Abstract
Background:
Bariatric surgery results in significant and durable weight loss and improved health in severely obese adolescents. An important adverse consequence of the massive weight loss after bariatric surgery is excess skin and soft tissue. The prevalence and clinical characteristics of excess-skin related symptoms have been described in adults undergoing bariatric surgery but not in adolescents. While the higher skin elasticity of adolescents may result in fewer excess skin problems compared to adults, this hypothesis remains untested. The purpose of the present study was to describe the natural history of excess skin and its associated complications among severely obese adolescents undergoing bariatric surgery.
Methods:
We evaluated data from the Teen-Longitudinal Assessment of Bariatric Surgery (Teen-LABS) cohort, a prospective, multi-institutional study of adolescents (13-19 years) undergoing bariatric surgery. Abdominal pannus severity (graded 0-5) and excess skin symptoms were evaluated pre-operatively and for the first five years after bariatric surgery.
Results:
Among the 217 study participants, 198 (90%) had an abdominal pannus and 16 (7%) reported pannus related symptoms at the time of bariatric surgery. Preoperative symptoms included intertriginous infections (n=12, 75%), recurrent cellulitis (n=5, 31%), and superficial cutaneous ulcerations (n=1, 6%). Participants with a higher pannus grade pre-operatively experienced both a greater reduction in pannus severity (p<0.0001) and a higher incidence of pannus related symptoms (p=0.002) post-operatively. Changes in pannus severity occurred during the first 24 months after bariatric surgery; mean pannus severity remained unchanged beyond 24 months.
Conclusions:
Severely obese adolescents who undergo bariatric surgery frequently presented with an abdominal pannus at the time of surgery with associated symptoms. Higher pre-operative pannus grade is associated with more pannus related symptoms following surgery. Counseling about need for body contouring surgery should be considered in this group.
Keywords: excess skin, adolescent bariatric surgery, pannus symptoms
INTRODUCTION
Despite the numerous long-term health benefits associated with bariatric surgery, in adults a common consequence of surgically-induced massive weight loss is the development of excess skin and subcutaneous soft tissue. Specific concerns include the development and progression of dermatitis, fungal infections, and skin ulceration; these concerns affect nearly 30% of adults with redundant skin folds 1. Anatomic regions frequently affected include the breasts, arms, thighs, and buttock, with the abdomen the most frequently affected2. In addition to infectious and inflammatory skin issues, the development of excess skin after bariatric surgery impacts the ability to fit into clothing, sexual relationships, and quality of life1,3-5. As a result of these symptoms, 80% of adults desire body contouring surgery after bariatric surgery 1.
Little is known about excess skin and soft tissue problems in adolescents with severe obesity who elect to undergo bariatric surgery. Since skin elasticity decreases with age6, some surgeons have hypothesized that adolescents who undergo bariatric surgery are less susceptible than adults to development of excess skin and soft tissue-related complications. In contradiction to this hypothesis, however, adolescents who have undergone bariatric surgery appear to have a similar rate of subsequent body contouring procedures7, and describe a higher level of discomfort related to their excess skin compared to adults8. This contradiction highlights the need to describe the natural history of excess skin and soft tissue after bariatric surgery in adolescents. The goal of the present study was to examine the natural history of excess skin and its associated problems in adolescents with severe obesity before and after bariatric surgery. In addition, we sought to identify pre-operative risk factors for occurrence of excess skin related problems following bariatric surgery.
METHODS
Data for this analysis was derived from Teen-Longitudinal Assessment of Bariatric Surgery (Teen-LABS), a prospective observational study of obese adolescents (13-19 years of age) who underwent bariatric surgery between 2007-2012 across five centers in the United States. Study details are available at clinicaltrials.gov using the identifier NCT004743189. This study was approved by individual IRBs of each institution and independent data and safety monitoring board prior to study initiation. All participants underwent either vertical sleeve gastrectomy (VSG), Roux-en-Y gastric bypass (RYGB), or adjustable gastric banding (AGB). Participants who underwent body contouring surgery after bariatric surgery were excluded from this analysis (n=25); symptom development and weight changes among Teen-LABS participants receiving body contouring surgery has been described previously7 and these prevented were excluded from the present study because their body contouring surgery prevented description of the natural history of excess skin problems.
