Abstract
Obesity has long been associated with endometrial cancer. However, there is a paucity of studies addressing the impact of morbid obesity in type II endometrial cancer on oncologic and surgical outcomes. In this study, the author retrospectively compared morbid to non-morbid obese in clinico-epidemiologic, surgical, and oncologic outcomes. Both groups were comparable as regards all clinico-epidemiologic parameters. Vaginal involvement, survival, and recurrence were also comparable between the 2 groups. Para-aortic adenopathy and treatment with preoperative therapy were the only significant predictors of DFS. Surgery is feasible with equivalent complications and oncologic outcomes in morbidly obese patients with type II endometrial cancer.
Keywords: Endometrial cancer, Hysterectomy, Obesity Non-endometrioid carcinoma
Background
Obesity is one of the most common risk factors in multiple diseases worldwide as type 2 diabetes, hypertension, and several cancers [1]. Endometrial cancer is one of the most commonly associated cancers with obesity [1]. Several studies have discussed the relation between the presence of obesity and the increased risk of endometrial cancer [2–4] and as surgery is considered the gold standard treatment of endometrial cancer, obesity is usually a challenge in such surgeries. [5, 6]
Endometrial cancer had been traditionally classified into type I and type II according to clinical and histopathologic differences [7–9]. Type I is usually hormonal dependent, grade 1 or 2 endometrioid histology with a favourable prognosis. On the other hand, type II is usually hormonal independent with a worse prognosis, including high-grade endometrioid, clear cell, serous, and carcinosarcomas [10–12]. While the relation between obesity and type I endometrial cancer had been well established for decades [13], several studies had also linked the risk of developing type II endometrial cancer with obesity. [14–16].
Egypt is one of the most affected countries by the prevalence of obesity, it was reported that about 35% of adult Egyptians are suffering from obesity which is one of the highest rates around the world. Also, about 10% of Egyptian children are considered to be overweight [17]. Hereby in this study, we discuss the impact of morbid obesity upon the outcomes of type II endometrial cancer patients in our institute.
Patients and Methods
Patient Cohort and Study Design
This is a retrospective cohort study of patients who had been surgically treated at an oncology centre for type II endometrial cancer. A total of 62 patients was retrieved in the period from 1/1/2014 to 1/1/2019. The basic epidemiologic and clinicopathologic data were displayed; thereafter, the patients were arranged on two arms with a cutoff point BMI = 40 kg/m2. The two arms were compared regarding epidemiologic, clinicopathologic criteria, and outcomes (surgical and oncological). In addition, a survey for the factors predicting overall and disease-free survival was contemplated.
Statistical Analysis
The data of these patients were analysed, and statistical values were obtained using SPSS version 22 (Chicago, IL). Continuous variables are presented as mean when symmetrical or median and range when asymmetrical. Categorical variables are presented as proportions. Bivariate analysis was done using the chi-square test and Fischer’s exact test. Survival analysis was done using the Kaplan–Meier curve and significance determined by log-rank test. P value < 0.05 was considered significant.
Results
Sixty-two patients were retrieved. The mean age of the studied population was 64.7 ± 6.8, and the mean BMI was 36.7 ± 7.2 kg/m2. Only 9 patients had BMI < 30 kg/m2. The commonest pathologic type was high-grade endometrioid, followed by serous, carcinosarcoma, and lastly clear cell carcinoma. Most of the patients were in early FIGO stage I (26 cases). Neoadjuvant chemotherapy was used in a minority of patients (10 cases) due to locally advanced diseases deemed not candidates for surgery. Most of the surgeries were done using an open technique (49 cases, 83.1%), and 4 patients (6.5%) underwent non-resectional surgery (i.e. an open biopsy was done only for widely spread disease on exploration). Another 4 patients (6.5%) received a subtotal hysterectomy initially outside our hospital by general gynaecologists and were further treated with adjuvant radiation therapy. 30.6% of the patients received complete surgical staging defined as TAH, BSO, omental biopsy, and bilateral pelvic lymphadenectomy. Regarding lymph node dissection (LND), 46.7% of the enrolled patients underwent LND, either pelvic LND only (26.7%) or pelvic and para-aortic (20%). Surgical complications occurred in 16 cases (4 intraoperative and the rest postoperative). Adjuvant therapy was given in 43 patients. Recurrence occurred in a nearly fifth of the patients (12 cases) (Table 1).
