Research ArticleClinical Studies
Open Access

Inflammatory Burden Index Is an Independent Prognostic Factor for Esophageal Cancer Patients Who Receive Curative Treatment

TORU AOYAMA, YUKIO MAEZAWA, ITARU HASHIMOTO, RYUKI ESASHI, SOSUKE YAMAMOTO, KEISUKE KAZAMA, KOJI NUMATA, MAMORU UCHIYAMA, AYAKO TAMAGAWA, AYA SAITO and NORIO YUKAWA
In Vivo November 2024, 38 (6) 2928-2934; DOI: https://doi.org/10.21873/invivo.13775

Abstract

Background/Aim: We hypothesized that the inflammatory burden index (IBI) is a promising biomarker for esophageal cancer (EC) treatment and management. To confirm our hypothesis, we evaluated the prognostic impact of IBI in patients with EC who received curative treatment. Patients and Methods: We conducted a retrospective review of medical records and collected data from consecutive patients with EC who underwent curative resection at Yokohama City University between 2005 and 2020. The IBI score was calculated as the C-reactive protein level multiplied by the neutrophil-to-lymphocyte ratio. Results: In total, 180 patients with EC were included in this study. The 3- and 5-year overall survival (OS) rates were 72.9% and 63.4%, respectively, in the IBI-low group, and 38.2% and 32.5% in the IBI-high group (p<0.001). In the multivariate analysis, IBI was identified as a significant prognostic factor for OS [hazard ratio (HR)=2.372; 95% confidence interval CI=1.478-3.806, p<0.001]. In addition, the 3- and 5-year recurrence-free survival (RFS) rates were 52.9% and 47.8%, respectively, in the IBI-low group, and 22.9% and 17.2% in the IBI-high group (p<0.001). In the multivariate analysis, IBI was identified as a significant prognostic factor for RFS (HR=2.484; 95%CI=1.373-4.494, p<0.001). When comparing the recurrence patterns between the IBI-high and IBI-low groups, there were significant differences in lymph node recurrence (46.0% vs. 26.2%, p=0.010) and hematological recurrence (52.0% vs. 18.5%, p<0.001). Conclusion: IBI affects both the short- and long-term oncological outcomes. Thus, IBI may be a promising prognostic factor for the treatment and management of EC.

Key Words:

Esophageal cancer (EC) was the eighth most common cancer and sixth leading cause of cancer-related deaths in 2020 (1, 2). The standard treatment for early to locally advanced EC is esophagectomy with or without perioperative adjuvant treatment (3, 4). Although the survival of patients with EC after standard treatment is gradually improving, that of patients with recurrent EC remains poor (5, 6). Therefore, it is necessary to identify promising biomarkers for more aggressive treatment and optimal management of patients with EC.

Recently, perioperative nutritional and inflammatory biomarkers have been developed and evaluated for various malignancies (7-10). These biomarkers include the albumin-bilirubin status, lymphocyte to C-reactive protein ratio, CALLY index, systemic inflammation score, and platelet-to-albumin ratio (11-15). These biomarkers affect both the short- and long-term oncological outcomes. Thus, perioperative nutritional and inflammation biomarkers might be promising prognostic or predictive biomarkers for patients with EC. Recently, the Inflammatory Burden Index (IBI) has been proposed for gastric cancer (16). The IBI was calculated by multiplying the C-reactive protein level by the neutrophil-to-lymphocyte ratio. When compared to other inflammatory and nutritional biomarkers, the IBI has emerged as a potentially accurate biomarker for estimating survival outcomes in cancer patients. Considering these findings, we hypothesized that the IBI might affect the short- and long-term oncological outcomes in patients with EC. In addition, we hypothesized that the IBI is a promising biomarker for EC treatment and management. To confirm our hypothesis, we evaluated the prognostic impact of the IBI in patients with EC who received curative treatment.

