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The Impact of Autologous Breast Reconstruction on Body Mass Index Patterns in Breast Cancer Patients: A Propensity-Matched Analysis

Cho, Eugenia H. B.S.; Shammas, Ronnie L. B.S.; Glener, Adam D. B.S.; Greenup, Rachel A. M.D., M.P.H.; Hwang, E. Shelley M.D., M.P.H.; Hollenbeck, Scott T. M.D.

Plastic and Reconstructive Surgery: December 2017 - Volume 140 - Issue 6 - p 1121–1131
doi: 10.1097/PRS.0000000000003841
Breast: Original Articles
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Background: Weight gain is common in breast cancer patients and increases the risk of recurrence and mortality. The authors assessed the impact of autologous breast reconstruction on body mass index patterns after diagnosis in mastectomy patients.

Methods: Women undergoing therapeutic mastectomy at the authors’ institution from 2008 to 2010 were identified. Patients undergoing no breast reconstruction or autologous breast reconstruction were propensity-matched by age at diagnosis, baseline obesity, mastectomy laterality, and adjuvant therapies. Multivariable regression was used to estimate covariate associations with percentage body mass index change and percentage body mass index change greater than 5.0 percent at 1 to 4 years after diagnosis.

Results: Of 524 total patients, 80 propensity-matched pairs were identified. In multivariable regression, women undergoing immediate autologous breast reconstruction had reduced body mass index changes after diagnosis, compared with nonreconstruction patients, at 1 year (β = −5.25 percent; p < 0.01), 2 years (β = −8.78 percent; p < 0.01), and 3 years (β = −7.21 percent; p < 0.01). After 4 years, all autologous reconstruction was predictive of reduced body mass index changes (β = −3.54 percent; p = 0.02). Higher body mass index increases were observed among women who were leaner at diagnosis (p < 0.01 at 1 year) and received chemotherapy (p = 0.02 at 3 years; p = 0.04 at 4 years).

Conclusions: Women undergoing autologous breast reconstruction gained less weight after diagnosis than nonreconstruction patients. Normal baseline body mass index and chemotherapy were predictive of greater body mass index increases. These findings may guide targeted weight management strategies in high-risk patients to maximize survival rates.

CLINICAL QUESTION/LEVEL OF EVIDENCE: Therapeutic, III.

Durham, N.C.; and Philadelphia, Pa.

From the Divisions of Plastic and Reconstructive Surgery and Advanced Oncologic and Gastrointestinal Surgery, Duke University Medical Center; and the Department of Bioengineering, University of Pennsylvania.

Received for publication April 1, 2017; accepted July 6, 2017.

Disclosure: The authors have no financial interest to declare in relation to the content of this article.

A “Hot Topic Video” by Editor-in-Chief Rod J. Rohrich, M.D., accompanies this article. Go to PRSJournal.com and click on “Plastic Surgery Hot Topics” in the “Digital Media” tab to watch. On the iPad, tap on the Hot Topics icon.

Scott T. Hollenbeck, M.D., Division of Plastic and Reconstructive Surgery, Duke University Medical Center, Box 3945, Durham, N.C. 27710, scott.hollenbeck@duke.edu

Breast cancer is the second most common cancer diagnosis among women in the United States, accounting for more than 300,000 new cases and 40,000 deaths in 2016.1 Weight gain is commonly reported among breast cancer patients, with gains ranging from 2.0 to 6.0 kg in the first year after diagnosis.2–6 Consistent level I clinical evidence suggests that weight gain after breast cancer diagnosis is associated with a greater risk of recurrence,7,8 second primary breast cancer incidence,9 and breast cancer–specific7,10 and all-cause mortality.11,12 Postdiagnosis weight gain also increases the risk of obesity-related morbidity and may contribute to significant psychosocial distress in breast cancer survivors.13,14

Currently, it is unknown how autologous breast reconstruction impacts body weight in breast cancer patients requiring therapeutic mastectomy. Evidence shows that chemotherapy is the treatment factor most strongly associated with weight gain in breast cancer patients, which may be related to reduced physical activity4,15 or metabolic disturbances.16–18 In contrast, hormone therapy19–21 and radiation therapy22 do not appear to affect postdiagnosis weight. As weight gain strongly impacts patient survival, reconstructive surgeons should be cognizant of clinical risk factors for weight gain in mastectomy patients undergoing breast reconstruction. Many breast cancer patients appear to be inadequately informed of the risk of weight gain after diagnosis and express unmet needs for education and interventions for weight management.23,24 Notably, women who gain more than 5.0 percent of their weight in their first postdiagnosis year rarely return to their prediagnosis weight.16,19,22,25 Thus, identifying clinical predictors of weight gain in the early postdiagnosis years may improve patient risk stratification, oncologic risk counseling, and targeted recommendations to maximize patient survival. This institutional propensity-matched study evaluates the impact of autologous breast reconstruction on longitudinal postdiagnosis body mass index patterns to stratify the risk of weight gain among mastectomy patients.