Table 1.
Basic clinico-epidemiologic and pathologic characters of the studied patients
| Parameter | Value |
|---|---|
| Age mean +/- SD | 64.7 ± 6.8 years |
| BMI mean +/- SD | 36.7 ± 7.2 kg/m2 |
| Presenting complaint* | |
| Vaginal bleeding | 55 (88.7%) |
| Abdominal symptoms | 4 (6.4%) |
| Vaginal bleeding and abdominal symptoms | 1 (1.6%) |
| Abdominal and urologic symptoms | 1 (1.6%) |
| Approach* | |
| Laparotomy | 49 (79%) |
| Laparoscopy | 10 (16.1%) |
| Laparoscopy | |
| Converted | 12/22 (54.5%) |
| Completed | 10/22 (45.5%) |
| Pathologic type | |
| Serous carcinoma | 18 (29%) |
| Clear cell carcinoma | 6 (9.7%) |
| High-grade endometrioid carcinoma | 21 (33.9%) |
| Carcinosarcoma | 17 (27.4%) |
| Neoadjuvant chemotherapy | |
| No | 52 (83.9%) |
| Yes | 10 (16.1%) |
| Surgery | |
| Total abdominal hysterectomy & bilateral salpingoophrectomy (TAHBSO) | 33 (53.2%) |
| TAHBSO and omentectomy | 2 (3.2%) |
| Complete surgical staging | 19 (30.6%) |
| Subtotal hysterectomy | 4 (6.5%) |
| Non-resectional surgery | 4 (6.5%) |
| Lymphadenectomy | |
| No | 32 (51.6%) |
| Pelvic | 16 (25.8%) |
| Pelvic and para-aortic | 12 (19.3%) |
| FIGO staging* | |
| IA | 14 (22.6%) |
| IB | 12 (19.3%) |
| II | 5 (8.1%) |
| IIIA | 3 (4.8%) |
| IIIB | 2 (3.2%) |
| IIIC | 6 (9.7%) |
| IVB | 6 (9.7%) |
| Operative time median (range) | 180 (60–420) min |
| Blood loss median (range) | 400 (50–500) ml |
| Hospital stay median (range) | 3 (0–19) days |
| Intraoperative complications* | |
| No | 57 (91.9%) |
| Yes | 4 (6.4%) |
| Postoperative complications* | |
| Yes | 13 (21%) |
| No | 34 (54.8%) |
| Adjuvant therapy* | |
| No | 11 (17.7%) |
| Yes | 43 (69.3%) |
| Recurrence* | |
| No | 41 (66.1%) |
| Yes | 12 (19.3%) |
| • Local recurrence | 5/12 (45.5%) |
| • Nodal recurrence | 2/12 (18.2%) |
| • Distant recurrence | 2/12 (18.2%) |
| • Local and distant recurrence | 3/12 (27.3%) |
| Time to recurrence median (range) | 14 (1–26) months |
*Variables contain some missing data
Excluding patients that received non-resectional surgery and those with no recorded BMI, 42 patients were arranged in two arms according to BMI < 40 or BMI ≥ 40 kg/m2. There was no significant difference between the two groups in epidemiologic and clinicopathologic parameters. Regarding the surgical outcome (complications, nodal status, recurrence, and survival), they were comparable between the 2 groups (Table 2).
Table 2.
