Open Access, Peer-reviewed
pISSN 2005-0380   eISSN 2005-0399
    J Gynecol Oncol. 2024;35:e32. Forthcoming. English.
    Published online Dec 19, 2023.
    https://doi.org/10.3802/jgo.2024.35.e32
    © 2024. Asian Society of Gynecologic Oncology, Korean Society of Gynecologic Oncology, and Japan Society of Gynecologic Oncology
    Original Article

    Trends in the incidence and survival outcomes of endometrial cancer in Korea: a nationwide population-based cohort study

    Seung-Hyuk Shim,1 Jiwon Lim,2 Ji Hyun Kim,3 Yeon Jee Lee,3 Hyeong In Ha,4 Myong Cheol Lim,3,5,6 and Young-Joo Won2,6,7
      • 1Department of Obstetrics and Gynecology, Research Institute of Medical Science, Konkuk University School of Medicine, Seoul, Korea.
      • 2Division of Cancer Registration and Surveillance, National Cancer Center, Goyang, Korea.
      • 3Center for Gynecologic Cancer, National Cancer Center, Goyang, Korea.
      • 4Department of Obstetrics and Gynecology, Pusan National University Yangsan Hospital, Pusan, Korea.
      • 5Gynecologic Cancer Branch, Research Institute and Hospital, National Cancer Center, Goyang, Korea.
      • 6Department of Cancer Control and Population Health, National Cancer Center Graduate School of Cancer Science and Policy, National Cancer Center, Goyang, Korea.
      • 7Division of Health Administration, College of Software and Digital Healthcare Convergence, Yonsei University, Wonju, Korea.
    • Correspondence to Myong Cheol Lim. Center for Gynecologic Cancer, Research Institute and Hospital, National Cancer Center, 323 Ilsan-ro, Ilsandong-gu, Goyang 10408, Korea. Email: mclim@ncc.re.kr
      Correspondence to Young-Joo Won. Division of Health Administration, College of Software and Digital Healthcare Convergence, Yonsei University, 1 Yeonsedae-gil, Wonju 26493, Korea. Email: youngwon@yonsei.ac.kr
    Received February 18, 2023; Revised July 23, 2023; Accepted November 26, 2023.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Objective

    To evaluate trends in the incidence and survival outcomes of endometrial cancer (EC) based on the year of diagnosis, stage, age, and histologic types.

    Methods

    Women with primary EC diagnosed between 1999 and 2018, and who were followed up with until 2019, were identified from the Korea Central Cancer Registry using the International Classification of Diseases, 10th revision. The age-standardized rates (ASRs) of incidence, annual percent changes (APCs), and survival were estimated according to age, stage, histology, and year of diagnosis.

    Results

    The ASR for EC increased from 2.38 per 100,000 in 1999 to 7.29 per 100,000 in 2018 across all histologic types (APCs of 9.82, 15.97, and 7.73 for endometrioid, serous, and clear cell, respectively, p<0.001). There were significant differences in the 5-year survival rates based on histology (90.9%, 55.0%, and 68.5% for endometrioid, serous, and clear cell, respectively, p<0.001), stage (93.4%, 77.0%, and 31.0% for localized, regional, and distant, respectively, p<0.001), and age (93.0% for <50 years and 80.6% for ≥50 years, p<0.001). The 5-year survival was significantly better in the group diagnosed between 2000 and 2018 (85.9%) than that in the 1999–2008 group (83.3%) (p<0.001). This trend was only observed for endometrioid cancer (p<0.001).

    Conclusion

    The incidence of EC increased across the all 3 subtypes. Survival of patients with endometrioid histology improved over the past two decades, but remained static for serous or clear cell histology. Healthcare strategies to prevent EC incidence in at-risk populations and apply effective treatments for high-risk histology are needed.

    Synopsis

    This cohort study analyzed 31,598 women with primary endometrial cancer (EC). Incidence increased across the endometrioid as well as serous and clear cell histology of EC. Survival improved for endometrioid but not for serous or clear cell cases. Strategies to prevent EC and to improve survival for those with high-risk EC histologies are needed.

