The systemic immune-inflammation index in the efficacy prediction of neoadjuvant chemotherapy in patients with endometrial cancer

Introduction

Endometrial cancer (EC) is a frequent malignant tumor of the uterine corpus. Its incidence rate and disease-related mortality have increased worldwide (1,2). For almost 50 years, ECs were divided into type I and type II, with type I mainly composed of endometrioid adenocarcinomas and type II composed of non-endometrioid histological types, mainly serous carcinoma (3). This classification was proved to be insufficient to explain the biological heterogeneity of EC in 2013, when The Cancer Genome Atlas identified the four molecular subtypes: ultramutated, hypermutated (high microsatellite instability), copy number-high, and copy number-low (4). The molecular classification integrated with the traditional clinicopathological parameters allows for more precise treatment decisions (5). This integration is appreciated in the recommendations from the European Society for Medical Oncology, European Society of Gynaecological Oncology, European Society for Radiotherapy and Oncology, and the European Society of Pathology, as well as the International Federation of Gynecology and Obstetrics (FIGO) staging system (6-8). Despite the broader possibilities of new systemic approaches, the primary treatment for EC remains surgical, which can be supplemented by comprehensive treatments such as radiotherapy, chemotherapy, endocrine therapy, and immunotherapy. Comprehensive staging surgery should be actively performed in all patients, except for those with severe co-morbidities, advanced age, advanced stage, unresectable tumor, or those with unsatisfactory initial surgical resection, for whom radiotherapy and drug treatment can be first applied.

The mortality of patients with EC significantly increases with the progression of the disease, with 5-year survival rates of 56% and 17% for patients with stage III and IV disease, respectively (2). Although only 10–15% of all EC cases are at an advanced stage, they account for over half of all deaths (9). Besides, it is estimated that the median survival time for patients with inoperable EC is only 2–8 months (10). Even for patients with advanced-stage disease, optimal cytoreduction is crucial, and neoadjuvant chemotherapy (NACT) reduces morbidity and can be considered for unresectable tumors or special conditions (11,12). Some studies have shown that patients with advanced or unresectable EC who undergo surgery after NACT have significantly improved progression-free survival (PFS) and overall survival (OS) rates (12-15).

The efficacy of NACT is crucial for the prognosis of patients with EC, but there is currently a lack of reliable predictive indicators in clinical practice. The systemic immune-inflammation index (SII) is a novel comprehensive inflammatory biomarker determined by the number of platelets multiplied by the number of neutrophils and then divided by the lymphocyte count. It is associated with the occurrence and development of various diseases (12,16,17). Moreover, SII levels can predict treatment efficacy and prognosis in patients with cancer receiving immune checkpoint inhibitor therapy for different types of cancer (18-20). An increase in SII levels can predict poor OS and PFS in patients with EC (21). The aim of this study was to retrospectively analyze the value of SII in predicting the efficacy of NACT in patients with EC. We present this article in accordance with the TRIPOD reporting checklist (available at https://tcr.amegroups.com/article/view/10.21037/tcr-2025-1386/rc).

Methods

Patients

In this retrospective study, we selected patients with histological diagnosis of EC through diagnostic curettage, pathology examination/endometrial biopsy through hysteroscopy, treated with NACT in Xiang’an Hospital of Xiamen University and Nuclear Industry 215 Hospital of Shaanxi Province from January 2019 to January 2022. Indications for NACT included imaging or laparoscopic exploration indicating doubtful satisfactory success of cytoreductive surgery and patients who could not tolerate surgery due to severe internal diseases or poor physical condition.

The exclusion criteria were as follows: (I) dysfunction or failure of organs such as the heart, liver, and kidneys; (II) presence of other malignant tumors; (III) complication with serious infectious diseases; (IV) presence of immune system diseases; and (V) previous radiotherapy or chemotherapy.

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The selected patients and their families provided informed consent, and the institutional ethics committee of Xiang’an Hospital of Xiamen University approved the research protocol (No. XAHLL2025023). Nuclear Industry 215 Hospital of Shaanxi Province was informed and agreed to this study.

Clinicopathological parameters

Information on age (years), menopause status, smoking history, alcoholism history, hypertension, diabetes, hyperlipidemia, body mass index (BMI), family history, ascites, and pleural effusion was obtained from the hospital medical record.

Histological tumor typing was based on the fifth edition of the 2020 World Health Organization classification of uterine tumors (22). Endometrioid and mucinous carcinoma were considered the same histological type (endometrioid). Non-endometrioid carcinomas included all other histological types: serous, clear cells, undifferentiated/dedifferentiated, and mixed. The International FIGO grading system is primarily based on the proportion of solid non-glandular and non-squamous areas (23). Briefly, 5% or less, 6% to 50%, and more than 50% of solid areas are classified as grade 1, 2, and 3, respectively. Tumors with severe cytological atypia in more than 50% of cells would have one level increase in their grade. Non-endometrioid tumors are considered as grade 3. Clinical staging was based on the FIGO staging system of endometrial cancer (8). All patients were staged before any treatment.

