Research ArticleClinical Studies
Open Access

The Usefulness of the Modified Advanced Lung Cancer Inflammation Index (mALI) as a Prognostic Factor in Patients With Esophageal Cancer who Have Undergone Curative Resection

SOSUKE YAMAMOTO, TORU AOYAMA, YUKIO MAEZAWA, ITARU HASHIMOTO, RYUKI ESASHI, KAZUKI OTANI, SUGURU NUKADA, TETSUSHI ISHIGURO, KIYOKO SHIMADA, KEISUKE KAZAMA, KOJI NUMATA, MAMORU UCHIYAMA, REI HATAYAMA, AYAKO TAMAGAWA, AYA SAITO and NORIO YUKAWA
In Vivo July 2025, 39 (4) 2176-2185; DOI: https://doi.org/10.21873/invivo.14013

Abstract

Background/Aim: In several previous studies, the modified advanced lung cancer inflammation index (mALI) has been reported to be a useful prognostic factor in non-small cell lung cancer. This study aimed to demonstrate the relationship between mALI and the oncological prognosis of patients with esophageal cancer (EC) who underwent curative treatment and to clarify the underlying mechanism.

Patients and Methods: We retrospectively followed up patients who underwent curative resection of esophageal cancer at Yokohama City University between 2000 and 2020 and extracted clinical data from their medical records. mALI was defined as follows: mALI=[L3 muscle index (L3MI) (cm2/m2)×albumin (g/l)]/neutrophil-to-lymphocyte ratio (NLR) [neutrophil count÷lymphocyte count].

Results: A total of 196 patients were selected for this study, and the cutoff value for mALI was set separately for male and females. When the cutoff value was set at 10 for males and 12 for females, 84 patients were assigned to the mALI-low group and 112 patients were assigned to the mALI-high group. A survival analysis revealed that the 5-year overall survival (OS) rate was 50.3% in the mALI-low group and 62.5% in the mALI-high group (p=0.014). A multivariate analysis of OS revealed that mALI was an independent prognostic factor. The 5-year recurrence-free survival (RFS) rates were 33.0% in the mALI-low group and 44.9% in the mALI-high group (p=0.044). The multivariate analysis of RFS revealed that mALI was an independent prognostic factor. In addition, the mALI-low group had a higher rate of hematogenous metastasis than the mALI-high group.

Conclusion: mALI is associated with the oncological prognosis of patients with EC who have undergone radical resection via several mechanisms and is a useful prognostic factor.

Keywords:

Introduction

Esophageal cancer (EC) is the 11th most commonly diagnosed cancer worldwide and the 7th leading cause of cancer-related death (1). The treatment for EC varies based on the stage of the disease. For resectable cases, treatment methods including preoperative and postoperative adjuvant chemotherapy, radiation therapy, perioperative nutritional therapy and robotic surgery are improving each year (2). However, postoperative recurrence is still associated with a very poor prognosis (3, 4). Therefore, when a patient is diagnosed with resectable cancer, predicting the prognosis is crucial for optimal preoperative management.

Several studies have indicated that the advanced lung cancer inflammation index (ALI) is a valuable prognostic factor for patients with small-cell lung cancer (5-8). However, since the body mass index (BMI), a component of ALI, does not accurately represent the patient’s body composition, several recent reports have highlighted the usefulness of modified ALI (mALI), which is calculated by dividing the muscle area at the L3 level of the lumbar spine by height (9-12). Several studies have highlighted the usefulness of ALI in predicting the oncological prognosis of patients with EC who have undergone surgery (13, 14), but we could not find any studies on the usefulness of mALI within the scope of our search.

The aim of our current study was to clarify the usefulness of mALI as a prognostic factor in patients with EC who have undergone curative resection, and to consider the mechanisms by which mALI affects the oncological prognosis of these patients.

Patients and Methods

Patients. Patients who underwent curative resection of EC at Yokohama City University between 2000 and 2020 were selected for this study, provided they met the following criteria. (i) Patients diagnosed with squamous cell carcinoma via pathological assessment; (ii) patients with clinical stage 0 to III, as defined in the 12th edition of the Japanese Esophageal Society’s “Regulations for the Treatment of Esophageal Cancer” (15); (iii) patients who received curative esophagectomy following preoperative chemoradiotherapy or preoperative adjuvant chemotherapy as the primary treatment for esophageal cancer; and (iv) patients who underwent complete resection (R0) of esophageal cancer.

Surgery and adjuvant therapy. All patients in this study underwent esophagectomy along with two- or three-field lymphadenectomy. Patients with pathological stage II or III disease were administered postoperative adjuvant chemotherapy.