    Keywords
    Endometrial Cancer; Incidence; Survival; Cancer Staging; Histology

    INTRODUCTION

    Endometrial cancer (EC) is the most common female genital tract cancer in Western countries. In the USA, there were 65,620 newly diagnosed cases of EC, making it the fourth most common cancer in females [1]. In Korea, the incidence of EC has increased, and there were 3,287 newly diagnosed cases of EC, making it the seventh most common cancer in females with an age-standardized rate (ASR) of 7.9 per 100,000 in 2019 [2]. This increase has been associated with an increase in obesity incidence, extended life expectancy, and adjuvant tamoxifen use for breast cancer [3].

    Although several epidemiologic studies have reported the increase in incidence of EC in Korea, the trends in the incidence and survival outcomes across the year of diagnosis and stage of disease have not been elucidated in a nationwide population [4, 5]. Moreover, most studies focused on data regarding EC without providing specific information by histologic type; thus, incidence and survival outcomes based on histological type (serous or clear cell type) is not well recognized. Understanding the trends in cancer incidence and survival using nationwide population-based data provides a key insight into the overall effectiveness of the health system [6]. Therefore, the present study aimed to evaluate the trends in incidence and survival outcomes of EC across the year of diagnosis, stage, age, and histologic types during the past two decades, using the nationwide population-based cancer registry from 1999 to 2018.

    MATERIALS AND METHODS

    1. Dataset

    We obtained data from the Korea Central Cancer Registry (KCCR). The KCCR is a nationwide, population-based cancer registry that covers the entire South Korean population, collects information on approximately 98% of the cancer cases in Korea, and publishes annual cancer statistics [5]. The completeness of the cancer incidence data for 2018 was estimated as 98.2% based on the method proposed by Ajiki et al. [7]. Detailed information regarding the KCCR is provided elsewhere [8, 9]. Patients diagnosed with EC from January 1, 1999, to December 31, 2018, were included and followed up with until December 2019. We only included cases of primary EC (C54), which was defined following the International Classification of Diseases, 10th revision. KCCR data are linked to the mortality statistics provided by Statistics, Korea.

    2. Variables and statistical analyses

    The following data were extracted: clinicodemographic variables, including age at diagnosis, date of diagnosis, histological type, stage, and date of death. Age at diagnosis was categorized into 2 (<50 years and ≥50 years). The period of diagnosis was categorized into 2 (1999–2008 and 2009–2018). Histological types were classified as endometrioid, serous, and clear cell. Staging information was based on the Surveillance, Epidemiology and End Results summary staging [10], which categorizes cancer spread from its origin (localized, regional, and distant). Data analyses according to the stage were performed on the women diagnosed from 2006 since stage variable is available from 2006 in the KCCR. The incidence rates of EC were expressed as ASR per 100,000 women and were estimated according to the year of diagnosis and histologic subtypes. The ASRs were calculated using the Segi's standard population [11]. The trends in the incidence rates of EC were estimated as an annual percent changes (APCs) using the following formula: [exp(β)−1]×100, where β was the slope calculated from a linear regression for natural logarithm of incidence rate [12]. Overall survival was estimated using the Kaplan-Meier method [13] and compared using the log-rank test. Statistical significance was set at an alpha level of 0.05. Statistical analyses were conducted using SAS software ver. 9.4 (SAS Institute Inc. Cary, NC, USA) and STATA software ver. 16 (Stata Corp. LLC, College Station, TX, USA). Ethical approval for the research protocol was provided by the Institutional Review Board of the National Cancer Center, Goyang, Korea (NCC2021-0341).