All participants were evaluated pre-operatively and at 6-, 12-, 24-, 36-, 48-, and 60-months following bariatric surgery. Trained study staff and clinical investigators collected anthropometric measurements at each visit; height, weight, waist circumference, sagittal abdominal diameter, and pannus severity. Pannus severity was categorized into six grades (0-5, Figure 1) based on skin and soft tissue morphology as well as overhang, using a previously described scale10. Participants also completed pannus-related symptoms questionnaires at each visit.
Figure 1:
Pannus Grading
Means and standard deviations were reported for age and body mass index (BMI), and counts and proportions were provided for gender, ethnicity, race, surgery type, excess skin problems, and pannus severities. The association between pre-operative pannus severity and BMI was tested using ordinal logistic regression adjusting for sex, waist circumference, and sagittal abdominal diameter. Pannus grades of 4 and 5 were grouped together due to sparse counts.
In the following analyses, time was modeled separately for the first 24 months and from 25-60 months post-surgery using either piece-wise linear terms in regressions or separate t-tests. The association between pre-operative pannus severity and pannus severity following surgery was tested with ordinal logistic regression adjusting for pre-operative BMI, sex, surgery type, and time. Additionally, change in pannus severity following surgery was evaluated on a continuous scale for interpretability; change in pannus severity over time was evaluated using a one-sample t-test for each pre-operative pannus severity using a false discovery rate adjustment. The presence of pannus symptoms following bariatric surgery was compared between the three pannus severity groups with logistic regression adjusting for BMI, sex, surgery type, and time. For the latter analysis, pannus grades were categorized into three groups to enhance clinical utility: small (grade 0 or 1), medium (grade 2 or 3), and large (4 or 5). Each multivariate analysis used a Laplace approximation with a random intercept for each participant and a robust covariance matrix (i.e. “sandwich” estimators). The threshold for determining statistical significance was set at p<0.05. Statistical analyses were performed in R (version 3.5.1) and SAS 9.4 software.
RESULTS
Pre-operative Characteristics
A total of 217 participants met the inclusion criteria. The majority of the cohort was female (76.0%), non-Hispanic (92.2%), and white (70.5%). The mean pre-operative BMI was 52.4 kg/m2 (SD 9.4). Among the 217 adolescents, 198 (90.3%) had an abdominal pannus (pannus severity ≥ 1, Table 1). A higher pre-operative BMI was associated with a more severe abdominal pannus after adjusting for waist circumference, sagittal abdominal diameter, and sex (p=0.0003). For every five kg/m2 increase in BMI, the odds of having a higher pannus severity were 1.8-fold greater (95% C.I. = 1.3, 2.4).
Table 1:
Pre-operative Characteristics
| Overall (n=217) |
|
|---|---|
| Sex | |
| Female | 165 (76.0%) |
| Male | 52 (24.0%) |
| Ethnicity | |
| Hispanic | 17 (7.8%) |
| Non-Hispanic | 200 (92.2%) |
| Race | |
| African American | 50 (23.0%) |
| American Indian | 1 (0.5%) |
| Asian | 1 (0.5%) |
| Multiple | 12 (5.5%) |
| White | 153 (70.5%) |
| Initial Surgery Type | |
| Gastric bypass | 143 (65.9%) |
| Laparoscopic adjustable gastric band | 14 (6.5%) |
| Sleeve gastrectomy | 60 (27.6%) |
| Pre-operative Age (years) | 16.7 (1.56) |
| Pre-operative BMI (kg/m2) | 52.4 (9.36) |
| Pre-operative Weight (kg) | 148.0 (30.9) |
| Pre-operative Pannus Symptoms | |
| No | 203 (92.7%) |
| Yes | 16 (7.3%) |
| Pre-operative Pannus severity | |
| 0 | 21 (9.7%) |
| 1 | 62 (28.6%) |
| 2 | 88 (40.6%) |
| 3 | 42 (19.4%) |
| 4 | 3 (1.4%) |
| 5 | 1 (0.5%) |
Legend: Categorical variables are presented with the number of patients (percent). Numerical variables are presented with the mean (standard deviation). BMI, body mass index.
