMedGoogle ScholarCrossref
15.
Tsiros  MD, Coates  AM, Howe  PR, Grimshaw  PN, Buckley  JD.  Obesity: the new childhood disability?  Obes Rev. 2011;12(1):26-36.PubMedGoogle ScholarCrossref
16.
Norman  A-C, Drinkard  B, McDuffie  JR, Ghorbani  S, Yanoff  LB, Yanovski  JA.  Influence of excess adiposity on exercise fitness and performance in overweight children and adolescents.  Pediatrics. 2005;115(6):e690-e696.PubMedGoogle ScholarCrossref
17.
Shultz  SP, Anner  J, Hills  AP.  Paediatric obesity, physical activity and the musculoskeletal system.  Obes Rev. 2009;10(5):576-582.PubMedGoogle ScholarCrossref
18.
Knöpfli  BH, Radtke  T, Lehmann  M,  et al.  Effects of a multidisciplinary inpatient intervention on body composition, aerobic fitness, and quality of life in severely obese girls and boys.  J Adolesc Health. 2008;42(2):119-127.PubMedGoogle ScholarCrossref
19.
Mendelson  M, Michallet  AS, Perrin  C, Levy  P, Wuyam  B, Flore  P.  Exercise training improves breathing strategy and performance during the six-minute walk test in obese adolescents.  Respir Physiol Neurobiol. 2014;200:18-24.PubMedGoogle ScholarCrossref
20.
Danielsson  P, Kowalski  J, Ekblom  Ö, Marcus  C.  Response of severely obese children and adolescents to behavioral treatment.  Arch Pediatr Adolesc Med. 2012;166(12):1103-1108.PubMedGoogle ScholarCrossref
21.
Knop  C, Singer  V, Uysal  Y, Schaefer  A, Wolters  B, Reinehr  T.  Extremely obese children respond better than extremely obese adolescents to lifestyle interventions.  Pediatr Obes. 2015;10(1):7-14.PubMedGoogle ScholarCrossref
22.
Serés  L, Lopez-Ayerbe  J, Coll  R,  et al.  Increased exercise capacity after surgically induced weight loss in morbid obesity.  Obesity (Silver Spring). 2006;14(2):273-279.PubMedGoogle ScholarCrossref
23.
de Souza  SA, Faintuch  J, Sant’anna  AF.  Effect of weight loss on aerobic capacity in patients with severe obesity before and after bariatric surgery.  Obes Surg. 2010;20(7):871-875.PubMedGoogle ScholarCrossref
24.
da Silva  RP, Martinez  D, Faria  CC,  et al.  Improvement of exercise capacity and peripheral metaboreflex after bariatric surgery.  Obes Surg. 2013;23(11):1835-1841.PubMedGoogle ScholarCrossref
25.
Wilms  B, Ernst  B, Thurnheer  M, Weisser  B, Schultes  B.  Differential changes in exercise performance after massive weight loss induced by bariatric surgery.  Obes Surg. 2013;23(3):365-371.PubMedGoogle ScholarCrossref
26.
de Souza  SA, Faintuch  J, Fabris  SM,  et al.  Six-minute walk test: functional capacity of severely obese before and after bariatric surgery.  Surg Obes Relat Dis. 2009;5(5):540-543.PubMedGoogle ScholarCrossref
27.
Inge  TH, Courcoulas  AP, Jenkins  TM,  et al; Teen-LABS Consortium.  Weight loss and health status 3 years after bariatric surgery in adolescents.  N Engl J Med. 2016;374(2):113-123.PubMedGoogle ScholarCrossref
28.
Jeffreys  RM, Inge  TH, Jenkins  TM,  et al.  Physical activity monitoring in extremely obese adolescents from the Teen-LABORATORIES Study.  J Phys Act Health. 2015;12(1):132-138.PubMedGoogle ScholarCrossref
29.
Maniscalco  M, Zedda  A, Giardiello  C,  et al.  Effect of bariatric surgery on the six-minute walk test in severe uncomplicated obesity.  Obes Surg. 2006;16(7):836-841.PubMedGoogle ScholarCrossref
30.
Owan  T, Avelar  E, Morley  K,  et al.  Favorable changes in cardiac geometry and function following gastric bypass surgery: 2-year follow-up in the Utah obesity study.  J Am Coll Cardiol. 2011;57(6):732-739.PubMedGoogle ScholarCrossref
31.
Jhaveri  RR, Pond  KK, Hauser  TH,  et al.  Cardiac remodeling after substantial weight loss: a prospective cardiac magnetic resonance study after bariatric surgery.  Surg Obes Relat Dis. 2009;5(6):648-652.PubMedGoogle ScholarCrossref
32.
Michalsky  MP, Raman  SV, Teich  S, Schuster  DP, Bauer  JA.  Cardiovascular recovery following bariatric surgery in extremely obese adolescents: preliminary results using cardiac magnetic resonance (CMR) imaging.  J Pediatr Surg. 2013;48(1):170-177.PubMedGoogle ScholarCrossref
33.
Ippisch  HM, Inge  TH, Daniels  SR,  et al.  Reversibility of cardiac abnormalities in morbidly obese adolescents.  J Am Coll Cardiol. 2008;51(14):1342-1348.PubMedGoogle ScholarCrossref
34.
Vázquez  LA, Pazos  F, Berrazueta  JR,  et al.  Effects of changes in body weight and insulin resistance on inflammation and endothelial function in morbid obesity after bariatric surgery.  J Clin Endocrinol Metab. 2005;90(1):316-322.PubMedGoogle ScholarCrossref
35.
Gokce  N, Vita  JA, McDonnell  M,  et al.  Effect of medical and surgical weight loss on endothelial vasomotor function in obese patients.  Am J Cardiol. 2005;95(2):266-268.PubMedGoogle ScholarCrossref
36.
Shultz  SP, Anner  J, Hills  AP.  Paediatric obesity, physical activity and the musculoskeletal system.  Obes Rev. 2009;10(5):576-582.PubMedGoogle ScholarCrossref
37.
Shaibi  GQ, Ryder  JR, Kim  JY, Barraza  E.  Exercise for obese youth: refocusing attention from weight loss to health gains.  Exerc Sport Sci Rev. 2015;43(1):41-47.PubMedGoogle ScholarCrossref
38.
Saibene  F, Minetti  AE.  Biomechanical and physiological aspects of legged locomotion in humans.  Eur J Appl Physiol. 2003;88(4-5):297-316.PubMedGoogle ScholarCrossref
39.
Legault  ÉP, Cantin  V, Descarreaux  M.  Assessment of musculoskeletal symptoms and their impacts in the adolescent population: adaptation and validation of a questionnaire.  BMC Pediatr. 2014;14(1):173.PubMedGoogle ScholarCrossref
Original Investigation
September 2016