    RESULTS

    1. Incidence

    During the study period, the KCCR database identified a total of 31,598 patients with primary EC. Clinicopathologic characteristics of patients are shown in Table 1. Endometrioid histology (68.9%) was the most common cancer type, followed by serous (3.1%) and clear cell (1.5%). The mean age at diagnosis was younger in the group with endometrioid histology (52.4 years) than in the groups with serous (62.6 years) or clear cell (62.4 years) histology. Localized disease was the most common stage in all histologic types (75.8% in endometrioid, 43.5% in serous, 52.6% in clear cell); however, regional and distant stages were significantly higher in serous (33.7%, 19.6%) and clear cell (27.0%, 14.1%) than in the endometrioid histology groups (15.9%, 3.8%) (p<0.001). Surgery was frequently selected as the treatment modality in all histologic types (91.8% for endometrioid, 91.2% for serous, 88.8% for clear cell). The use of radiotherapy was more frequent in serous (21.7%) and clear cell (23.3%) histology than in endometrioid (16.0%) histology (p<0.001). Specifically, the use of chemotherapy was more prominent in serous (54.1%) and clear cell (41.0%) histology than in endometrioid (15.7%) histology (p<0.001).

    Table 1
    Clinicopathologic characteristics of patients with primary endometrial cancer in Korea, 1999–2018

    The ASRs and APCs for primary EC are shown in Table 2. The absolute number of cases with EC has increased progressively from 624 in 1999 to 3,025 in 2018. The ASR for EC has been increasing from 2.38 per 100,000 in 1999 to 7.29 in 2018 with the APC of 6.03 (p<0.001). This increase was observed in all histological types (APC of 9.82 for endometrioid, p<0.001; 7.73 for clear cell, p<0.001; and 15.97 for serous type, p<0.001).

    Table 2
    The incidence of primary endometrial cancer in Korea, 1999–2018

    We showed clinicopathologic characteristics of the patients by time period of diagnosis (2009–2018 vs. 1999–2008) in Table S1 (which is an expansion of Table1). The proportion of older patients (>50 years) has increased and the age at diagnosis was increased in both endometrioid (from 51.1 years to 52.8 years, p<0.001) and serous histologies (from 60.6 years to 63.0 years, p=0.003). In particular, the proportion of elderly patients over 70 years of age with serous histology increased significantly (from 15.0% to 24.5%, p=0.039). In addition, local stage in endometroid histology increased significantly from 69.9% to 76.8% (p<0.001), whereas the distribution of stage at diagnosis for serous histology showed no statistically significant difference (p=0.367).

    2. Survival by histology, time period of diagnosis, stage, and age group

    The survival curve of primary EC decreased from 85.1% at 5 years after diagnosis to 79.9% at 10 years after diagnosis (Fig. 1A). The 5-year and 10-year survival were significantly lower for patients with serous (55.0%, 47.7%) than endometrioid (90.9%, 86.1%) or clear cell (68.5%, 59.3%) histologies (p<0.001, log-rank test) (Fig. 1B).

    Fig. 1
    Overall survival of patients with endometrial stratified according to histology, 2006–2016. (A) All, (B) Histology.

    When analyzed by time period of diagnosis, the 5-year survival was significantly higher in the 2009–2018 (85.9%) than in the 1999–2008 group (83.3%) (p<0.001, log-rank test) (Fig. 2A). This trend was only observed for endometrioid histology (p<0.001, log-rank test), and not for serous (p=0.535, log-rank test) or clear cell histologies (p=0.347, log-rank test) (Fig. 2B-D).

    Fig. 2
    Overall survival of patients with endometrial stratified according to year of diagnosis (1999–2008 vs. 2009–2018). (A) All, (B) Endometrioid, (C) Serous, (D) Clear cell.

    The group with localized-stage disease had better 5-year survival (93.4%) rates than the group with regional (77.0%) or distant-stage disease (31.0%) (p<0.001, log-rank test) (Fig. 3A). This trend was observed in all histologies (Fig. 3B-D). Of note, the 5-year survival of the localized stage group was lower for serous (72.5%) than for clear cell (83.5%) histology.

    Fig. 3
    Overall survival of patients with endometrial stratified according to stage (localized, regional, and distant). (A) All (B) Endometrioid (C) Serous (D) Clear cell.