Among the 217 participants, 16 (7.4%) experienced pannus symptoms pre-operatively. Out of the 16 participants who reported pre-operative symptoms, 12 (75%) had intertriginous infection, 5 (31.3%) had recurrent cellulitis, and 1 (6.3%) had a superficial ulceration. No participant reported deep ulceration, necrotizing fasciitis, or lymphedema pre-operatively. Examining symptom prevalence by pannus grade, 4.8% (1/21) of participants with a pannus grade of 0 had symptoms, 0.0% (0/62) with a pannus grade 1, 13.6% (12/88) with a pannus grade 2, 7.1% (3/42) with a pannus grade 3, 0.0% (0/4) with a pannus grade of 4 or 5 had symptoms.
Pannus and Excess Skin Symptom Characterization Over Time
Pre-operative pannus severity was associated with pannus severity over time (p<0.0001, using ordinal logistic regression treating pannus severity as an ordinal outcome). To explain this finding in more detail, we examined changes in pannus severity as a continuous value to aid in interpretability, using t-tests for comparisons rather than the difficult interpretation of odds ratios from ordinal logistic regression. Adolescents with a pannus severity of 0 (i.e. no abdominal pannus at the time of surgery) had a modest mean increase of 0.29 in pannus severity between surgery and 24 months (p=0.02). Adolescents with a pannus severity of 1 at the time of surgery had no significant change after surgery (p=0.15). Adolescents with a pannus severity of 2 or 3 at the time of surgery experienced a decrease in pannus severity of 0.99 and 1.38 on average, respectively, by 24 months (p<0.0001). Adolescents with a pannus severity of 4 or 5 at the time of surgery experienced an average decrease in pannus severity of 2.25 by 24 months (p=0.02). There was no significant change in mean pannus severity between 24 and 60 months in any group (Figure 2).
Figure 2:
Pannus Severity Over Time
The prevalence of pannus symptoms pre-operatively was 7.4% and post-operatively was 17%, so in total, 48 participants (22.1%) experienced pannus symptoms at least once before or within 5 years after metabolic and bariatric surgery (MBS). Most commonly, participants reported intertriginous infections (46 reports over the five years). Among the 16 adolescents with pre-operative excess skin related symptoms, five (31%) reported excess skin related symptoms following bariatric surgery. Among the 201 adolescents with no pre-operative excess skin symptoms, 32 (15.9%) experienced symptoms at least once after surgery. Symptom prevalence for individual study participants is reported in the Supplemental Table.
After adjusting for BMI, time, sex, and surgery type, post-operative pannus severity was associated with post-operative pannus symptoms (p=0.002). The odds of experiencing pannus symptoms at any time point were 76% lower on average (95% C.I. = 47% to 89% lower) for those with pannus severity of zero or one (small group) compared to those with a pannus severity of two or three (medium group, p=0.0004). Although not statistically significant, the odds of experiencing pannus symptoms at any time point were 81% lower on average (95% C.I. = 98% lower to 530% greater) for those with pannus severity of zero or one (small group) compared to those with a pannus severity of four or five (large group, p=0.41).
DISCUSSION
This study represents the first prospective evaluation of excess skin related issues in adolescents undergoing bariatric surgery. At the time of bariatric surgery, 90.3% of adolescents had an abdominal pannus and 7% suffered from excess skin related issues. Over the course of the five year study, nearly a quarter of adolescents reported symptoms at some point (pre- or post-operatively). We found that a higher post operative pannus severity was associated with a higher risk of post-operative pannus related symptoms on average.