Changes in Functional Mobility and Musculoskeletal Pain After Bariatric Surgery in Teens With Severe Obesity: Teen–Longitudinal Assessment of Bariatric Surgery (LABS) Study

Author Affiliations
  • 1University of Minnesota Medical School, Minneapolis
  • 2Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio
  • 3Nationwide Children’s Hospital, Columbus, Ohio
  • 4Women and Children’s Hospital of Buffalo, Buffalo, New York
JAMA Pediatr. 2016;170(9):871-877. doi:10.1001/jamapediatrics.2016.1196
Abstract

Importance  Severe obesity is associated with mobility limitations and higher incidence of multijoint musculoskeletal pain. It is unknown whether substantial weight loss improves these important outcomes in adolescents with severe obesity.

Objective  To examine the association of bariatric surgery with functional mobility and musculoskeletal pain in adolescents with severe obesity up to 2 years after surgery.

Design, Setting, and Participants  The TeenLongitudinal Assessment of Bariatric Surgery Study is a prospective, multicenter, observational study, which enrolled 242 adolescents (≤19 years of age) who were undergoing bariatric surgery from March 2007 through February 2012 at 5 US adolescent bariatric surgery centers. This analysis was conducted in November 2015.

Interventions  Roux-en-Y gastric bypass (n = 161), sleeve gastrectomy (n = 67), or laparoscopic adjustable gastric band (n = 14).

Main Outcomes and Measures  Participants completed a 400-m walk test prior to bariatric surgery (n = 206) and at 6 months (n = 195), 12 months (n = 176), and 24 months (n = 149) after surgery. Time to completion, resting heart rate (HR), immediate posttest HR, and HR difference (resting HR minus posttest HR) were measured and musculoskeletal pain concerns, during and after the test, were documented. Data were adjusted for age, sex, race/ethnicity, baseline body mass index (calculated as weight in kilograms divided by height in meters squared), and surgical center (posttest HR and HR difference were further adjusted for changes in time to completion).

Results  Of the 206 adolescents with severe obesity included in the study, 156 were female (75.7%), the mean (SD) age was 17.1 (1.6) years, and the mean (SD) body mass index was 51.7 (8.5). Compared with baseline, significant improvements were observed at 6 months for the walk test time to completion (mean, 376 seconds; 95% CI, 365-388 to 347 seconds; 95% CI, 340-358; P < .01), resting HR (mean, 84 beats per minute [bpm]; 95% CI, 82-86 to 74 bpm; 95% CI, 72-76), posttest HR (mean, 128 bpm; 95% CI, 125-131 to 113 bpm; 95% CI, 110-116), and HR difference (mean, 40 bpm; 95% CI, 36-42 to 34 bpm; 95% CI, 31-37). These changes in time to completion, resting HR, and HR difference persisted at 12 months and 24 months. Posttest HR further improved from 6 months to 12 months (mean, 113 bpm; 95% CI, 110-116 to 108 bpm; 95% CI, 105-111). There were statistically significant reductions in musculoskeletal pain concerns at all points.