    The 5-year survival was lower in the group aged ≥50 years (80.6%) than in that aged <50 years (93.0%) (p<0.001, log-rank test) (Fig. 4A). This trend was observed in endometrioid (p<0.001, log-rank test) (Fig. 4B) and serous histology (p=0.002, log-rank test) (Fig. 4C), but not clear cell histology (p=0.113, log-rank test) (Fig. 4D).

    Fig. 4
    Overall survival of patients with endometrial stratified according to age (<50 years and ≥50 years). (A) All, (B) Endometrioid, (C) Serous, (D) Clear cell.

    DISCUSSION

    The results of this nationwide population-based cohort study showed a continuous increase in the incidence of all 3 subtypes of EC from 1999 to 2018 in Korea. Survival rates showed distinct differences according to histologic type, stage, and age, which are traditional prognostic factors. These findings are biologically plausible based on the results from previous studies. Over past two decades, improved survival was observed for endometrioid EC, whereas the survival rate remained static for serous and clear cell types. Our results indicate the need for developing prevention strategies that can target populations at risk and aid in the creation of efficient treatment modalities for high-risk EC in routine clinical practice.

    The overall increase in EC could be explained by several major risk factors. Obesity is well known to have a strong impact in increasing the incidence for type I EC; however, in recent studies, an association with obesity was observed regardless of the subtype of EC [14, 15]. In Korea, the prevalence of obesity increased linearly for 10 years: the prevalence of overall obesity was 38.5% in 2018 compared to 32.5% in 2009 [16]. A recent study found that a body mass index higher than 25 kg/m2 among Asian women increased the risk of EC by 1.57 times [17]. Other factors for the increase in EC incidence can be explained by westernized dietary habits, contraceptive use, and increase in hormonal therapy use due to the increase in breast cancer [18].

    A significant increase in the incidence of serous carcinoma was particularly observed in the present study, while type II EC was static in the UK data [19]. As serous carcinoma generally presents at an advanced age, discrepancies in the incidence proportion of serous carcinoma from other countries might be related to the aging population. According to the Organization for Economic Cooperation and Development data, Korea has the fastest pace to reach aging population by 3.3% of the average annual aging rate [20]; by 2040, elderly people aged >65 years are expected to account for 33.9% of Korea’s population, the second highest figure in the world. This figure is expected to reach 46.5% by 2067, making Korea the world’s most aged society, up 3-fold from its current figure of 14.9%. In addition, improvement in the pathologic diagnostic process might also explain the increased incidence of serous carcinoma. Serous carcinoma is morphologically difficult to distinguish from high-grade EC, so there has been a significant interobserver variability among high-grade endometroid carcinoma [21, 22]. An immunohistochemical panel has also been recently validated. With multiple biomarkers including ER, p16, PTEN, and PGR, differentiating between serous carcinoma and high-grade endometrioid carcinoma has improved [23].

    In the present study, the survival rate following EC showed improved in the later 10 years (2009–2018) compared to the initial 10 years (1999–2008). This is primarily due to the improvement of clinical outcomes in endometrioid histology. However, only the endometrioid subtype showed statistically significant 5-year survival improvement. In the case of endometrioid EC, the most prominent difference is the disease stage at diagnosis. The percentage of patients with endometroid histology with local stage increased from 69.9% to 76.8% (p<0.001). However, the distribution of stage during diagnosis of serous histology had no statistically significant difference (Table S1). Unlike common expectations that the proportion of younger patients would have increased in endometrioid histology, the percentage of older patients (>50) has increased and the age at diagnosis was increased in endometrioid histology. However, the age at diagnosis among those with endometroid subtype was still lower than that of those with serous or clear cell EC, thus impacting clinical outcomes.

    In the present study, the age of diagnosis of those with serous EC increased from 60.6 to 63.0 years, and the distribution of age at diagnosis moved to older age. Distinctively, the proportion of elderly patients over 70 years of age has increased significantly (15.0% to 24.5%), which may affect survival deterioration. Although the proportion of patients receiving chemotherapy increased from 43.1% to 56.1% (p<0.001), this seems to be insufficient to improve the survival rate (Table S1).