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PATIENTS AND METHODS

After institutional review board approval, all women undergoing mastectomy for incident stage 0 to III breast cancer at Duke University Health System from 2008 to 2010 were identified. Patients were included if they underwent no breast reconstruction (mastectomy alone) or autologous breast reconstruction less than 12 months after mastectomy. Patient exclusion criteria included a history of cancer, time interval greater than 18 months from breast cancer diagnosis to breast reconstruction, and multimodal reconstruction using both autologous and implant-based methods.

Propensity score matching was performed to reduce the risk of selection bias in the receipt of autologous breast reconstruction in this study. Patients who underwent autologous breast reconstruction versus no breast reconstruction were matched 1:1 by a local optimal matching algorithm derived from the following factors: age at diagnosis (<45, 45 to 65, and >65 years), baseline obesity (body mass index ≥30.0 kg/m2), hypertension, mastectomy laterality, receipt of neoadjuvant or adjuvant chemotherapy, and hormone therapy (caliper = 0.001). These variables were selected a priori based on their association with having undergone autologous breast reconstruction and the study outcome (postdiagnosis body mass index change) as described.26

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Assessment of Body Mass Index Change

The primary outcome was percentage change in body mass index at 1, 2, 3, and 4 years ± 2 months after breast cancer diagnosis. These time points were examined to assess significant changes in body mass index and to allow sufficient time for weight stabilization after the completion of treatment. Body mass index was recorded as weight in kilograms per height in meters squared. Percentage body mass index change was calculated as follows: [(follow-up body mass index − baseline body mass index)/baseline body mass index] × 100. The secondary comparison was body mass index change as a binary outcome: percentage body mass index increase less than or greater than 5.0 percent. This cutoff of 5.0 percent for clinically significant body mass index increase was used based on previous reports examining associations of postdiagnosis weight gain and mortality.11,12,27 A 5.0 percent body mass index change is equivalent to a 5.0 percent weight change when height is assumed to be constant.

Baseline patient variables at diagnosis included age, race, body mass index, menopausal status, and the following comorbidities: obesity, hypertension, diabetes mellitus, hyperlipidemia, and reported tobacco use. Clinical breast cancer stage at diagnosis was coded according to the AJCC Cancer Staging Manual, 7th edition.28 Estrogen receptor and progesterone receptor status were categorized as follows: estrogen receptor–positive/progesterone receptor–positive (positive), estrogen receptor–negative/progesterone receptor–negative (negative), and estrogen receptor–positive/progesterone receptor–negative or estrogen receptor–negative/ progesterone receptor–positive (mixed). Treatment variables included the receipt of unilateral versus bilateral mastectomy, neoadjuvant or adjuvant chemotherapy, adjuvant hormone therapy, and postmastectomy radiation therapy. The primary study variable of interest was the receipt of autologous breast reconstruction less than 12 months after mastectomy and within 18 months after diagnosis, compared with mastectomy alone. Breast reconstruction was considered immediate if performed concurrent with the mastectomy procedure, and delayed if performed after the mastectomy procedure. Other reconstructive factors included laterality, reconstruction type, plication of the anterior rectus sheath as part of abdominal wall closure, and the time interval from cancer diagnosis to breast reconstruction. Patients undergoing reconstruction within 12 to 18 months after diagnosis were excluded from body mass index assessment at the 1-year time point.

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Statistical Analysis

Univariable analyses were performed using the Fisher’s exact or chi-square tests for categorical variables and the Mann-Whitney U and unpaired t tests for continuous variables. Multivariable regression models were used to estimate covariate associations with postdiagnosis percentage body mass index change (linear regression) and percentage body mass index increase greater than 5.0 percent (logistic regression). Significant covariates with values of p < 0.10 in univariable analyses were assessed for their independent predictive value using backward stepwise selection. Trends in percentage body mass index change after diagnosis were assessed by ordinary one-way analysis of variance and post hoc tests for trend. Trends in percentage body mass index increase greater than 5.0 percent after diagnosis were analyzed by chi-square tests for trend. All tests were two-sided, with statistical significance assigned to p < 0.05. Statistical analyses were performed using R version 3.3.1 (The R Foundation for Statistical Computing, Vienna, Austria).