Conclusions and Relevance  These data provide evidence that bariatric surgery in adolescents with severe obesity is associated with significant improvement in functional mobility and in the reduction of walking-related musculoskeletal pain up to 2 years after surgery.

Introduction

Adolescent severe obesity (body mass index [BMI, calculated as weight in kilograms divided by height in meters squared] ≥1.2 times the 95th BMI percentile) is characterized by a number of chronic comorbid conditions including functional mobility limitations and musculoskeletal pain.1-7 In adults, limitations in functional mobility, assessed using walking tests, are associated with lower quality of life,8 chronic pain,9 and early mortality.10,11 Importantly, the degree of adiposity appears to play a pivotal role in exacerbating functional mobility limitations.12-14 Youth with obesity are not immune to these consequences, often experiencing musculoskeletal pain,15 which can lead to declines in physical activity patterns and impaired functional mobility.16,17 Improving and preserving functional mobility while subsequently reducing musculoskeletal pain in adolescents with severe obesity might encourage more physical activity, thereby improving many important long-term health outcomes.

Lifestyle modification interventions in youth with severe obesity who have incorporated physical activity have shown significant improvements in cardiovascular fitness18 and walking distance.19 However, these structured programs are usually offered for a relatively short period and the long-term challenges of adherence to lifestyle changes for youth with severe obesity are well documented.20,21 Thus, there is a need to investigate whether alternative treatments offer sustained improvements in functional mobility and musculoskeletal pain outcomes in youth with severe obesity. For adults who have undergone bariatric surgery, significant improvements in standardized walk test time, mobility tasks, and cardiovascular fitness along with reductions in musculoskeletal pain have been documented.22-26 However, to our knowledge, the extent to which similar benefits accrue after bariatric surgery in adolescents is unknown.

The overall goal of this study was to examine the effect of bariatric surgery on functional mobility and musculoskeletal pain in adolescents enrolled in the Teen–Longitudinal Assessment of Bariatric Surgery (Teen-LABS) Study up to 2 years after surgery. We used a standardized 400-m walk test with assessments of time to test completion, resting heart rate (HR), immediate posttest HR, HR recovery, and walking-related musculoskeletal pain to examine changes over time.

Box Section Ref ID

Key Points

  • Question Does bariatric surgery improve functional mobility and reduce musculoskeletal pain in adolescents with severe obesity?

  • Findings Within the context of a longitudinal multicenter study of adolescent bariatric surgery, time to completion of a 400-m walk test, resting heart rate, and heart rate difference were improved compared with baseline and at 6, 12, and 24 months after surgery. There were statistically significant reductions in musculoskeletal pain concerns at all times.

  • Meaning Bariatric surgery is associated with improved functional mobility and reduction in musculoskeletal pain in adolescents with severe obesity up to 2 years after surgery.

Methods
Study Cohort and Measurement Points

Participants from the Teen-LABS Study were included in this analysis conducted in November 2015.27 The Teen-LABS Study is an ongoing National Institute of Diabetes and Digestive and Kidney Diseases–funded, prospective, longitudinal, multicenter observational study that enrolled consecutive adolescents (≤19 years of age) undergoing bariatric surgery at 5 clinical centers. Written parental permission, participant assent (<18 years old), and consent from older adolescents (≥18 years old) were obtained. Data collection points used for this analysis were baseline (preoperative) and 6-month, 12-month, and 24-month postoperative assessments. At each assessment, height was measured on a wall-mounted stadiometer and weight on an electronic scale (Scale-Tronix 5200, Scale Tronix, or Tanita TBF310) and BMI was calculated.

The protocol and data and safety monitoring plans were approved by the institutional review board at each institution and by a data and safety monitoring board for the study as a whole.

Assessment of Functional Mobility

Participants completed a 400-m walk test prior to planned bariatric surgery and again at 6 months, 12 months, and 24 months after surgery. Time to completion, resting HR, immediate posttest HR, 2-minute HR recovery (posttest HR minus 2-minute postcompletion HR), and HR difference (resting HR minus immediate posttest HR) were measured. Heart rate was measured by a Polar HR monitor (Polar Electro Inc), while completion time was measured by stopwatch. We have previously reported the accuracy and validity of physical activity measurement during a 400-m walk test in youth with severe obesity.28 Musculoskeletal pain concerns were documented during and after the completion of the 400-m walk tests and consisted of knee, hip, calf, foot, and back pain, along with numbness or tingling and leg cramps. Any of these indications during or after the test qualified as a musculoskeletal pain concern and were combined for analysis (composite end point).