    Those with clear cell EC showed lower survival rate than those with endometrioid EC but better survival rate than those with serous EC. There are few articles directly comparing serous and clear cell histology [24] as grade 3 endometrioid EC and high-risk cancers (both serous and clear cell histology as one group) are compared [25]. The reason for the survival differences between the 2 high-risk groups are unknown. However, in the present study, when comparing the 2 histologies, the stage distribution between serous and clear cell was statistically significantly different, and clear cell EC tended to be more an early-stage disease (p<0.001). Unlike endometrioid EC that has known risk factors (prolonged exposure to unopposed estrogen), the etiology of serous and clear cell EC is unknown. Therefore, more research needs to be done to illustrate the reasons for the survival differences. Unfortunately, several pivotal studies on EC focused endometrioid histology alone, not on serous and clear cell histologies [26, 27]. In addition, targeted therapy is not actively being used as medical insurance and does not cover the routine clinical use of these in Korea. To improve the survival outcomes of high risk, advanced, and infrequent EC patients, a new multidisciplinary approach, different from that for low-grade endometrioid histology, is needed.

    In the present study, there was a difference in the 5-year survival rate according to age. The 5-year survival rate was increased in those under 50 years of age compared to that in those over 50 years of age. These findings are consistent with those of previous studies [28, 29]. However, the difference in survival rate according to age in clear cell histology was not clear compared to that of other types. This might be partly explained by the fact that the mean age at the time of diagnosis among patients with clear cell histology was higher than that in those with other histologies; thus, a significant proportion (87.5%) were diagnosed when they were older than 50 years.

    A strength of this nationwide population-based study is the inclusion of a large number of women with EC from entire Korean population. Thus, our findings are much more representative of the real-world clinical practice. Moreover, the database provides information regarding clinicopathologic variables and ensured completeness of mortality data. However, this study has several limitations. First, there was limited clinical information, including data on body weight, molecular classification for EC, and adjuvant treatment. Although this did not considerably affect our analysis, this is an intrinsic limitation of using the cohort data in the cancer registry database KCCR. Second, we did not perform multivariable analysis with adjustment of relevant covariates to estimate the effect of prognostic factors on survival outcomes. Third, the KCCR provide SEER stage variables from 2006 only; thus, data analyses according to the stage were performed on the women diagnosed from 2006. Lastly, the incidence of EC was not adjusted for the rates of hysterectomies because these data were unavailable for the study period. However, as the overall rates of hysterectomy were negligible (162 of 100,000 females) [30], this limitation would seem to have a minimal influence on our results.

    In conclusion, the incidence in EC increased across all histologic subtypes from 1999 to 2018 in Korea. Distinct differences in survival according to histologic type, stage, and age were demonstrated. Our real-world results indicate the need for future health-care services with prevention strategies that can target populations at risk. In addition, improved survival was observed in endometrioid EC over the past two decades, while survival remained static for serous and clear cell ECs. Given the differential increase in survival over time across the histologic types, there is a need for effective treatment modalities such as targeted therapy or immunotherapy for those with high-risk EC histologies in routine clinical practice. It is also essential to monitor the impact of therapeutic changes at the population level.

    SUPPLEMENTARY MATERIAL

    Table S1

    Clinicopathologic characterisitics of patients with primary endometrial cancer by time period of diagnosis (2009–2018 vs. 1999–2008)

    Click here to view.(33K, xls)

    Notes

    Funding:This research was supported by the National Cancer Center of Korea (grant No. 1910132-3) and “Regional Innovation Strategy (RIS)” through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (MOE) (2022RIS-005).

    Conflict of Interest:No potential conflict of interest relevant to this article was reported.

    Authors Contributions:

    • Conceptualization: S.S.H., L.M.C., W.Y.J.

    • Formal analysis: L.J.

    • Funding acquisition: L.M.C., W.Y.J.

    • Methodology: L.M.C., W.Y.J.

    • Writing - original draft: S.S.H., L.J.

    • Writing - review & editing: K.J.H., L.Y.J., H.H.I., L.M.C., W.Y.J.

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