Definition of the modified advanced lung cancer inflammation index (mALI) score. The mALI score was determined using the following formula:

Embedded Image

The neutrophil-to-lymphocyte ratio (NLR) and albumin level were determined using pretreatment blood test data. NLR was calculated as the neutrophil count/lymphocyte count. The L3 muscle index (L3MI) was the cross-sectional area of the muscle at the third lumbar vertebra level divided by the square of the height and was referenced from the computed tomography (CT) images at the time of the diagnosis of EC. Blood test data were collected before treatment.

Follow-up. Follow-up evaluation was performed during outpatient care after surgery, and patients were followed for five years, undergoing blood tests and physical examinations, including the measurement of tumor markers, at least once every three months. In addition, CT scans were performed once within three months of surgery and once every six months until five years after surgery.

Statistical analysis. Data are presented as counts and percentages. mALI and clinicopathological factors were analyzed in the mALI-high and mALI-low groups using the chi-squared test. The Kaplan-Meier method was used to draw curves for overall survival and recurrence-free survival, and the log-rank test was used to compare survival curves between the two groups. Univariate and multivariate survival analyses were performed using a Cox proportional hazards model. Statistical significance was set at p<0.05. All statistical analyses were performed using SPSS (ver. 27.0 Win; IBM, Armonk, NY, USA).

Ethical approval. This study was approved by the Yokohama City University Ethics Committee.

Results

Patient characteristics. The study included 196 (male, n=166; female, n=30) patients, with a median age of 70 years, including 93 patients of 70 years of age or older. Cutoff values were established separately for males and females based on the 3- and 5-year overall survival rates, considering the differences in skeletal muscle mass between the sexes. In this study, the cutoff value for mALI was established at 10 for males and 12 for females. This is because the 3- and 5-year overall survival rates are lower for both men and women. Based on the above, men were assigned to the mALI-low group if mALI was <10 and to the mALI-high group if mALI was ≥10. Women were assigned to the mALI-low group if the mALI was <12 and to the mALI-high group if the mALI was ≥12. Using these cutoff values, 196 patients were categorized into the mALI-low group (n=84) and the mALI-high group (n=112) (Table I). When comparing the patient backgrounds of the mALI-low and mALI-high groups, the mALI-high group had a greater proportion of male patients. Conversely, the mALI-low group had a significantly higher proportion of patients with Hb <11 g/dl in preoperative blood tests, as well as a higher proportion of patients who received blood transfusions during the perioperative period. The proportion of patients receiving preoperative radiotherapy was significantly higher in the mALI-low group than in the mALI-high group, and a greater proportion of patients in the former group also underwent salvage surgery.

View this table:
Table I.

Comparison of survival rates stratified by patient characteristics.

Overall survival (OS) rate. The survival analysis of OS between the two groups yielded some interesting results. The 5-year survival rate was 50.3% in the mALI-low group and 62.5% in the mALI-high group, with a significant difference observed between the two groups (p=0.014) (Figure 1). A univariate analysis indicated that mALI may be a useful prognostic factor, while a multivariate analysis confirmed it as an independent prognostic factor [odds ratio (OR)=1.786, 95% confidence interval (CI)=1.145-2.785, p=0.011]. In terms of other clinicopathological factors, the univariate analysis identified T classification, lymph node metastasis, lymphatic invasion, and vascular invasion as significant prognostic factors, while the multivariate analysis ultimately recognized lymph node metastasis and vascular invasion as key prognostic indicators (Table II).

Figure 1.
Figure 1.

Overall survival of patients with esophageal cancer in the modified advanced lung cancer inflammation index (mALI)-high and mALI-low groups.

View this table:
Table II.

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

Recurrence-free survival (RFS). The RFS rates in the two groups were in line with the OS rates. The 5-year RFS rates in the high and low mALI groups were 44.9% and 33.0%, respectively (p=0.044) (Figure 2). mALI was also identified as a significant prognostic factor in the univariate analysis, and other identified prognostic factors included T classification, lymph node metastasis, lymphatic vessel invasion, and vascular invasion (Table III). However, in the univariate analysis, age, sex, and postoperative complications were not identified as prognostic factors. Furthermore, in the multivariate analysis, mALI was identified as an independent prognostic factor (OR=1.554, 95%CI=1.055-2.288, p=0.026). In addition, the multivariate analysis identified the T status and lymph node metastasis as independent prognostic factors.

Figure 2.
Figure 2.

Recurrence-free survival of patients with esophageal cancer in the modified advanced lung cancer inflammation index (mALI)-high and mALI-low groups.

View this table:
Table III.