Statistical Analysis

Standard descriptive statistics summarized participant characteristics at baseline. Categorical variables were calculated as frequencies and percentages. A quantile-quantile plot was used to determine whether response variables (time to completion, resting HR, posttest HR, 2-minute HR recovery, and HR difference) were normally distributed. On the basis of the observed plot, log transformations were used to normalize the time-to-completion distribution for subsequent modeling. Linear mixed-effects models were used to determine the changes over time in functional mobility parameters from baseline. Initially, both random intercept and slope were used to fit the data, but random slope was dropped from the final model because it was not statistically significant. The unstructured covariance was used in order for each variance and covariance to be freely estimated. Generalized estimating equations were used to estimate the relative risk associated with musculoskeletal pain concerns (with vs without pain) following surgery. An unstructured correlation with robust variance estimators was used for model estimates. All models were adjusted for age, race/ethnicity, sex, baseline BMI, and surgical center. Surgery type was also entered in the initial models but was not statistically significant in any models, and so it was removed from the final models. Data using postsurgery (6-month, 12-month, and 24-month) follow-up visits for immediate posttest HR, 2-minute HR recovery, and HR difference were further adjusted for changes in time to completion. Multiple imputation was used for missing covariates for all models. Data are presented as means with 95% CIs. The estimates presented in the figures represent marginally adjusted means and associated 95% CIs from the models. The statistical significance level was set at α = .05. Bonferroni adjustment for multiple testing was used for all post hoc comparisons between time points within each hypothesis considered in this study. All analyses were conducted with SAS statistical software version 9.4 (SAS Institute Inc).

Results

Preoperative demographic, anthropometric, and clinical characteristics of the sample are displayed in the Table. Most patients were female (n = 156, 75.7%) and white (n = 149, 72.3%). Of the 3 surgical procedures performed, most were Roux-en-Y gastric bypass (n = 139, 67.5%) followed by vertical sleeve gastrectomy (n = 56, 27.2%) and laparoscopic adjustable gastric banding (n = 11, 5.3%). Owing to the relatively small number of patients who received laparoscopic adjustable gastric banding and the well-described differences in BMI outcome compared with Roux-en-Y gastric bypass and vertical sleeve gastrectomy, this group was excluded from the analysis. The BMI percentage change from baseline to 6 months was a decrease of 32.5%; from 6 months to 12 months, an additional decrease of 7.8% (40.3% cumulative BMI percentage reduction); and from 12 months to 24 months, an additional decrease of 0.2% (40.4% cumulative BMI percentage reduction). A total of 109 patients (53%) had measurements for all 4 visits, and 67 (33%) had 3 measurements of 4 visits. A total of 22 (11%) and 8 (4%) completed 2 measurements and 1 measurement, respectively, of all 4 visits.

At baseline, BMI was significantly positively associated (P < .05) with posttest HR (r = 0.33; P < .01), time to completion (r = 0.16; P = .02), and 2-minute HR recovery (r = 0.18; P = .01) and was significantly inversely associated with HR difference (r = 0.17; P = .01) after adjusting for age, sex, and race/ethnicity (eTable in the Supplement). Changes in time to completion and resting HR, adjusted for age, sex, race/ethnicity, baseline BMI, and surgical center at baseline, 6 months, 12 months, and 24 months are displayed in Figure 1. At 6 months after surgery, significant improvements were observed in time to completion (mean [SD], 376 [1] seconds; 95% CI, 365-388 to 347 [1] seconds; 95% CI, 340-358; P < .01) and resting HR (mean [SD], 84 [1] beats per minute [bpm]; 95% CI, 82-86 to 74 [1] bpm; 95% CI, 72-76; P < .01). The changes in time to completion and resting HR persisted at 12 months and 24 months, with no additional statistically significant improvements observed.

Changes in posttest HR, HR difference, and 2-minute HR recovery, adjusted for age, sex, race/ethnicity, baseline BMI, surgical center, and change in time to completion at baseline, 6 months, 12 months, and 24 months are displayed in Figure 2. At 6 months after surgery, significant improvements were observed in posttest HR (mean [SD], 128 [2] bpm; 95% CI, 125-131 to 113 [2] bpm; 95% CI, 110-116; P < .01), and HR difference (mean [SD], 40 [2] bpm; 95% CI, 36-42 to 34 [2] bpm; 95% CI, 31-37; P < .01). There was a significant improvement in 2-minute HR recovery from baseline to 12 months (mean [SD], −31 [1] bpm; 95% CI −33 to −28 to −25 [1] bpm; 95% CI, −28 to −23; P < .01) but no other statistically significant differences were observed between time points. There was no additional statistically significant improvement in HR difference at 12 months and 24 months. Posttest HR further improved from 6 months to 12 months (mean [SD], 113 [2] bpm; 95% CI, 110-116 to 108 [2] bpm; 95% CI, 105-111; P = .01) with no additional improvements observed at 24 months.