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RESULTS

A total of 524 women underwent therapeutic mastectomy with autologous breast reconstruction (n = 85) or no reconstruction (n = 439) at a mean interval of 2.1 ± 2.5 months after breast cancer diagnosis. The baseline characteristics and matching factors in unmatched versus propensity-matched cohorts are listed in Table 1. In unmatched cohorts, nonreconstruction patients were older (p < 0.01), had a higher prevalence of hypertension (p = 0.01), were current or past smokers (p = 0.03), and were more commonly diagnosed with invasive rather than in situ breast cancer (p < 0.01), compared with the autologous breast reconstruction cohort. Compared with the nonreconstruction group, more autologous reconstruction patients had bilateral mastectomy (p = 0.01), neoadjuvant chemotherapy (p < 0.01), and hormone therapy (p < 0.01).

Table 1

Table 1

Postdiagnosis body mass index changes were assessed in propensity-matched cohorts of 80 nonreconstruction patients and 80 patients who underwent autologous breast reconstruction (mean follow-up, 3.9 ± 1.3 years). Of the breast reconstructions, 85 percent were abdominally based and included the deep inferior epigastric perforator (n = 23), muscle-sparing free transverse rectus abdominis myocutaneous (n = 36), pedicled transverse rectus abdominis myocutaneous (n = 5), and superficial inferior epigastric artery flaps (n = 4). Other flap choices included the latissimus dorsi (n = 10), transverse upper gracilis (n = 1), and superior gluteal artery perforator flaps (n = 1). Among all 160 patients, percentage increases in body mass index after diagnosis were observed at 1 year (mean, 1.6 ± 6.6 percent), 2 years (mean, 3.4 ± 8.0 percent), 3 years (mean, 3.1 ± 9.1 percent), and 4 years (mean, 4.1 ± 9.8 percent).

Table 2 shows the unadjusted associations of postdiagnosis percentage body mass index change with clinical, pathologic, and mastectomy characteristics. One year after diagnosis, percentage body mass index change differed by age (p = 0.03) and body mass index classification at diagnosis (p = 0.01). Table 3 shows the unadjusted associations of percentage body mass index change with treatment and reconstruction variables. Chemotherapy was associated with greater percentage body mass index increases at 3 to 4 years compared with controls, with significant increases seen with neoadjuvant chemotherapy starting at 2 years after diagnosis. In contrast, autologous breast reconstruction was associated with reduced percentage body mass index increases at 2 to 4 years compared with mastectomy alone, with modest increases seen in bilateral reconstruction patients at 2 to 3 years and body mass index decreases observed in immediate reconstruction patients over all 4 years after diagnosis. Postdiagnosis body mass index changes were not associated with abdominal versus non–abdominally based breast reconstructions or abdominal wall plication. Among abdominally based reconstructions, body mass index patterns did not differ according to flap type or reconstruction laterality. Figure 1, above and center shows the relative and absolute weight changes after diagnosis in the autologous reconstruction and nonreconstruction cohorts. Over the 4 years after diagnosis, women undergoing autologous breast reconstruction or no reconstruction gained a total of 1.5 ± 0.8 kg and 4.7 ± 1.0 kg, respectively.

Table 2

Table 2

Table 3

Table 3

Fig. 1

Fig. 1

In multivariable linear regression, immediate autologous breast reconstruction was independently predictive of reduced body mass index increases, compared with mastectomy alone, after 1 year (β = –5.25; 95 percent CI, –8.77 to –1.73; p < 0.01), 2 years (β = –8.78; 95 percent CI, –13.70 to –3.86; p < 0.01), and 3 years (β = –7.21; 95 percent CI, –12.61 to –1.81; p < 0.01) (Table 4). After 4 years, all autologous breast reconstruction irrespective of timing was independently predictive of a reduced percentage body mass index change (β = –3.54; 95 percent CI, –6.60 to –0.48; p = 0.02). Compared with overweight or obese women, women with a normal body mass index at diagnosis had a greater percentage body mass index change after 1 year (β = 3.70; 95 percent CI, 1.60 to 5.80; p < 0.01). Chemotherapy was independently predictive of greater percentage body mass index increases at 3 years (β = 3.93; 95 percent CI, 0.52 to 7.33; p = 0.02) and 4 years after diagnosis (β = 3.54; 95 percent CI, 0.07 to 7.02; p = 0.04).