Patients and Methods

Patients. We conducted a retrospective study by reviewing medical records and collecting data on all consecutive patients with EC who underwent curative resection at Yokohama City University from 2005 to 2020. The inclusion criteria were as follows: histologically diagnosed primary esophageal adenocarcinoma or squamous cell carcinoma; clinical stage IB to III disease [Union for International Cancer Control (UICC) Tumor Node-Metastasis classification, 7th edition]; and complete (R0) resection.

Measurement of inflammatory burden index (IBI). The IBI score was calculated by multiplying C-reactive protein with the neutrophil-to-lymphocyte ratio.

Surgery and adjuvant treatment. Subtotal esophagectomy typically involved a right thoracotomy with reconstruction utilizing a gastric tube. Patients diagnosed with middle- to lower-thoracic tumors underwent a 2-field lymph node dissection procedure, whereas those with upper-thoracic tumors underwent 3-field dissection. Preoperative chemotherapy consisted of two courses of 5-Fluorouracil (800 mg/m2 on days 1-5) and cisplatin (80 mg/m2 on day 1), which was repeated every three weeks.

Definition of postoperative complications. The Clavien-Dindo classification was employed to define postoperative complications (POCs). The study utilized patient records to identify grade 2-5 postoperative complications that were identified either during hospitalization or within 30 days postoperatively.

Patient follow-up. Patients underwent follow-up examinations on an outpatient basis. The patients received hematological tests, which involved measuring CEA and CA19-9 tumor marker levels, along with physical examinations every three months for a period of five years. After surgery, computed tomography examinations were performed at a 3-month interval for the first three years, and then at a 6-month interval until five years postoperatively.

Ethical approval. The institutional review board of Yokohama City University approved the present study (IRB number; F220500064).

Statistical analysis. Associations between the AFR and clinicopathological parameters were analyzed using the χ2 test. The Kaplan-Meier method was used to draw curves for overall survival (OS) and recurrence-free survival (RFS). Univariate and multivariate Cox proportional hazards analyses were performed for the analysis of survival. p-Values of <0.05 were considered to indicate statistical significance. The SPSS software program (v27.0 J Win; IBM, Armonk, NY, USA) was used for all statistical analyses.

Results

Patients background. In total, 180 patients with EC were included in this study. Based on previous reports and 3- and 5-year OS, we used the cutoff value of 10 in the present study. One-hundred thirty patients (72.2%) were classified into the IBI-low group and 50 patients (27.8%) were classified into the IBI-high group. When comparing the patients’ backgrounds between the IBI-high and IBI-low groups, there were significant differences in the T status and lymph node metastasis status (Table I). Patients in the IBI-high group had a more aggressive tumor status than those in the IBI-low group. In contrast, age, sex ratio, tumor site, postoperative surgical complications, and neoadjuvant chemotherapy status were similar between the IBI-low and IBI-high groups.

View this table:
Table I.

Comparison of survival rates stratified by patient characteristics.

Survival analysis. The 3- and 5-year OS rates were 72.9% and 63.4%, respectively, in the IBI-low group and 38.2% and 32.5% in the IBI-high group (p<0.001) (Figure 1). In the univariate analysis of OS, T status, lymph node metastasis, IBI, and lymphovascular invasion were identified as significant prognostic factors. In the multivariate analysis, IBI was identified as a significant prognostic factor for OS [hazard ratio (HR)=2.372; 95% confidence interval (CI)=1.478-3.806, p<0.001] (Table II). In addition, the 3- and 5-year RFS rates were 52.9% and 47.8%, respectively, in the IBI-low group and 22.9% and 17.2% in the IBI-high group (p<0.001) (Figure 2). In the univariate analysis of RFS, T status, lymph node metastasis, IBI, and lymphovascular invasion were identified as significant prognostic factors. In the multivariate analysis, IBI was identified as a significant prognostic factor for RFS (HR=2.484; 95%CI=1.373-4.494, p<0.001) (Table III). When comparing the recurrence patterns between the IBI-high and IBI-low groups, there were significant differences in lymph node recurrence (46.0% vs. 26.2%, p=0.010) and hematological recurrence (52.0% vs. 18.5%, p<0.001) (Table IV).

