Objective
The purpose of this study was to describe the acceptability of bariatric referrals when offered by gynecologic oncologists to women with a history of complex atypical hyperplasia or early-stage endometrial cancer and to detail compliance with referrals and weight loss attempts that are initiated 3 months after the referral.
Study Design
Obese women with complex atypical hyperplasia or early-stage endometrial cancer were approached for inclusion in this prospective cohort study. Those women who were not in the care of a bariatric specialist were offered a medical referral with or without a surgical referral. A survey was administered at inclusion and after 3 months.
Results
Of 121 women who were approached, 106 women were consented. Women reported that it was acceptable for their gynecologic oncologist to discuss weight loss (91.09%) and that a 10% loss of body weight would be beneficial (86.14%). Six women were already in the care of a bariatric specialist. Of the remaining 100 women, 43 accepted a referral: 35 of 100 medical and 8 of 66 surgical referrals that were offered. At 3 months, 17 women complied with a referral (16 medical and 1 surgical), and 59 women had initiated any weight loss attempt. On multivariate analysis, a higher initial weight ( P = .0403), Charlson Comorbidity Index ≥5 ( P = .0278), and shorter time from surgery to bariatric referral ( P = .0338) predicted acceptance of a referral.
Conclusion
Weight-loss counseling is well received by these women. After being offered bariatric referral, only 17% comply, but most women (59%) subsequently initiate a weight loss attempt. Referrals should be offered early in the course of cancer care to maximize acceptance.
More than two-thirds of endometrial cancer survivors are obese. Despite excellent cancer-specific outcomes, survivors of early-stage endometrial cancer experience poor general health outcomes and high mortality rates because of obesity-related comorbidities. Over time, these women are more likely to die of cardiovascular disease than any other cause, including cancer. Gynecologic oncologists desire to address obesity but report having received insufficient training. Cancer survivors confirm that gynecologic oncologists rarely and inadequately address the issue.
The Society of Gynecologic Oncology has joined ranks with other large medical organizations in calling on providers to address obesity actively with cancer survivors. With aggressive nutritional and medical treatment obese endometrial cancer survivors can lose weight. Bariatric surgery is associated with dramatic weight loss outcomes but is under-studied in this population. Gynecologic oncologists express interest in offering medical and surgical bariatric referrals to obese cancer survivors. However, the acceptability of and compliance with these referrals has not been described in this setting.
Gynecologic oncologists are poised uniquely to harness the ‘teachable moment’ provided by a cancer diagnosis and have liberal access to women during the survivorship period, which is a time when women are motivated but experience distinct challenges to healthy weight loss. In this prospective cohort study, we offered medical and surgical bariatric referrals to women with complex atypical hyperplasia or stage I or II endometrioid endometrial cancers. We describe the acceptability of and compliance with these referrals and detail weight loss attempts that are initiated within 3 months after the bariatric referral is offered. Additionally, we explore factors that are associated with the acceptability of and compliance with referrals and the initiation of weight loss attempts.
Materials and Methods
Institutional review board approval was obtained through the Cleveland Clinic (protocol # 13-1528) for this prospective intervention cohort study. Women were approached between December 2013 and September 2014 during gynecologic oncology clinic visits at Cleveland Clinic Main Campus, Hillcrest and Fairview Hospitals. Inclusion criteria were a history of complex atypical hyperplasia or a stage I or II endometrioid adenocarcinoma of the endometrium, 18-65 years old, a body mass index (BMI) ≥30 kg/m 2 , and agreement of their gynecologic oncologist that they could be approached for enrollment. Exclusion criteria included stage III or IV, recurrent or progressive cancer, nonendometrioid histologic condition, poorly controlled psychiatric or medical conditions that contraindicate weight loss interventions, or an active second primary malignancy.
One of the authors (A.J.) identified potential subjects for recruitment in advance based on the inclusion and exclusion criteria that were mentioned earlier to minimize bias. The author and, occasionally research nurses at the remote sites, obtained consent and coordinated bariatric referrals, administered surveys, and collected data. Women who were already in the care of a bariatric specialist were surveyed but were not offered a referral. All other women were offered a medical referral with a bariatrician who specializes in medically supervised weight loss. Otherwise, women were offered a surgical referral if they met National Institutes of Health criteria for a bariatric surgery referral: BMI ≥40 kg/m 2 or ≥35 kg/m 2 with an obesity-related comorbidity.
