Abstract
Importance
Severe obesity is associated with mobility limitations and higher incidence of multi-joint musculoskeletal pain. Whether substantial weight loss improves these important outcomes in adolescents with severe obesity is unknown.
Objective
To examine the effect of bariatric surgery on functional mobility and musculoskeletal pain in adolescents with severe obesity up to 2 years post-surgery.
Design
Teen- Longitudinal Assessment of Bariatric Surgery (Teen-LABS) 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.
Setting
Five adolescent bariatric surgery centers in the United States.
Participants
Adolescents with severe obesity (n=242; Male = 59 / Female = 183; mean±SD: age = 17±2 years; body mass index [BMI] = 53±9 kg/m2).
Intervention(s)
Roux-en-Y gastric bypass (n=161), sleeve gastrectomy (n=67) or laparoscopic adjustable gastric band (n=14).
Main Outcome and Measure(s)
Participants completed a 400m walk test prior to bariatric surgery (n=206) and at 6mo (n=195), 12mo (n=176), and 24mo (n=149) post-surgery. Time-to-completion, resting heart rate (HR), immediate post-test HR, and HR difference (resting HR-post-test HR) were measured and musculoskeletal pain complaints, during and post-test, were documented. Data were adjusted for age, gender, race, baseline BMI, and surgical center (post-test HR and HR difference were further adjusted for changes in time-to-completion).
Results
Compared to baseline, significant improvements were observed at 6mo for walk test time-to-completion (mean (95% CI [throughout]): 376 (365, 388) to 347 (340, 358) sec), resting HR (84 (82, 86) to 74 (72, 76) bpm), post-test HR (128 (125, 131) to 113 (110, 116) bpm), and HR difference (40 (36, 42) to 34 (31, 37) bpm). These changes in time-to-completion, resting HR, and HR difference persisted at 12mo and 24mo. Post-test HR further improved from 6mo to 12mo (113 (110, 116) to 108 (105, 111) bpm. There were statistically significant reductions in musculoskeletal pain complaints at all time-points.
Conclusions and Relevance
These data provide evidence that bariatric surgery in adolescents with severe obesity significantly improves functional mobility and reduces walking-related musculoskeletal pain up to 2 years post-surgery.
Keywords: Adolescent, Bariatric Surgery, Functional Mobility, Musculoskeletal Pain, Obesity, Walk Test
Background
Adolescent severe obesity (Body mass index [BMI] ≥ 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 that 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 of time 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, 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 post-surgery. We utilized a standardized 400m walk test with assessments of time to test completion, resting heart rate (HR), immediate post-test HR, HR recovery, and walking-related musculoskeletal pain to examine changes over-time.
Methods
Study Cohort and Measurement Time-Points
Participants from Teen-LABS were utilized for this analysis.27 Teen-LABS is an ongoing National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) - funded, prospective, longitudinal, multicenter observational study that enrolled consecutive adolescents (≤ 19 years of age) undergoing bariatric surgery at five clinical centers. Parental permission and participant assent (<18 years old), and consent from older adolescents (≥18 years old) were obtained. Data collection time-points used for this analysis were baseline (pre-operative) and 6mo, 12mo, and 24mo post-operative assessments. At each assessment, height was measured on a wall-mounted stadiometer and weight on an electronic scale (Scale-Tronix 5200, Scale Tronix, White Plains, NY, USA or Tanita TBF310, Arlington Heights, Illinois, USA) and BMI was calculated.
Assessment of Functional Mobility
Participants completed a 400 meter walk test prior to planned bariatric surgery and again at 6mo, 12mo, and 24mo post-surgery. Time-to-completion, resting HR, immediate post-test HR, 2-min HR recovery (post-test HR – 2-min post-completion HR), and HR difference (resting HR – immediate post-test HR) were measured. HR was measured by a Polar heart rate monitor (Polar Electro Inc., NY, USA), while completion time was measured by stopwatch. We have previously reported the accuracy and validity of physical activity measurement during a 400m walk test in youth with severe obesity.28 Musculoskeletal pain complaints were documented during and after the completion of the 400m 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 complaint and were combined for analysis (composite endpoint).
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, post-test HR, 2-min HR recover, 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 since 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 complaints (with versus without pain) following surgery. An Unstructured correlation with robust variance estimators was used for model estimates. All models were adjusted for age, race, gender, baseline BMI, and surgical center. Surgery type was also entered in the initial models but was not statistically significant in any models, and so removed from the final models. Data utilizing post-surgery (6mo, 12mo, and 24mo) follow-up visits for immediate post-test HR, 2-min 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 mean with 95% confidence intervals. The estimates presented in the figures represent marginally adjusted means and associated 95% confidence intervals from the models. Statistical significance level was set at α=0.05. 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., Cary, NC).