At 6 months, no association between percentage change in BMI and any measure of functional mobility or musculoskeletal pain was observed. At 12 months (β = 1.08) and 24 months (β = 1.01) only, change in time to completion was associated with percentage change in BMI (P < .01). Additionally, no consistent associations between changes in systolic blood pressure, diastolic blood pressure, or mean arterial pressure with changes in HR responses were observed.

The cumulative number of participants reporting walking-related musculoskeletal pain concerns is displayed in Figure 3. From baseline, the relative risk (RR) of musculoskeletal pain concerns after adjusting for age, sex, race/ethnicity, baseline BMI, and surgical center was reduced at 6 months (RR, 0.76; 95% CI, 0.67-0.84]), 12 months (RR, 0.62; 95% CI, 0.51-0.71), and 24 months (RR, 0.47; 95% CI, 0.37-0.62) (P < .01 all from baseline).

Discussion

The findings from this prospective observational study of bariatric surgery in adolescents with severe obesity suggest that meaningful and durable improvements in functional mobility and reductions in musculoskeletal pain occur in the postsurgical setting. Most improvements were observed at 6 months after surgery, which is concurrent with the greatest weight loss achieved. However, the changes at 6 months were not associated with the magnitude of reduction in BMI. Importantly, all measures of functional mobility and musculoskeletal pain, which improved at 6 months, were maintained up to the 2-year follow-up point.

To our knowledge, this is the first study to conduct standardized 400-m walk tests in adolescents with severe obesity prior to and following bariatric surgical intervention (ie, up to 2 years). Our findings are in line with several adult studies, which observed significant improvements in resting HR, posttest HR, exercise capacity, and reductions in musculoskeletal pain after bariatric surgery.22-26 Direct comparison between adult studies and the present study are challenging because most adult studies used a time-based assessment (6-minute walk test) rather than a distance-based assessment (400-m walk test) as was measured in our study. However, the mean completion time for the walk test among participants in our study was only slightly longer than 6 minutes (6 minutes and 17 seconds) and the distance covered in most adult studies was around 400 m (381-489 m), suggesting that it might be reasonable to make comparisons.24,26,29 De Souza et al26 observed improvements in resting HR and immediate posttest HR in adults 7 to 12 months following bariatric surgery along with greater distance achieved. Similarly, Maniscalco and colleagues29 reported improvements in resting HR, immediate posttest HR, and changes in respiratory function 1 year after bariatric surgery. The magnitude of change in HR response prior to and after testing was comparable between the present study and those reported in adults. Taken together, the body of literature suggests that functional mobility in both adults and adolescents with severe obesity can be improved in a relatively short period following bariatric surgery.

The mechanism(s) responsible for reductions in HR response at rest and after testing are unknown and may not be entirely weight loss dependent. Others have shown that adults 3 months following bariatric surgery exhibited significantly reduced resting HR and, during a 6-minute walk test, had significantly improved HR responses during and immediately following the test as well as demonstrated improved HR recovery.24 Interestingly, these changes in HR were accompanied by peripheral muscular metaboreflex responses, which are indicative of enhanced muscle profusion. Studies in adults30,31 and adolescents32,33 have shown beneficial adaptations in cardiac structure and function following bariatric surgery, which when coupled with improvements in systemic vascular function,34,35 may play an important role in regulating HR responses during rest and after exercise. Although physiologically plausible, this theory is somewhat speculative, and we observed no association between changes in HR response and changes in blood pressure at any point. However, the mechanism(s) of beneficial adaptation in resting and exercise HR response following bariatric surgery warrants further evaluation.

We also observed meaningful reductions in musculoskeletal pain concerns both during and after the 400-m walk test. The reduction in pain following bariatric surgery could translate to increased physical activity patterns in adolescents with severe obesity because joint pain can influence willingness to engage in activity.36 Correspondingly, increasing physical activity could yield many important improvements in cardiometabolic health without the necessity for further weight loss.37 Therefore, by reducing musculoskeletal pain, bariatric surgery may make many activities of daily life less burdensome for youth with severe obesity and could contribute to reducing factors that affect long-term health risks.