Figure 1.
Figure 1.

Overall survival of esophageal cancer patients in the Inflammatory Burden Index (IBI)-high and IBI-low groups.

View this table:
Table II.

Uni and multivariate Cox proportional hazards analysis of clinicopathological factors for overall survival.

Figure 2.
Figure 2.

Recurrence-free survival of esophageal cancer patients in the Inflammatory Burden Index (IBI)-high and IBI-low groups.

View this table:
Table III.

Uni and multivariate Cox proportional hazards analysis of clinicopathological factors for recurrence-free survival.

View this table:
Table IV.

Patterns of recurrence according to Inflammatory Burden Index (IBI).

Perioperative clinical course in IBI-high group and IBI-low group. When comparing the perioperative clinical course between the IBI-high and IBI-low groups, significant and marginal differences were observed in the details of postoperative surgical complications and the response to neoadjuvant chemotherapy. The incidence of postoperative anastomotic leakage was 40.0% in the IBI-high group and 30.0% in the IBI-low group (p=0.200). The incidence of pneumonia was 32.0% and 22.3% in the IBI-high and IBI-low groups, respectively (p=0.179). In the present study, 31 patients in the IBI-high group and 61 patients in the IBI-low group received neoadjuvant chemotherapy. Among them, the incidence of a grade ≥2 pathological response was 3.2% in the IBI-high group and 18.0% in the IBI-low group (p=0.046).

Discussion

The aim of the present study was to evaluate the prognostic impact of IBI in patients with EC who received curative treatment. The major finding was that IBI was a significant prognostic factor for both OS and RFS in patients with EC. Our results suggest that IBI may be a promising nutritional and inflammatory biomarker for the treatment and management of EC.

In the present study, patients in the IBI-high group had a significantly poorer prognosis than those in the IBI-low group. In addition, IBI was identified as a significant prognostic factor for OS (HR=2.372; 95%CI=1.478-3.806, p<0.001). Similar results have been reported previously. In the EC setting, Yin et al. evaluated the clinical impacts of IBI in 147 patients with EC who received esophagectomy (17). They calculated the IBI as CRP (mg/d)×neutrophil count (number/μl)/lymphocyte count (number/μl). They set the cutoff value of the IBI to 0.325 based on a receiver operating characteristic (ROC) curve analysis. They found that an increased level of preoperative IBI was significantly associated with an advanced T stage and lymphovascular invasion. In the survival analysis, patients in the IBI-high group had a significantly poorer prognosis than those in the IBI-low group for both OS and disease-free survival (DFS). The HR for OS was 3.56 (95%CI=1.79-7.34, p=0.0003) and DFS was 3.03 (95%CI=1.60-5.92, p=0.0003). They concluded that the preoperative IBI may serve as a useful predictor of the prognosis in patients with EC after esophagectomy. In addition, in the gastric cancer setting, Pelc et al. evaluated the prognostic value of IBI in 93 gastric cancer patients who received multimodal treatment (16). They set the cutoff value of IBI at 9.7 based on a ROC analysis. They divided 93 patients into an IBI-low group (n=46) and an IBI-high group (n=47). Patients who received neoadjuvant chemotherapy and those with postoperative surgical complications had significantly higher IBI values than those who did not receive neoadjuvant chemotherapy or had postoperative surgical complications. Moreover, when comparing the median OS between the IBI-low and IBI-high groups, there were significant differences. In addition, the IBI status was identified as an independent prognostic factor for OS (HR=2.56; 95%CI=1.28-5.13, p=0.0083).