Results
Pre-operative demographic, anthropometric, and clinical characteristics of the sample are displayed in Table 1. The majority of patients were female (75.7%) and white (72.3%). Of the 3 surgical procedures performed, the majority underwent Roux-en-Y gastric bypass (RYGB; 67.4%) followed by vertical sleeve gastrectomy (VSG; 27.1%) and laparoscopic adjustable gastric banding (LAGB; 5.3%). Due to the relatively small number of patients who received LAGB and the well-described differences in BMI outcome compared to RYGB and VSG, this group was excluded from the analysis. The BMI percent 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 reduction); and from 12 months to 24 months an additional decrease of 0.2% (40.4% cumulative %BMI reduction). A total of 109 (53%) subjects had measurements for all four visits, and 67 (33%) had three measurements out of four visits. A total of 22 (11%) and 8 (3%) completed two measurements and one measurement respectively out of all four visits.
Table 1.
Pre-operative (baseline) demographic, anthropometric, and surgical type for the Teen-LABS cohort (n=206).
| Mean (SD) or Frequency (%) | Minimum | Maximum | |
|---|---|---|---|
| Age at operation (yr) | 17.1 (1.57) | 13.2 | 20.3 |
| BMI (kg/m2) | 51.7 (8.5) | 33.9 | 80.4 |
| Gender | Male 50 (24.2%) / Female 156 (75.7%) | ||
| Race | |||
| -White | 149 (72.3) | ||
| -Black | 44 (21.3) | ||
| -Asian | 1 (0.5%) | ||
| -Multi-racial | 12 (0.83) | ||
| Surgical Type | |||
| -RYGB | 139 (67.4%) | ||
| -VSG | 56 (27.1%) | ||
| -LAGB** | 11 (5.3%) | ||
Data were not included in the present analysis
BMI = Body mass index; RYGB =Roux-en-Y gastric bypass; VSG= Vertical sleeve gastrectomy; LAGB = Laparoscopic adjustable gastric banding
At baseline, BMI was significantly positively associated (p<0.05) with post-test HR, time-to-completion, and 2-min HR recovery and significantly inversely associated HR difference after adjusting for age, gender, and race (Table S1). Changes in time-to-completion and resting HR, adjusted for age, gender, race, baseline BMI, and surgical center at baseline, 6mo, 12mo, and 24mo are displayed in Figure 1. At 6mo post-surgery, significant improvements were observed in time-to-completion (376±1 sec [95% CI: 365, 388] to 347±1 sec [95% CI: 340, 358], p<0.01) and resting HR (84±1 bpm [95% CI: 82, 86] to 74±1 bpm [95% CI: 72, 76], p<0.01). The changes in time-to-completion and resting HR persisted at 12mo and 24mo, with no additional statistically significant improvements observed.
Figure 1.
Changes in time-to-completion (A) for the 400m walk test and resting HR (B) prior to testing from baseline to 6mo, 12mo, and 24mo. Data are adjusted for age, gender, race, baseline BMI, and surgical center. Error bars represent the 95% CI with an * indicating p<0.01 from baseline.
Changes in post-test HR, HR difference, and 2-min HR recovery, adjusted for age, gender, race, baseline BMI, surgical center, and change in time-to-completion at baseline, 6mo, 12mo, and 24mo are displayed in Figure 2. At 6mo post-surgery, significant improvements were observed in post-test HR (129±2 bpm [95% CI: 126, 133] to 112±2 bpm [95% CI: 109, 116], p<0.01), and HR difference (40±2 bpm [95% CI: 37, 43] to 34±2 bpm [95% CI: 31, 37], p<0.01). There was a significant improvement in 2-min HR recovery from baseline to 12mo (−31±1 bpm [95% CI: −33, −28] to −25±1 bpm [95% CI: −28, −23], p<0.01) but no other statistically significant differences were observed between time-point. There was no additional statistically significant improvement in HR difference at 12mo and 24mo. Post-test HR further improved from 6mo to 12mo (112±2 bpm [95% CI: 109, 116] to 107±2 bpm [95% CI: 103, 110], p=0.01) with no additional improvements observed at 24mo.
Figure 2.
Changes in post-test HR (A), HR difference (B), and 2-min HR recovery [post-test HR – 2min post-completion HR] (C) from baseline to 6mo, 12mo, and 24mo. Data are adjusted for age, gender, race, baseline BMI, surgical center, and change in time-to-completion. Error bars represent the 95% CI with an * indicating p<0.01 from baseline and
indicating p=0.10 from 6mo.