This study had several strengths including a large sample size, strong longitudinal follow-up, and use of a clinically relevant measure of functional mobility, which was consistently delivered across enrollment sites. Moreover, our adjustments for specific confounding variables (eg, baseline BMI and changes in time to completion), which might influence HR response, aid in the interpretation of the results as differing levels of adiposity and completion time may influence energy demands during movement.38 Our study was limited by the lack of a nonsurgical control group with which to compare outcomes over time. We were underpowered to determine whether any differences were present in changes in functional mobility or musculoskeletal pain between surgery types (Roux-en-Y gastric bypass vs vertical sleeve gastrectomy), but this comparison is scientifically relevant given the likely differences in mechanisms of metabolic change with these operations. Despite measuring musculoskeletal pain concerns during and after testing, the limited number of concerns, specifically after surgery, limited our ability to determine joint-specific changes. We do not present data on day-to-day variation in musculoskeletal pain,39 which could have aided in the interpretation of our research findings. Finally, despite being a clinically translatable measure of functional mobility, the 400-m walk test is not a gold-standard measure of physical fitness as compared with a graded exercise test; therefore, these results may or may not be indicative of true changes in cardiorespiratory fitness.

Conclusions

Bariatric surgery in adolescents with severe obesity is associated with significant improvement in resting HR, completion time of a standardized 400-m walk test, and immediate posttest HR response; it is also associated with a reduction in walking-related musculoskeletal pain concerns at 6 months after surgery. These meaningful improvements were maintained up to 2 years after surgery. Whether these positive changes in functional mobility and musculoskeletal pain persist over the long-term and lead to further improvements in cardiometabolic risk requires evaluation.

Back to top
Article Information

Accepted for Publication: April 20, 2016.

Corresponding Author: Justin R. Ryder, PhD, Department of Pediatrics, University of Minnesota Medical School, 420 Delaware St SE, MMC 715, Minneapolis, MN 55455 (jrryder@umn.edu).

Published Online: July 18, 2016. doi:10.1001/jamapediatrics.2016.1196.

Author Contributions: Dr Jenkins had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Ryder, Edwards, Michalsky, Harmon, Inge, Kelly.

Acquisition, analysis, or interpretation of data: Ryder, Edwards, Gupta, Khoury, Jenkins, Bout-Tabaku, Michalsky, Inge, Kelly.

Drafting of the manuscript: Ryder, Gupta, Michalsky, Harmon.

Critical revision of the manuscript for important intellectual content: Ryder, Edwards, Gupta, Khoury, Jenkins, Bout-Tabaku, Michalsky, Inge, Kelly.

Statistical analysis: Ryder, Gupta, Khoury, Jenkins.

Obtained funding: Harmon, Inge.

Administrative, technical, or material support: Kelly.

Study supervision: Edwards, Bout-Tabaku, Inge, Kelly.

Conflict of Interest Disclosures: Dr Inge has received bariatric research grant funding from Ethicon Endosurgery and has served as consultant for Sanofi, NPS Pharma, Up To Date, and Independent Medical Expert Consulting Services, all unrelated to this project. Dr Kelly serves as a consultant for Takeda Pharmaceuticals and Novo Nordisk Pharmaceuticals and is the signatory author for a pediatric obesity clinical trial sponsored by Novo Nordisk Pharmaceuticals; he does not accept personal or professional income for his services. Dr Kelly receives research support from AstraZeneca Pharmaceuticals in the form of drug/placebo. No other disclosures were reported.

Funding/Support: Funding for Teen-LABS was provided by grants U01DK072493 and UM1 DK072493 from the National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health (NIH) (Dr Inge) and grants 8UL1TR000077 and UL1TR000114 from the National Center for Research Resources and the National Center for Advancing Translational Sciences, NIH. Dr Ryder is supported by individual training grant F32-HL127881 from the National Heart, Lung, and Blood Institute, NIH.

Role of the Funder/Sponsor: The funding agencies had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.