Comparison of non-morbid obese and morbid obese patients regarding pathologic data and surgical and oncological outcomes
| Parameter | Non-morbid obese (28 patients) | Morbid obese (14 patients) | P value |
|---|---|---|---|
| Age mean ± SD | 64.1 ± 7.3 years | 64.6 ± 5.5 years | .8 |
| Co-morbidities | .7 | ||
| No | 6 (21.4%) | 2 (14.3%) | |
| Yes | 22 (78.6%) | 12 (85.7%) | |
| Approach* | 1 | ||
| Laparotomy | 22 (78.6%) | 11 (78.6%) | |
| Laparoscopy | 5 (17.9%) | 3 (11.4%) | |
| Laparoscopic conversion | 1 | ||
| No | 5/11 (45.5%) | 3/6 (50%) | |
| Yes | 6/11 (54.5%) | 3/6 (50%) | |
| Pathologic type | .6 | ||
| Serous carcinoma | 10 (35.7%) | 4 (28.6%) | |
| Clear cell carcinoma | 2 (7.1%) | 0 | |
| High grade endometrioid carcinoma | 10 (35.7%) | 5 (35.7%) | |
| Carcinosarcoma | 6 (21.4%) | 5 (35.7%) | |
| FIGO* | .76 | ||
| IA | 8 (28.6%) | 4 (28.6%) | |
| IB | 5 (17.9%) | 3 (21.4%) | |
| II | 4 (14.3%) | 1 (7.1%) | |
| IIIC | 3 (10.7%) | 2 (14.3%) | |
| IVB | 1 (3.6%) | 2 (14.3%) | |
| Neoadjuvant chemotherapy | 1 | ||
| No | 26 (92.9%) | 13 (92.9%) | |
| Yes | 2 (7.1%) | 1 (7.1%) | |
| Operative time median (range) | 180 (90–420) min | 180 (90–420) min | .78 |
| Blood loss median (range) | 300 (50–500) mL | 400 (300–500) mL | 1 |
| Hospital stay median (range) | 3 (1–18) days | 3 (1–8) days | .9 |
| Complications* | |||
| Introperative | 2 (7.1%) | 1 (7.1%) | 1 |
| Postoperative | 7 (25%) | 1 (7.1%) | .2 |
| Positive pelvic nodes# | .65 | ||
| No | 10/13 (76.9%) | 6/9 (66.6%) | |
| Yes | 3/13 (23.1%) | 3/9 (33.3%) | |
| Positive para-aortic nodes# | .5 | ||
| No | 5/6 (83.3%) | 2/4 (50%) | |
| Yes | 1/6 (16.7%) | 2/4 (50%) | |
| Vaginal margin involvement* | 1 | ||
| No | 24 (85.7%) | 13 (92.9%) | |
| Yes | 1 (3.6%) | 1 (7.1%) | |
| Adjuvant therapy* | 1 | ||
| No | 3 (10.7%) | 2 (14.3%) | |
| Yes | 22 (78.6%) | 12 (85.7%) | |
| Recurrence | 1 | ||
| No | 22 (78.6%) | 11 (78.6%) | |
| Yes | 6 (21.4%) | 3 (21.4%) | |
| Estimated mean OAS | 60.95 months | 62.7 months | .89 |
| Estimated mean DFS | 45.7 months | 41.6 months | .6 |
*Some data are missing
#In patients who underwent lymphadenectomy
The estimated mean overall survival of the recruited patients was 67.8 months with 95% CI 54.96–80.6, while the estimated mean DFS was 50.78 months with 95% CI 34.4–67.1. The only significant predictor of overall survival was the recurrence (P value = 0.024), while the only significant predictor of DFS was the presence of malignant para-aortic adenopathy in imaging (P value = 0.002) and the treatment with neoadjuvant therapy (P value = 0.007) (Table 3).
Table 3.