After informed consent was obtained, women were asked to fill out a questionnaire. Three items asked women to rate their baseline beliefs regarding the acceptability of a bariatric referral, the health benefits of modest weight loss, and their relationship with their gynecologic oncologist on a Likert scale ( Figure 1 ). Baseline quality-of-life, function and symptoms were assessed with the validated European Organisation for Research and Treatment of Cancer Quality of Life Questionnaires, both the 30-item questionnaire (EORTC QLQ-30, version 3) and the endometrial cancer module. These questionnaires were administered and scored in accordance with published guidelines. Women who declined a referral were asked to provide reasons. A priori, it was decided that these reasons would be categorized as fear of surgery, financial or insurance coverage concerns, distance from hospital, wanting to attempt weight loss independently, or not desiring weight loss.
A chart review was performed to collect baseline demographics that included age and race. Distance from the hospital in minutes without traffic and in miles was calculated between their home address and the hospital with the use of google-maps. Median household income was estimated with the use of their residential zip code and 2010 US Census Data. Height and weight were collected, and medical comorbidities were recorded with the use of the data from their clinic visit; BMI and Charlson Comorbidity Index (CCI) score were calculated subsequently. Tumor histologic condition, stage, treatment, and postoperative complications were recorded. Timing between intervention and diagnosis, surgery, and last treatment (surgery, chemotherapy, hormonal therapy, or radiation therapy) was calculated in days to the date the referral was offered; if treatment was ongoing, zero days were considered to have lapsed.
Three months after referral, women were contacted with an email or phone survey. Women who did not initiate a weight loss attempt were asked to identify barriers to the initiation of changes. A chart review verified compliance with bariatric referrals, defined as attending a visit with the bariatric specialist. Women who did not respond to the 3-month follow-up survey or did not have any record of compliance with a referral or initiation of weight loss attempts on chart review were considered to have not initiated a weight loss attempt.
We planned to describe our findings after 100 women were offered referrals. Study data were collected and managed with the REDCap electronic data capture tools (Vanderbilt, Nashville, TN). Statistical analysis was performed using JMP (version 10.0.2d1; SAS Institute Inc, Cary NC). Univariate analysis was performed for a relationship between demographic, treatment variables, and EORTC scores with acceptance of a referral, compliance with a referral, and initiation of a weight loss attempt. Associations between categoric covariates were assessed with χ 2 tests. Group differences in means of continuous measures were evaluated with Student t tests. In addition, outcomes that were associated with continuous independent variables were compared with the use of outcomes for 1st and 4th quartiles with χ 2 tests. Multivariate logistic regression models were used to assess for an association between demographic, treatment variables, and EORTC scores with acceptance of a referral, compliance with a referral, and initiation of a weight loss attempt. Confounders that were associated significantly with an outcome in the univariate model ( P < .05) were identified and included in the multivariate model. All tests were 2-tailed and were considered significant at a probability value of < .05.
Results
The recruitment process is detailed in Figure 2 . We approached 121 women: 14 declined, and 1 who initially consented later withdrew her consent, citing other health concerns. One hundred one women completed their initial surveys; Figure 1 gives those results. Most of the women believed that a 10% weight loss would be beneficial, that it is appropriate for their gynecologic oncologist to address weight loss, and that their gynecologic oncologist cared about their overall health.
Of the 106 women who agreed to participate, 6 were already in the care of a weight loss specialist: 3 had bariatric surgery within the past year, 2 were seeing a medical weight loss expert, and 1 was seeing a nutritionist and her primary care physician for weight loss. The remaining 100 women were offered referrals ( Figure 3 ). All 100 women were offered medical referrals; 66 women were qualified for and were also offered surgical referrals. Forty-three women accepted a referral: 35 medical (35%) and 8 surgical (12%). Demographics and cancer staging and treatment information for the 100 women who were offered referrals are detailed in Table 1 . Median age was 57 years (95% CI, 28.68–65.00), weight 242.5 lb (95% CI, 168.31–421.13), and BMI was 40.87 kg/m 2 (95% CI, 30.14–65.10). Eight women had complex atypical hyperplasia, and 92 women had a history of endometrial cancer.