References
1.
Gidding  SS, Nehgme  R, Heise  C, Muscar  C, Linton  A, Hassink  S.  Severe obesity associated with cardiovascular deconditioning, high prevalence of cardiovascular risk factors, diabetes mellitus/hyperinsulinemia, and respiratory compromise.  J Pediatr. 2004;144(6):766-769.PubMedGoogle ScholarCrossref
2.
Stovitz  SD, Pardee  PE, Vazquez  G, Duval  S, Schwimmer  JB.  Musculoskeletal pain in obese children and adolescents.  Acta Paediatr. 2008;97(4):489-493.PubMedGoogle ScholarCrossref
3.
Taylor  ED, Theim  KR, Mirch  MC,  et al.  Orthopedic complications of overweight in children and adolescents.  Pediatrics. 2006;117(6):2167-2174.PubMedGoogle ScholarCrossref
4.
Krul  M, van der Wouden  JC, Schellevis  FG, van Suijlekom-Smit  LWA, Koes  BW.  Musculoskeletal problems in overweight and obese children.  Ann Fam Med. 2009;7(4):352-356.PubMedGoogle ScholarCrossref
5.
Wearing  SC, Hennig  EM, Byrne  NM, Steele  JR, Hills  AP.  The impact of childhood obesity on musculoskeletal form.  Obes Rev. 2006;7(2):209-218.PubMedGoogle ScholarCrossref
6.
Kelly  AS, Barlow  SE, Rao  G,  et al; American Heart Association Atherosclerosis, Hypertension, and Obesity in the Young Committee of the Council on Cardiovascular Disease in the Young, Council on Nutrition, Physical Activity and Metabolism, and Council on Clinical Cardiology.  Severe obesity in children and adolescents: identification, associated health risks, and treatment approaches: a scientific statement from the American Heart Association.  Circulation. 2013;128(15):1689-1712.PubMedGoogle ScholarCrossref
7.
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):552-559.PubMedGoogle ScholarCrossref
8.
Forhan  M, Gill  SV.  Obesity, functional mobility and quality of life.  Best Pract Res Clin Endocrinol Metab. 2013;27(2):129-137.PubMedGoogle ScholarCrossref
9.
Okifuji  A, Hare  BD.  The association between chronic pain and obesity.  J Pain Res. 2015;8:399-408.PubMedGoogle ScholarCrossref
10.
Vestergaard  S, Patel  KV, Bandinelli  S, Ferrucci  L, Guralnik  JM.  Characteristics of 400-meter walk test performance and subsequent mortality in older adults.  Rejuvenation Res. 2009;12(3):177-184.PubMedGoogle ScholarCrossref
11.
Newman  AB, Simonsick  EM, Naydeck  BL,  et al.  Association of long-distance corridor walk performance with mortality, cardiovascular disease, mobility limitation, and disability.  JAMA. 2006;295(17):2018-2026.PubMedGoogle ScholarCrossref
12.
Correia de Faria Santarém  G, de Cleva  R, Santo  MA,  et al.  Correlation between body composition and walking capacity in severe obesity.  PLoS One. 2015;10(6):e0130268.PubMedGoogle ScholarCrossref
13.
Hergenroeder  AL, Brach  JS, Otto  AD, Sparto  PJ, Jakicic  JM.  The influence of body mass index on self-report and performance-based measures of physical function in adult women.  Cardiopulm Phys Ther J. 2011;22(3):11-20.PubMedGoogle Scholar
14.
King  WC, Engel  SG, Elder  KA,  et al.  Walking capacity of bariatric surgery candidates.  Surg Obes Relat Dis. 2012;8(1):48-59.PubMedGoogle ScholarCrossref
15.
Tsiros  MD, Coates  AM, Howe  PR, Grimshaw  PN, Buckley  JD.  Obesity: the new childhood disability?  Obes Rev. 2011;12(1):26-36.PubMedGoogle ScholarCrossref
16.
Norman  A-C, Drinkard  B, McDuffie  JR, Ghorbani  S, Yanoff  LB, Yanovski  JA.  Influence of excess adiposity on exercise fitness and performance in overweight children and adolescents.  Pediatrics. 2005;115(6):e690-e696.PubMedGoogle ScholarCrossref
17.
Shultz  SP, Anner  J, Hills  AP.  Paediatric obesity, physical activity and the musculoskeletal system.  Obes Rev. 2009;10(5):576-582.PubMedGoogle ScholarCrossref
18.
Knöpfli  BH, Radtke  T, Lehmann  M,  et al.  Effects of a multidisciplinary inpatient intervention on body composition, aerobic fitness, and quality of life in severely obese girls and boys.  J Adolesc Health. 2008;42(2):119-127.PubMedGoogle ScholarCrossref
19.
Mendelson  M, Michallet  AS, Perrin  C, Levy  P, Wuyam  B, Flore  P.  Exercise training improves breathing strategy and performance during the six-minute walk test in obese adolescents.  Respir Physiol Neurobiol. 2014;200:18-24.PubMedGoogle ScholarCrossref
20.