Neoadjuvant treatment

All patients received a platinum-based three-cycle chemotherapy regimen (paclitaxel/platinum), along with supportive treatments such as liver protection, gastric protection, antiemetic therapy, and, if necessary, supplementation with granulocyte colony-stimulating factor to correct bone marrow suppression.

The efficacy of NACT was evaluated based on the Response Evaluation Criteria in Solid Tumors 1.1 (24) rating for solid tumors, which categorizes the disease as having complete response, partial response, stable disease, and progressive disease. Patients with complete or partial response were included in the remission group, while patients with stable and progressive disease were included in the non-remission group. The objective response rate (ORR) was calculated as the percentage of patients with complete or partial response among the total population.

Blood tests and SII calculation

Peripheral blood was collected before treatment to determine the tumor markers cancer antigen 125 (CA125) (U/mL), carcinoembryonic antigen (CEA) (ng/mL), and human epididymis protein 4 (HE4) (pmol/L), as well as neutrophil count (10⁹/L), lymphocyte count (10⁹/L), and platelet count (10⁹/L). The SII was calculated as follows: platelet counts multiplied by neutrophil count and then divided by lymphocyte count.

Statistical analyses

This study used Stata version 15.1 software (StataCorp LLC; College Station, TX, USA) for statistical analyses. Quantitative data were described as the median and interquartile range and compared using Mann-Whitney U test. Categorical variables were expressed by frequency and percentage and compared using the Pearson chi-squared test or the Fisher’s exact test. The receiver operating characteristic curve (ROC) and area under the curve (AUC) were used to assess the predictive value of each parameter. Independent variables were screened through a multiple logistic regression model. A two-tailed P value of 0.05 or less was considered statistically significant.

Results

This study included 150 patients with EC who met the inclusion criteria, including 113 who received NACT and achieved remission and 37 in the non-remission group, representing an ORR of 75.33% (Figure 1). A total of 42 (28.00%) patients achieved complete response, 71 (47.33%) achieved partial response, 30 (20%) had stable disease, and 7 (4.67%) had progressive disease. The clinicopathological parameters are summarized in Table 1. There was no statistical difference between the two groups according to the age of patients, smoking history, alcoholism history, diabetes, hypertension, BMI, menopausal status, ascites, and pleural effusion. Only hyperlipidemia, histological type, tumor grade, and FIGO staging were associated with remission.

Figure 1 Flowchart of patients included in the study.

Hyperlipidemia was negatively associated with remission. Among patients with hyperlipidemia, 6/13 (46.1%) presented remission, in contrast to 107/137 (78.1%) in the non-remission. On the other hand, endometrioid histological type (79% vs. 41.2%), low-grade (tumor grade 1/2) (82.7% vs. 58.7%), and FIGO stage II vs. III/IV (100% vs. 67.5%) were associated with remission.

Tumor markers CA125, CEA and HE4 were compared in the two groups, either as continuous or categorical variables with cut-offs of 35 U/mL, 2.5 ng/mL, and 76.2 pmol/L, respectively. There was no significant statistical difference in their expression between the two groups (Table 2).

Although there was no significant difference in the individual immune inflammation levels (neutrophil, platelet, and lymphocyte counts) between the remission and non-remission groups, the SII levels were higher in the group of non-remission group (Table 3).

Prediction indicators and value of NACT efficacy in patients with EC

After 3 years of follow-up, 42 (28.00%) patients had died, including 25 (22.1%) in the remission group and 17 (45.9%) in the non-remission group. The ROC curve indicated that hyperlipidemia, SII, histological type, FIGO staging, and histological grade all had a specific predictive value for the efficacy of NACT (AUC =0.5680, AUC =0.7407, AUC =0.6042, AUC =0.6872, and AUC =0.6445, respectively). The ROC curve and AUC value indicated that the optimal diagnostic threshold for SII in predicting the efficacy of NACT in patients with EC was 494.26 (Table 4 and Figure 2). Based on logistic regression analysis, it was found that hyperlipidemia, SII ≥494.26, non-endometrioid histological type, high FIGO staging, and high tumor grade were independent influencing factors for ineffective NACT in patients with EC (P=0.01, P<0.001, P=0.002, P=0.001, and P=0.01, respectively) (Table 5).

Figure 2 Prediction indicators and value of neoadjuvant chemotherapy efficacy in patients with endometrial cancer. AUC, area under the curve; FIGO, International Federation of Gynecology and Obstetrics; SII, systemic immune-inflammation index.

Discussion

Among the 150 patients with EC administered with NACT in this study, we obtained an ORR of 75.33%. Lim et al. reported 32 patients with FIGO stages IIIC-IVB administered with NACT followed by debulking surgery, and they found ORR of 87.5% and 71.9% having achieved complete cytoreduction (15). Nakanishi et al., in their study to evaluate the feasibility of NACT followed by debulking surgery in 51 patients with stage IVB endometrial cancer found a response ratio of 65.3% [95% confidence interval (CI): 50.4–78.3%], while the median disease-free survival and median OS of patients who underwent surgery after neoadjuvant therapy were reported to be 9.1 months (95% CI: 6.5–11.9) and 23.2 months (95% CI: 11.9–27.8), respectively (25). Our results and these numbers from the literature show that NACT can be an option for selected cases.