Why does the IBI affect long-term oncological outcomes in patients with EC? There are two possible explanations for this observation. The first is that the IBI affects the response to chemotherapy. In the present study, 31 patients in the IBI-high group and 61 in the IBI-low group received neoadjuvant chemotherapy. Among them, a grade ≥2 pathological responses was observed in 3.2% of the patients in the IBI-high group and 18.0% of the patients in the IBI-low group (p=0.046). Previous studies have demonstrated that nutritional and inflammatory biomarkers, such as the neutrophil-to-lymphocyte ratio and fibrinogen-to-albumin ratio, affect the response to chemotherapy (18, 19). Recent studies have demonstrated that the chemotherapy response is associated with long-term oncological outcomes (20, 21). Thus, our results suggest that IBI might be associated with the chemotherapy response, resulting in a poor prognosis. The second possible reason is that IBI affects the postoperative surgical complications. In the present study, although there were no statistically significant differences, the IBI-high group had a higher incidence of postoperative surgical complications. The incidence of postoperative anastomotic leakage was 40.0% in the IBI-high group and 30.0% in the IBI-low group (p=0.200). Moreover, the incidence of pneumonia was 32.0% and 22.3% in the IBI-high and IBI-low groups, respectively (p=0.179). Previous studies have reported similar results. Yin et al. reported that a high preoperative IBI was a significant independent risk factor for perioperative surgical site infection in patients with EC (odds ratio=2.35; 95%CI=1.00-6.38; p=0.049) (17). Moreover, Pelc et al. reported that a high IBI was significantly associated with a higher risk of postoperative complications (odds ratio=2.95, 95%CI=1.13-7.72) (16). Recent studies have demonstrated that postoperative surgical complications affect the long-term oncological outcomes (22, 23). According to the present and previous studies, the IBI might be associated with postoperative complications, resulting in a poor prognosis.

To utilize the IBI in daily clinical practice, it is necessary to establish and set the optimal cutoff value. In the present study, we set the cutoff value of the IBI according to the 3- and 5-year survival rates. In contrast, Yin et al. used a cutoff value of 0.325 and Pelc used a cutoff value of 9.7, according to the ROC. Thus, future studies should focus on the appropriate methods for determining the cutoff value of the IBI and the optimal cutoff value.

Although the present study demonstrated that the IBI is a promising prognostic marker, the present study was associated with some limitations. First, this was a retrospective study conducted at a single institution. Thus, there might have been patient and selection biases. Second, there was a time bias in the present study, which was conducted in 2005-2020. During the study period, we introduced minimally invasive surgery, a program to enhance recovery after surgery, and changed the perioperative adjuvant treatment. These changes have improved both short- and long-term oncological outcomes. Considering these findings, our results need to be confirmed in another large cohort in the future.

In conclusion, the IBI was a significant prognostic factor for both OS and RFS in patients with EC who received curative treatment. Our results suggest that the IBI might become a promising nutritional and inflammation biomarker for the treatment and management of patients with EC.

Acknowledgements

This study was supported in part by the nonprofit organization of the Yokoyama Surgical Research Group (YSRG).

Footnotes

  • Authors’ Contributions

    TA and YM contributed substantially to this concept and study design. TA, IH, SY, RE, KK, AT, MU, and KN made substantial contributions to the data acquisition, analysis, and interpretation. TA, MN, AS, and NY were involved in drafting and critically revising the manuscript for important intellectual content. TA and YM approved the final version of the manuscript.

  • Conflicts of Interest

    The Authors declare no conflicts of interest in association with the present study.

  • Received July 12, 2024.
  • Revision received July 31, 2024.
  • Accepted August 1, 2024.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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Inflammatory Burden Index Is an Independent Prognostic Factor for Esophageal Cancer Patients Who Receive Curative Treatment
TORU AOYAMA, YUKIO MAEZAWA, ITARU HASHIMOTO, RYUKI ESASHI, SOSUKE YAMAMOTO, KEISUKE KAZAMA, KOJI NUMATA, MAMORU UCHIYAMA, AYAKO TAMAGAWA, AYA SAITO, NORIO YUKAWA
In Vivo Nov 2024, 38 (6) 2928-2934; DOI: 10.21873/invivo.13775
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