Danielsson  P, Kowalski  J, Ekblom  Ö, Marcus  C.  Response of severely obese children and adolescents to behavioral treatment.  Arch Pediatr Adolesc Med. 2012;166(12):1103-1108.PubMedGoogle ScholarCrossref
21.
Knop  C, Singer  V, Uysal  Y, Schaefer  A, Wolters  B, Reinehr  T.  Extremely obese children respond better than extremely obese adolescents to lifestyle interventions.  Pediatr Obes. 2015;10(1):7-14.PubMedGoogle ScholarCrossref
22.
Serés  L, Lopez-Ayerbe  J, Coll  R,  et al.  Increased exercise capacity after surgically induced weight loss in morbid obesity.  Obesity (Silver Spring). 2006;14(2):273-279.PubMedGoogle ScholarCrossref
23.
de Souza  SA, Faintuch  J, Sant’anna  AF.  Effect of weight loss on aerobic capacity in patients with severe obesity before and after bariatric surgery.  Obes Surg. 2010;20(7):871-875.PubMedGoogle ScholarCrossref
24.
da Silva  RP, Martinez  D, Faria  CC,  et al.  Improvement of exercise capacity and peripheral metaboreflex after bariatric surgery.  Obes Surg. 2013;23(11):1835-1841.PubMedGoogle ScholarCrossref
25.
Wilms  B, Ernst  B, Thurnheer  M, Weisser  B, Schultes  B.  Differential changes in exercise performance after massive weight loss induced by bariatric surgery.  Obes Surg. 2013;23(3):365-371.PubMedGoogle ScholarCrossref
26.
de Souza  SA, Faintuch  J, Fabris  SM,  et al.  Six-minute walk test: functional capacity of severely obese before and after bariatric surgery.  Surg Obes Relat Dis. 2009;5(5):540-543.PubMedGoogle ScholarCrossref
27.
Inge  TH, Courcoulas  AP, Jenkins  TM,  et al; Teen-LABS Consortium.  Weight loss and health status 3 years after bariatric surgery in adolescents.  N Engl J Med. 2016;374(2):113-123.PubMedGoogle ScholarCrossref
28.
Jeffreys  RM, Inge  TH, Jenkins  TM,  et al.  Physical activity monitoring in extremely obese adolescents from the Teen-LABORATORIES Study.  J Phys Act Health. 2015;12(1):132-138.PubMedGoogle ScholarCrossref
29.
Maniscalco  M, Zedda  A, Giardiello  C,  et al.  Effect of bariatric surgery on the six-minute walk test in severe uncomplicated obesity.  Obes Surg. 2006;16(7):836-841.PubMedGoogle ScholarCrossref
30.
Owan  T, Avelar  E, Morley  K,  et al.  Favorable changes in cardiac geometry and function following gastric bypass surgery: 2-year follow-up in the Utah obesity study.  J Am Coll Cardiol. 2011;57(6):732-739.PubMedGoogle ScholarCrossref
31.
Jhaveri  RR, Pond  KK, Hauser  TH,  et al.  Cardiac remodeling after substantial weight loss: a prospective cardiac magnetic resonance study after bariatric surgery.  Surg Obes Relat Dis. 2009;5(6):648-652.PubMedGoogle ScholarCrossref
32.
Michalsky  MP, Raman  SV, Teich  S, Schuster  DP, Bauer  JA.  Cardiovascular recovery following bariatric surgery in extremely obese adolescents: preliminary results using cardiac magnetic resonance (CMR) imaging.  J Pediatr Surg. 2013;48(1):170-177.PubMedGoogle ScholarCrossref
33.
Ippisch  HM, Inge  TH, Daniels  SR,  et al.  Reversibility of cardiac abnormalities in morbidly obese adolescents.  J Am Coll Cardiol. 2008;51(14):1342-1348.PubMedGoogle ScholarCrossref
34.
Vázquez  LA, Pazos  F, Berrazueta  JR,  et al.  Effects of changes in body weight and insulin resistance on inflammation and endothelial function in morbid obesity after bariatric surgery.  J Clin Endocrinol Metab. 2005;90(1):316-322.PubMedGoogle ScholarCrossref
35.
Gokce  N, Vita  JA, McDonnell  M,  et al.  Effect of medical and surgical weight loss on endothelial vasomotor function in obese patients.  Am J Cardiol. 2005;95(2):266-268.PubMedGoogle ScholarCrossref
36.
Shultz  SP, Anner  J, Hills  AP.  Paediatric obesity, physical activity and the musculoskeletal system.  Obes Rev. 2009;10(5):576-582.PubMedGoogle ScholarCrossref
37.
Shaibi  GQ, Ryder  JR, Kim  JY, Barraza  E.  Exercise for obese youth: refocusing attention from weight loss to health gains.  Exerc Sport Sci Rev. 2015;43(1):41-47.PubMedGoogle ScholarCrossref
38.
Saibene  F, Minetti  AE.  Biomechanical and physiological aspects of legged locomotion in humans.  Eur J Appl Physiol. 2003;88(4-5):297-316.PubMedGoogle ScholarCrossref
39.
Legault  ÉP, Cantin  V, Descarreaux  M.  Assessment of musculoskeletal symptoms and their impacts in the adolescent population: adaptation and validation of a questionnaire.  BMC Pediatr. 2014;14(1):173.PubMedGoogle ScholarCrossref
×