In adults, pre-operative BMI and pannus severity have been shown to directly correlate with pannus severity after bariatric surgery11,12. Our findings align with these reports in that an increased BMI was associated with a greater abdominal pannus pre-operatively and preoperative pannus severity predicted post-operative pannus severity as well. We also observed that adolescents with a greater pre-operative pannus severity experienced a larger decrease in pannus severity compared to those with a lower pannus severity up until 24 months. After 24 months, pannus severity remained at that level at least out to five years. These results provide valuable information regarding the natural history of pannus changes and help to set expectations pre-operatively when adolescents and families inquire about expected long term changes to their bodies, especially related to excess skin. Previous studies have examined excess skin in adolescents after bariatric surgery have focused on the experience of the degree of excess skin and the discomfort associated with it, but have not examined objective measures of the degree or discomfort and how it changes over time post operatively13.
Most excess skin related symptoms occur because friction and moisture between redundant skin folds precipitates erythema and erosion, predisposing to bacterial and fungal infections. While the spectrum of reported skin problems is broad, 80-90% of obese adults experience skin issues prior to bariatric surgery14,15. These may be as simple as swelling, itching, discoloration, burning, and eczema, or more severe in 25% of adults including symptoms such as superficial ulcerations and fungal infections pre-operatively 16. As skin elasticity decreases with age, it may be reasonably assumed that adolescents would be protected against excess skin related issues that develop within redundant skin folds. On the contrary, we found that approximately adolescents experience excess skin problems with an almost identical frequency (22%) as adults (intertriginous infections, cellulitis, and ulceration). Consistent with our findings, Elander et al found that adolescents undergoing bariatric surgery experienced a greater degree of excess skin and discomfort related to excess skin compared to an adult cohort13.
In addition to skin-specific symptoms analyzed here, excess skin may have more generalized effects on obese individuals who have undergone a bariatric procedure. Among adults, a strong correlation between the amount of excess skin and the degree of patient dissatisfaction has also been reported 8,17-19. Staalesen et al. found that adolescents report similar or even worse excess skin related quality of life concerns after bariatric surgery13. Thus, in addition to skin-specific symptoms, the constellation of symptoms suggest that excess skin remains a problem after bariatric surgery. In a recent publication by our group, we found that those who had undergone panniculectomy were much more likely to have experienced pannus symptoms at baseline, and that resolution of excess skin related symptoms was reported by all adolescents who underwent body contouring surgery after bariatric surgery20. In the current study, we found that pannus severity stabilized by two years after bariatric surgery. Furthermore, most of the pannus grade change occurred by twelve months with only minor changes in pannus grade between year one and two. This is supported by our previous publication demonstrating that adolescents start to have BCS between year 1 and 2 post operatively20.
We acknowledge several limitations inherent in the study design. Although the number of study participants exceeded 200, few reported skin and soft tissue related problems, and thus this study may be underpowered to evaluate changes in prevalence of pannus symptoms over time, particularly in patient subgroups. Furthermore, the study cohort lacks ethnic diversity, which potentially limits generalizability of the findings. We did exclude adolescents who underwent body contouring surgery after bariatric surgery as all of their symptoms resolved which would have biased the analysis of symptoms and pannus severity after bariatric surgery. Lastly, excess skin issues were self-reported and thus there is a risk of recall bias, particularly as these were annual visits. The likely effect was report of more severe symptoms rather than mild ones as these were possibly more memorable to the subjects.
CONCLUSION
In conclusion, we describe the prevalence of abdominal pannus and pannus-related symptoms among adolescents undergoing bariatric surgery, and the change in pannus severity and symptoms following bariatric surgery. While the natural history of excess skin related problems is difficult to predict, adolescents with a higher pre-operative pannus severity are more susceptible and should be counseled appropriately.
Supplementary Material
Supplemental Table: Individual Post-Operative Pannus Symptoms
Highlights.
7% of adolescents reported pannus symptoms at the time of surgery
Higher preoperative pannus severity predicted greater pannus reduction post operatively and a higher incidence of symptoms
ACKNOWLEDGEMENTS
Research support was provided through the following grants: NIH UM1DK072493 and NIH UM1DK095710.
Footnotes
DISCLOSURES
The authors have nothing to disclose with the exception of Thomas Inge who is a consultant for Standard Bariatrics.
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Associated Data
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Supplementary Materials
Supplemental Table: Individual Post-Operative Pannus Symptoms