Demographic, cancer, and treatment variables | Measurement |
---|---|
Age, y a | 57 (28.68–65) |
Race, n (%) | |
Black | 12 (12.00) |
White | 88 (88.00) |
Distance from hospital a | |
Miles | 29.45 (3.1–159.8) |
Driving without traffic, m | 36 (10.05–153.83) |
Median household income, $ a,b | 48,810 (25,986.4–80,809.7) |
Weight at inclusion, lb a | 242.5 (168.31–421.13) |
Body mass index, kg/m 2 a | 40.87 (30.14–65.10) |
Charlson Comorbidity Index score a | 4 (2–7) |
Diabetes mellitus, n (%) | 37 (37) |
Hypertension, n (%) | 57 (57) |
Disease, n (%) | |
Complex atypical hyperplasia | 8 (8.00) |
Endometrial cancer | 92 (92.00) |
Stage | |
IA | 78 (78.00) |
IB | 9 (9.00) |
II | 5 (5.00) |
Grade | |
1 | 65 (65.00) |
2 | 24 (24.00) |
3 | 3 (3.00) |
Treatment, n (%) | |
Treated without surgery | 7 (7.00) |
Surgically treated | 93 (93.00) |
Postoperative complications | 21 (21.00) |
Adjuvant therapy | 28 (28.00) |
Chemotherapy | 6 (6.00) |
Radiation therapy | 23 (23.00) |
Combination chemotherapy and radiation | 4 (4.00) |
Hormonal therapy | 4 (4.00) |
At the time of approach, d a | |
Diagnosis | 399 (22.15–1989.75) |
Last therapy | 344.5 (0–1896.47) |
Surgery | 389.5 (12.33–1951.15) |
a Data are given as mean (95% confidence interval)
Fifty-seven women declined a bariatric referral. Of the 66 women who were offered surgical referral, 58 declined and provided the following reasons: 31 (53.45%) reported fear of additional surgery; 13 (22.41%) reported living too far away; 13 (22.41%) reported financial or insurance coverage concerns, and 20 (34.48%) wanted to attempt weight loss independently. Of the 57 women who declined medical referrals, 18 (31.58%) reported that they lived too far away; 13 (22.81%) reported financial or insurance coverage concerns, and 30 (52.63%) reported that they wanted to pursue weight loss independently. No one expressed that they did not want to lose weight.
Three months after being offered a referral, 78 women completed the follow-up survey; the charts were reviewed for all 100 women. Of the 59 women who initiated weight loss attempts, 17 complied with bariatric referrals: 16 medical and 1 surgical. Six women initiated a commercial weight loss program (1 of these 6 women had also complied with a medical referral). One woman reported attending community nutrition classes. Thirty-six women reported initiating self-guided weight loss attempts: 18 women dieted exclusively; 7 women exclusively exercised, and 11 women did both.
Forty-one women had not initiated weight loss attempts: 19 confirmed on survey and chart review; 22 based on chart review alone. Of the 19 women who confirmed that they had done “nothing” to try to lose weight on the survey, 17 women provided reasons, with some women providing >1 reason. Reasons that women cited for not initiating a weight loss attempt included being overwhelmed by other health issues (8 women) or nonhealth-related issues (6 women), being unable to afford weight loss programs (5 women), and not believing that weight loss would improve their health (1 woman). None reported that they did not want to lose weight.
Table 2 provides univariate analysis of factors that were associated with the acceptance of a referral when it was offered. Women were more likely to accept a referral if they had a higher BMI ( P = .035), a higher CCI ( P = .025), a lower estimated median household income ( P = .0302), and had been approached more recently after surgery ( P = .0030). In a comparison of the 1st and 4th quartiles, 54.55% of women who were approached within 26 days of surgery vs 8.70% of women who were approached >967 days after surgery accepted a referral ( P = .0006). Women were more likely to accept a referral when approached within the first year rather than more than a year after diagnosis (46.67% vs 34.55%; P = .0586). Higher numbness and tingling EORTC symptom scores were associated with acceptance of a referral ( P = .0356). On further analysis, 21 of 37 women with diabetes mellitus (56.76%) accepted a bariatric referral compared with 22 of 62 women who did not have diabetes mellitus (34.92%; P = .0332); women with diabetes mellitus did report higher numbness and tingling scores, but this did not reach statistical significance (27.45% vs 20.68%; P = .2965).