Some of our results were intriguing, such as the role of hyperlipidemia in the NACT response. It is well known that the development of endometrial cancer is significantly correlated with metabolic factors, with hyperlipidemia being the leading risk factor (26). These factors are associated with type I endometrial cancers, younger patients, endometrioid histology, low tumor grade, and low stage (3). In the large retrospective study conducted by Abdol Manap et al. with 281 patients with EC, premenopausal women presented a higher incidence of obesity and tumors with more favorable features and better prognoses (27). However, our results did not reveal any impact of age or menopausal status on the efficacy of NACT. Besides, while endometrioid histology, low-grade and low-stage, features of type I EC were positively associated with remission, hyperlipidemia had the opposite behavior. One possible explanation is that the patients of our cohort with hyperlipidemia were older and with more co-morbidities. In the study of Lyu et al., postmenopausal or older age patients with EC were more likely to experience hyperlipidemia (28).

Another provoking result from our data was the features of the group that achieved remission. The NACT used in our cases was a platinum-based regimen acting on proliferative cells. We expected that response would be higher in the more aggressive tumors. Instead, we observed better efficacy among endometrioid histology, low tumor grade, and earlier stage, all conditions associated with lower proliferative activity. We hypothesize that other factors contributed to these results. Among them, we have to consider the role of tumor microenvironment (TME), which can explain our results with the SII.

Elevated SII has been described as a negative predictive and prognostic factor. It has been reported to be an independent risk factor for lymph node metastasis in patients with endometrial cancer and a predictive indicator for muscle infiltration and higher pathological grade in premenopausal patients (29). In addition, elevated SII has been demonstrated to be an independent risk factor for advanced disease progression in patients with EC aged ≥55 years or those who are postmenopausal (29). In the multivariate analysis of one study, SII was associated with adverse clinical pathological factors but not with survival rates (30). Another study found that in patients with non-endometrioid carcinomas, an elevated ratio of monocytes to lymphocytes was significantly associated with adverse clinical outcomes and an independent prognostic marker (31). The formula of SII has lymphocyte counts in the denominator, so we can expect a low mobilization of these crucial cells for local immune response. The association between SII and local immune TME could be demonstrated in at least two types of cancers (32,33). Ruiz-Ranz et al. evaluated 348 oral squamous cell carcinomas for the local infiltration by immune cells and demonstrated an inverse correlation with SII levels (33). In that same study, high levels of SII were associated with poor OS. The same inverse correlation between SII and local immune cells, like T-cells and cytotoxic T-cells, was demonstrated in 51 patients with germ cell tumors (32). These data support SII as a potential biomarker for immunotherapy in EC, especially if we consider that (I) this is the option for the treatment of advanced/recurrent EC, and (II) its value has been demonstrated in other types of cancer, such as in non-small cell lung cancer, for example (34).

There are some weaknesses in this study, including the retrospective design that might interfere with the accuracy of the information in the medical records. Besides, we could not analyze the impact of molecular subtypes of endometrial cancer on our results. On the other hand, there are strengths that can be highlighted. The sample size is one of them. NACT is an exception treatment, so the sample size that we analyzed is significant and this study provides useful information about biological events in aggressive tumors. The SII is poorly explored as a prognostic and predictive biomarker in EC. Considering the new options for the diagnosis and treatment of EC, such as poly ADP ribose polymerase inhibitors, HER2-directed therapies, antibody-drug conjugated (35,36), pre-operative MRI-radiomics analyses (37,38), immune checkpoints (39), our study can provoke interest in expanding its investigation in other scenarios. Besides, even though NACT is rarely indicated in the treatment of EC, our study offers valuable information for better case selection. There are few studies on the correlation between the efficacy of NACT in patients with EC and the SII, and further validation is needed through large-scale prospective studies.

Conclusions

In patients with EC, the presence of hyperlipidemia, SII levels, histological type, FIGO staging, and tumor grade are predictive of the efficacy of NACT. Hyperlipidemia, SII levels ≥494.26, non-endometrioid histological type, high FIGO staging, and high tumor grade are all independent factors affecting the ineffective response of patients with EC to NACT.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the TRIPOD reporting checklist. Available at https://tcr.amegroups.com/article/view/10.21037/tcr-2025-1386/rc

Data Sharing Statement: Available at https://tcr.amegroups.com/article/view/10.21037/tcr-2025-1386/dss

Peer Review File: Available at https://tcr.amegroups.com/article/view/10.21037/tcr-2025-1386/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tcr.amegroups.com/article/view/10.21037/tcr-2025-1386/coif). F.M.C. receives fees from GSK (GlaxoSmithKline) and Merck Sharp & Dohme for lectures related to endometrium carcinoma because she’s a university professor. The companies that hired her do not influence her opinions or scientific activities. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The selected patients and their families provided informed consent, and the institutional ethics committee of Xiang’an Hospital of Xiamen University approved the research protocol (No. XAHLL2025023). Nuclear Industry 215 Hospital of Shaanxi Province was informed and agreed with this study.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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(English Language Editor: J. Gray)