At 6mo, no association between percent change in BMI and any measure of functional mobility or musculoskeletal pain was observed. At 12mo and 24mo only, change in time-to-completion was associated with percent change in BMI (P<0.01). 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 complaints is displayed in Figure 3. From baseline, the relative risk (RR) of musculoskeletal pain complaints after adjusting for age, gender, race, baseline BMI, and surgical center was reduced at 6mo (RR: 0.76 [95% CI: 0.67, 0.84]), 12mo (RR: 0.62 [95% CI: 0.51,0.71]), 24mo (0.47 [95% CI: 0.37, 0.62]) (p<0.01 all from baseline).
Figure 3.
Percentage of patients with and without musculoskeletal pain complaints during or after 400m walk test at baseline (pre-operative), and 6mo, 12mo, and 24mo follow-up. Relative risk (RR) of having musculoskeletal pain complaints from baseline with 95% CI are listed below. P-value indicates difference 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 post-surgical setting. The majority of improvements were observed at 6mo post-surgery, which is concurrent with the greatest weight loss achieved. However, the changes at 6mo were not associated with the magnitude of reduction in BMI. Importantly, all measures of functional mobility and musculoskeletal pain, which improved at 6mo, were maintained up to the 2 year follow-up time point.
To our knowledge this is the first study to conduct standardized 400m walk tests in adolescents with severe obesity prior to and following bariatric surgical intervention (i.e. up to 2 years). Our findings are in line with several adult studies, which observed significant improvements in resting HR, post-test HR, exercise capacity, and reductions in musculoskeletal pain post-bariatric surgery.22–26 Direct comparison between adult studies and the present study are challenging since the majority of adult studies utilized a time-based assessment (6min walk test) rather than a distance-based assessment (400m 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 above 6min (6min 17s) and the distance covered in most adult studies was around 400m (381–489m), suggesting that it might be reasonable to make comparisons.24,26,29 de Souza et al. observed improvements in resting HR and immediate post-test HR in adults 7–12mo following bariatric surgery along with greater distance achieved.26 Similarly, Maniscalco and colleagues reported improvements in resting HR, immediate post-test HR, and changes in respiratory function 1 year after bariatric surgery.29 The magnitude of change in HR response prior and post-test 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 of time following bariatric surgery.
The mechanism(s) responsible for reductions in HR response at rest and post-test are unknown and may not be entirely weight loss-dependent. Others have shown that adults 3mo following bariatric surgery exhibited significantly reduced resting HR and, during a 6min 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 post-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 time 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 complaints both during and after the 400m walk test. The reduction in pain following bariatric surgery could translate to increased physical activity patterns in adolescents with severe obesity since 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 which effect long-term health risks.
This study has several strengths including a large sample size, strong longitudinal follow-up, and utilization of a clinically-relevant measure of functional mobility, which was consistently delivered across enrollment sites. Moreover, our adjustments for specific confounding variables (e.g. 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 greatly influence energy demands during movement.38 Our study is limited by the lack of a non-surgical control group with which to compare outcomes over time. We were underpowered to determine if any differences were present in changes in functional mobility or musculoskeletal pain between surgery types (RYGB vs. VSG), but this comparison is scientifically relevant given the likely differences in mechanisms of metabolic change with these operations. Despite measuring musculoskeletal pain complaints during and post-test, the limited number of complaints, specifically post-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 400m walk test is not a gold-standard measure of physical fitness as compared to a graded exercise test; therefore, these results may or may not be indicative of true changes in cardiorespiratory fitness.
Conclusion
Bariatric surgery in adolescents with severe obesity significantly improves resting HR, completion time of a standardized 400m walk test, and immediate post-test HR response, and reduces walking-related musculoskeletal pain complaints at 6mo post-surgery. These meaningful improvements were maintained up to 2 years post-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.
Supplementary Material
Acknowledgments
Trial Registration: Funded by the National Institute of Diabetes and Digestive and Kidney Diseases; Teen-LABS ClinicalTrials.gov number, NCT00474318
Funding for Teen-LABS was provided by the National Institutes of Health (NIH) (U01DK072493 / UM1 DK072493 to T.H.I.) and the National Center for Research Resources and the National Center for Advancing Translational Sciences, NIH (8UL1TR000077). Support also came from National Center for Research Resources and the National Center for Advancing Translational Sciences, NIH, (UL1TR000114). J.R.R. is supported by an individual training grant from the National Heart Lung and Blood Institute, NIH (F32-HL127881). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. Dr. Jenkins had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. 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.
Footnotes
Author Disclosures: Dr. Inge has received bariatric research grant funding from Ethicon Endosurgery, and has served as consultant for Sanofi Corporation, NPS Pharma, and 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 also receives research support from Astra Zeneca Pharmaceuticals in the form of drug/placebo.
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