Predictors of overall and disease-free survival
| Parameter | Estimated mean OAS in months | Significance | Estimated mean DFS in months | Significance |
|---|---|---|---|---|
| Morbid obesity | ||||
| No | 60.95 | .89 | 45.7 | .6 |
| Yes | 62.7 | 41.6 | ||
| Approach | .39 | .215 | ||
| Laparotomy | ||||
| Laparoscopy | ||||
| Pathology | .49 | .47 | ||
| Serous carcinoma | 32.1 | 29.5 | ||
| Clear cell carcinoma | 19 | 16.7 | ||
| High grade endometrioid carcinoma | 78.1 | 57.5 | ||
| Carcinosarcoma | 34 | 24.6 | ||
| FIGO stage | .38 | .15 | ||
| Pelvic nodes in radiology | .66 | .43 | ||
| No | 70.3 | 60.3 | ||
| Yes | 28.2 | 22.8 | ||
| Para-aortic nodes in radiology | .39 | .002 | ||
| No | 72.6 | 73.8 | ||
| Yes | 25.8 | 15.6 | ||
| Neoadjuvant chemotherapy | .065 | .007 | ||
| No | 73.4 | 61.5 | ||
| Yes | 46.7 | 26.6 | ||
| Pathologic nodes | .46 | .3 | ||
| Negative | 76.96 | 65.6 | ||
| Positive | 28 | 15.5 | ||
| Vaginal safety margin | .51 | .86 | ||
| Free | 62.7 | |||
| Infiltrated | 37.5 | |||
| Adjuvant therapy | .78 | .86 | ||
| No | 76 | 55 | ||
| Yes | 50.4 | 41.03 | ||
| Recurrence | .024 | |||
| No | 80.2 | |||
| Yes | 58.3 | |||
Discussion
Obesity is considered a major health problem in Egypt, which has an impact on several medical practices. A lot of studies have reported the relation between obesity and surgical outcomes in endometrial cancer [2–4]. In our locality, we have a significant percentage of obese and morbidly obese women, especially in rural areas, and these patients are usually referred to tertiary referral centres as our institute for surgical and medical service. We hereby discuss the surgical outcomes of these patients and the impact of obesity on their outcomes, as well as, the disease-free and overall survival.
The mean estimated blood loss in obese and morbidly obese patients was reported between 94 and 570 mL in obese and between 64.1 and 330 mL in non-obese patients in a number of studies; this difference was found to be statistically significant [18–21]. We reported a mean EBL of 300 mL for non-morbidly obese and 400 mL for morbidly obese patients without statistical significance between both groups, but this can be explained by the fact that almost all of our non-morbidly obese patients were obese or overweight.
The mean operative time was found to be statistically significant between non-obese, obese, and morbidly obese patients in several publications [18–20, 22]. We reported a mean operative time of 180 min in both groups without significant statistical difference.
As regards the intraoperative and postoperative complications, no statistically significant difference between both groups in our study was documented. All the postoperative complications in this cohort were related to the wound as seromas and collections except for one patient who had an intraoperative ureteric injury and was complicated later by ureteric fistula. This coincides with previous studies were no significant statistical difference was found among obese and morbidly obese patients as regards intra- and postoperative complications [20, 23, 24]. Gambacorti-Passerini et al. and Januszek et al. also reported no significant differences in perioperative complications in their studies comparing obese and non-obese patients [21, 25].
The presence of nodal metastases is considered one of the most important prognostic factors that affect the disease-free and overall survival [26, 27]. In the analysis of gynaecologic oncology group GOG-33, the progression-free survival was 90% in early-stage endometrial cancer compared to only 38% in patients with para-aortic lymph node metastasis [28]. In our study, the only significant predictor of disease-free survival was the presence of positive para-aortic nodes in imaging and the treatment with neoadjuvant therapy, both in fact represent and advanced disease. While, the only predictor of shorter overall survival was the occurrence of tumour recurrence.
Obesity did not affect the disease-free or overall survival as reported in several studies [25, 29, 30]. In our study, also the difference in BMI did not affect the disease-free survival or overall survival.
Our study of course had several limitations, including that the study was retrospective, not all the patients were operated on by the same surgeon, and most of our patients even in the non-morbidly obese group were either overweight (BMI between 25 and 30) or obese (BMI 30–40).
Conclusion
Morbid obesity did not have a significant impact on the surgical outcomes of type II endometrial cancer patients. In addition, the disease-free and overall survival and recurrence rate were comparable to non-morbidly obese patients. As such, we recommend offering the same surgical principles for this subgroup of patients. However, randomized controlled trials with longer follow-up periods would be beneficial to consolidate our results.
Declarations
Ethics Approval
All procedures performed in the study involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Approval was obtained from Mansoura Faculty of Medicine Institutional Review Board (MFM-IRB) with code number R.20.12.1137.
Consent to Participate
Informed consent was obtained from the patient included in the study.
Consent for Publication
Consent for publication was obtained from the patients included in the study.
Conflict of Interest
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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