Table 4

Table 4

Next, we examined postdiagnosis body mass index change using a cutoff greater than 5.0 percent for significant weight gain. In multivariable logistic regression, autologous reconstruction patients were 58 percent less likely than nonreconstruction patients to have a body mass index increase greater than 5.0 percent in their first postdiagnosis year (OR, 0.42; 95 percent CI, 0.19 to 0.94; p = 0.04) (Table 5). Age younger than 45 years at diagnosis was independently predictive of a body mass index increase greater than 5.0 percent in the first year (OR, 2.62; 95 percent CI, 1.17 to 5.88; p = 0.02). After 4 years, autologous reconstruction patients were 55 percent less likely than nonreconstruction patients to have a body mass index increase greater than 5.0 percent (OR, 0.45; 95 percent CI, 0.20 to 0.99; p = 0.04). Figure 1, below shows the rising prevalence of a body mass index increase greater than 5.0 percent following cancer diagnosis.

Table 5

Table 5

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DISCUSSION

This study is the first to evaluate the impact of autologous breast reconstruction on postdiagnosis body mass index changes to stratify the risk of weight gain among mastectomy patients. Overall, patients progressively gained weight over the 4 years after breast cancer diagnosis. We found that autologous breast reconstruction was independently predictive of reduced body mass index increases after diagnosis compared with mastectomy alone, with the strongest effects seen in patients who had immediate breast reconstruction. In the first postdiagnosis year, age-matched autologous breast reconstruction patients were 58 percent less likely than nonreconstruction patients to gain over 5.0 percent of their body mass index, and this difference persisted after 4 years. Independently, body mass index increases were higher among women who were leaner and younger at diagnosis and received chemotherapy. Our study suggests that autologous breast reconstruction positively affects weight management in mastectomy patients. Our findings may help clinicians identify breast cancer patients at high risk for weight gain and guide targeted strategies to optimize cancer survivorship.

Overall, our study shows a pattern of progressive weight gain after diagnosis among mastectomy patients, rising from 1.6 percent body mass index at 1 year to 4.1 percent body mass index at 4 years. In addition, the prevalence of a body mass index gain greater than 5.0 percent increased longitudinally, reaching 42 percent of all patients by 4 years after diagnosis. Weight gain of 5.0 percent or higher within 4 years of a new breast cancer diagnosis is clinically significant because it is associated with increased hazards of relapse,29 diagnosis of a second primary breast cancer,9 breast cancer–specific mortality,11 and all-cause mortality.12 Furthermore, weight gain of 10.0 percent or higher in this postdiagnosis period confers a significantly heightened risk of all-cause mortality among breast cancer survivors, compared with weight gains of 5.0 to 10.0 percent.11,12,30 Despite mounting evidence, however, many breast cancer patients appear to be inadequately informed of these risks and express unmet needs for guidance on weight management.23,24 Strikingly, women who gain more than 5.0 percent weight in their first postdiagnosis year rarely return to their original weight.16,19,22,25 Collectively, these findings underscore the importance of identifying predictors of weight gain in the early postdiagnosis years to guide clinical recommendations for weight gain prevention.

Women who received autologous breast reconstruction had a 55 percent reduced risk of gaining greater than 5.0 percent body mass index 4 years after diagnosis, which has positive implications for overall health and breast cancer survivorship. Autologous reconstruction patients gained approximately 0.4 kg each year after diagnosis (versus 1.4 kg/year in nonreconstruction patients), which is comparable to the normal weight gain rate of 0.5 kg/year in cancer-free midlife women.31,32 Although this study did not examine behavioral and lifestyle factors, weight management among breast cancer survivors is linked to their psychosocial adjustment and coping strategies.33 Most women undergoing mastectomy experience some level of psychosocial distress over the course of their cancer treatment. This psychological response to mastectomy is highly individual and may include anxiety34; perceived loss of femininity35; and interpersonal, sexual, and marital dysfunction.36 In general, breast reconstructive surgery has an important role in managing breast cancer in these patients, with significant benefits in restoring psychosocial and sexual health.37,38 Many women who undergo autologous breast reconstruction report improved levels of satisfaction and psychosocial well-being as early as 3 weeks after surgery,39 which may in turn affect their weight patterns. Notably, we found that postdiagnosis body mass index increases were markedly reduced among women who received immediate rather than delayed autologous breast reconstruction, compared with mastectomy alone. Immediate autologous breast reconstruction may provide earlier improvements in vitality and body image and facilitate a quicker return to physical activity,37,40 thereby limiting weight gain.