Factor | Measure | ||
---|---|---|---|
Accepted | Declined | P value | |
Age a,b | 55.23 | 54.63 | .7411 |
Race, n (%) | |||
Black (n = 12) | 6 (50.00) | 6 (50) | .6031 |
White (n = 88) | 37 (42.05) | 51 (57.96) | |
Distance b | |||
Miles a | 43.30 | 42.22 | .9330 |
Minutes a | 48.72 | 48.86 | .9900 |
Estimated household income, $ a,b,c | 47,977.2 | 53,823.6 | .0302 |
Baseline weight, lb a,b | 269.62 | 239.55 | .0204 |
BMI in kg/m 2 a,b | 44.54 | 40.54 | .0352 |
Charlson Comorbidity Index a,b | 4.14 | 3.56 | .0252 |
<5 (n = 76), n (%) | 26 (34.21) | 50 (62.79) | .0015 |
≥5 (n = 24), n (%) | 17 (70.83) | 7 (29.17) | |
Disease, n (%) | |||
Complex atypical hyperplasia (n = 8) | 3 (37.50) | 5 (62.50) | .7418 |
Endometrial cancer (n = 92) | 40 (43.48) | 52 (56.52) | |
Treatment, n (%) | |||
Surgical (n = 93) | 39 (41.94) | 54 (58.06) | .4360 |
Nonsurgical (n = 7) | 4 (57.14) | 3 (42.86) | |
Postoperative complications (n = 21), n (%) | 12 (57.14) | 9 (42.86) | .9226 |
Minimally invasive surgical staging (n = 70), n (%) | 27 (38.57) | 42 (61.43) | .2536 |
Received adjuvant therapy (n = 28), n (%) | 12 (42.86) | 16 (57.14) | .9059 |
Treatment status when offered referral, n (%) | |||
Treatment ongoing (n = 16) | 7 (43.75) | 9 (56.25) | .9473 |
Treatment completed (n = 84) | 36 (42.86) | 48 (57.14) | |
Time from diagnosis when offered referral, d a b | 567.81 | 654.97 | .6578 |
<1 y (n = 45), n (%) | 21 (46.67) | 24 (53.33) | .0586 |
≥1 y (n = 55), n (%) | 19 (34.55) | 36 (65.45) | |
Time from surgery when offered referral, d a,b | 363.97 | 753.70 | .0030 |
<1 y (n = 43), n (%) | 22 (51.16) | 21 (48.84) | .1102 |
≥1 y (n = 49), n (%) | 17 (34.69) | 32 (65.31) | |
European Organization for Research and Treatment of Cancer Quality of Life and endometrial cancer module scores b | |||
Global health status, quality of life | 67.1 | 72.92 | .2490 |
Physical functioning | 79.66 | 82.64 | .4821 |
Role functioning | 80.77 | 84.59 | .4857 |
Emotional functioning | 70.00 | 77.56 | .1081 |
Cognitive functioning | 82.92 | 87.50 | .2128 |
Social functioning | 83.33 | 83.98 | .8923 |
Fatigue | 34.44 | 27.46 | .1559 |
Nausea and vomiting | 6.41 | 5.13 | .6461 |
Pain | 29.17 | 24.84 | .4671 |
Dyspnea | 19.66 | 12.84 | .2423 |
Insomnia | 29.91 | 21.15 | .1546 |
Appetite loss | 11.11 | 12.17 | .8211 |
Constipation | 11.11 | 13.46 | .6040 |
Diarrhea | 10.83 | 7.05 | .2935 |
Financial difficulties | 22.50 | 24.84 | .7104 |
Sexual interest | 75.24 | 66.67 | .1410 |
Sexual activity | 86.28 | 81.33 | .3314 |
Sexual enjoyment | 53.33 | 45.24 | .4583 |
Lymphedema | 27.08 | 18.59 | .1529 |
Urologic symptoms | 17.29 | 17.41 | .9721 |
Gastrointestinal symptoms | 13.38 | 11.80 | .5434 |
Poor body image | 26.75 | 21.07 | .3663 |
Sexual and vaginal problems | 25.92 | 23.88 | .8033 |
Pain in back and pelvis | 28.33 | 28.20 | .9828 |
Tingling numbness | 30.83 | 17.30 | .0356 |
Muscular pain | 40.83 | 30.22 | .3364 |
Hair loss | 16.67 | 13.07 | .4946 |
Taste change | 7.69 | 5.13 | .5168 |