Increases in body mass index were higher among women who were younger than 45 years and closer to ideal body mass index at diagnosis, and who received chemotherapy. Women within normal body mass index range at diagnosis (≤25.0 kg/m2) gained 3.7 percent body mass index relative to overweight or obese women in their first postdiagnosis year, adjusted for the receipt of immediate autologous reconstruction. Our findings are supported by level I prospective evidence showing an increased risk of weight gain41 and a stronger association of weight gain with mortality12 among women with a baseline body mass index under 25.0 kg/m2. Breast cancer patients with a higher body mass index are less likely to gain weight, which differs from cancer-free midlife women for whom higher body mass index is associated with weight gain.32 In addition, we found that the receipt of chemotherapy was independently predictive of greater body mass index increases in the first 2 to 4 years after diagnosis. Evidence indicates that chemotherapy is strongly associated with weight gain in breast cancer patients, which may be related to reduced physical activity14,15 and/or metabolic disturbances including insulin resistance16–18 and increased inflammation.42,43 Collectively, our results suggest that mastectomy patients who are younger or leaner at diagnosis, or receive chemotherapy, may be at higher risk for weight gain. Future investigation is warranted to determine the overall survival benefit of targeted interventions for weight maintenance or loss in this population.

Current guidelines for weight management are derived from the American Cancer Society report on nutrition and physical activity in cancer survivors, which was published in 200644 and updated in 2012.45 In these reports, cancer patients are advised to ask their physician for a referral for nutritional assessment and guidance as soon as possible after diagnosis. Cancer care providers should encourage healthy lifestyle choices and then refer patients to registered dieticians who are certified in cancer supportive care. Our findings have important implications for multidisciplinary breast cancer care, where weight management strategies are often focused on patients who are overweight or obese. First, mastectomy patients who are younger, leaner, and/or receive chemotherapy should be referred to oncology nutritional support services as early as possible and be strongly encouraged to make informed lifestyle choices to improve their survival rates. In addition, mastectomy patients who do not receive breast reconstruction may be at even higher risk of gaining weight and may therefore benefit from tailored weight management support. In 2006, the Institute of Medicine issued a report recommending that every breast cancer patient receive an individualized survivorship care plan, which includes a treatment summary and provides guidelines for monitoring cancer, managing late treatment effects, and promoting overall physical and psychosocial health.46–48 As weight gain impacts patient survival, reconstructive surgeons should be cognizant of the clinical prevalence of weight gain and provide evidence-based recommendations to optimize survivorship in high-risk individuals. Our study provides new insights to guide clinical recommendations in women undergoing autologous breast reconstruction, including targeted strategies to prevent weight gain as part of the survivorship care plan.

This retrospective study has limitations. Although propensity-score matching was used to reduce the risk of selection bias, women who choose to undergo autologous breast reconstruction may be more body image conscious and therefore more motivated to maintain their weight. As our study did not survey patients before cancer diagnosis, we were unable to account for these potential baseline psychosocial differences between the two cohorts. Second, we did not control for mastectomy specimen weight versus flap weight, which may affect the reported associations with body mass index changes. In addition, this study did not evaluate important drivers of weight gain, such as physical activity and treatment-related fatigue. Thus, we are unable to draw conclusions on why women who receive autologous breast reconstruction gain less weight, compared with nonreconstruction patients. Finally, our findings are limited to women undergoing autologous breast reconstruction, and inferences cannot be drawn on the effect of implant-based reconstruction on body mass index patterns. Further study on weight changes in patients undergoing implant-based reconstruction is needed to guide risk-reduction strategies and optimize survivorship among all mastectomy patients who undergo breast reconstruction.

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CONCLUSIONS

This propensity-matched study is the first to assess longitudinal body mass index patterns after breast cancer diagnosis among mastectomy patients. Although weight gain was common overall, women who underwent autologous breast reconstruction gained significantly less weight after diagnosis than nonreconstruction patients. Populations at greater risk for postdiagnosis weight gain included women who were younger and leaner at diagnosis and received chemotherapy. Our findings can be used to identify high-risk patients, enhance oncologic risk counseling, and guide targeted weight management strategies to maximize patient survival rates.

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ACKNOWLEDGMENTS

The authors thank the following individuals who contributed to the management of patients in this study: Michael R. Zenn, M.D., M.B.A., and Gregory S. Georgiade, M.D. The authors also thank Jennifer Gallagher, B.A., for assistance in the preparation of the institutional review board for this work.

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