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

Comparison of postoperative clinical course. When comparing the mALI-high and mALI-low groups in terms of recurrence patterns, there was no significant difference in lymph node recurrence between the two groups. However, the two groups showed a significant difference in hematological recurrence, with the mALI-low group experiencing a higher rate than the mALI-high group (34.5% vs. 19.6%, p=0.019) (Table IV).

View this table:
Table IV.

Patterns of recurrence according to Modified Advanced Lung Cancer Inflammation Index (mALI).

Discussion

This study aimed to clarify the utility of mALI as a prognostic factor for patients with EC who have undergone curative resection. In the survival analysis, the OS and RFS rates were significantly higher in the mALI-high group than in the mALI-low group. Additionally, the rate of hematogenous metastasis was significantly higher in the mALI-low group than in the mALI-high group. These findings suggest that mALI influences the oncological prognosis of patients with EC who have undergone radical resection.

The correlation between mALI and the oncological prognosis of patients with non-small cell lung cancer (NSCLC) has been reported in several prior studies. Sato et al. examined the correlation between mALI and long-term postoperative outcomes in 665 patients who underwent surgical lung resection for stage I-III NSCLC in 2024 (16). A total of 665 patients were assigned to the mALI-low group (168 patients) and mALI-high group (497 patients). Analysis of OS and RFS revealed differences between the mALI-high and mALI-low groups. Specifically, the mALI-high group exhibited a significantly higher 5-year OS and 5-year RFS compared to the mALI-low group. Furthermore, the multivariate analysis indicated that mALI is an independent prognostic factor for both OS and RFS.

However, within the scope of our research on mALI we could not identify any previous studies reporting the usefulness of mALI as a prognostic factor in patients with EC who had undergone curative surgical resection. The following is a report of a study that investigated the correlation between ALI and the oncological prognosis of patients with EC. In 2021, Tan et al. reported the correlation between ALI and the skeletal muscle index (L3SMI) at the third lumbar vertebra (L3) level in elderly patients with EC and the usefulness of each as a prognostic factor (17). They retrospectively analyzed the survival of 158 elderly patients with EC by dividing them into L3MI-high and L3MI-low groups. A logistic regression analysis showed that low L3MI was correlated with low ALI in patients with EC. In addition, the low L3MI and ALI groups had significantly lower OS in comparison to the high L3MI and ALI groups. Univariate and multivariate analyses showed that L3MI and ALI were independent prognostic factors in patients with EC. mALI is a factor that includes ALI and replaces BMI with L3MI, but there are several points to note regarding the relationship between mALI and the long-term prognosis of patients with EC.

First, anemia before surgery and perioperative blood transfusions may have had an effect. In this study, there were significant differences between the two groups in terms of anemia and blood transfusion. In comparison to the mALI-high group, the mALI-low group had a higher proportion of patients with Hb <11 g/dl before treatment (mALI-low group vs. mALI-high group, 27.4% vs. 9.8%, p=0.001). In addition, with regard to perioperative blood transfusions, the mALI-low group had a higher rate of cases that required blood transfusion during the perioperative period in comparison to the mALI-high group (mALI-low group vs. mALI-high group, 29.8% vs. 17.9%, p=0.005). Many studies have reported that preoperative anemia and perioperative blood transfusions affect the prognosis and survival rate of patients (18-20). Conor et al. retrospectively investigated 348 patients who underwent esophagectomy for EC and reported that anemia was associated with a poor survival rate in patients with EC in a multivariate analysis (21). They also considered that reducing the use of blood transfusions by accurately assessing anemia and adhering to strict transfusion guidelines could improve survival rates after EC surgery. In this study, the fact that preoperative anemia and perioperative blood transfusions were more common in the mALI-low group may have affected the oncological prognosis of EC. Another point to consider is that the salvage surgery rate was higher in the mALI-low group than in the mALI-high group (mALI-low group vs. mALI-high group, 21.4% vs. 4.5%, p<0.001). Jamel et al. compared the postoperative outcomes of patients with EC who underwent radical esophagectomy after preoperative chemoradiotherapy and those who underwent salvage surgery after radical chemoradiotherapy and found that the rate of anastomotic leakage (AL) was significantly higher in the salvage surgery group (22). Aoyama et al. have shown that anastomotic leakage in patients with EC who have undergone curative resection affects the prognosis of both OS and RFS (23). In this study, although there was no significant difference between the two groups, the rate of AL was higher in the mALI-low group than in the mALI-high group (mALI-low group vs. mALI-high group, 35.7% vs. 27.7%, p=0.229). Therefore, the high rate of salvage surgery in the mALI-low group may have led to an increase in anastomotic leakage, which in turn may have been associated with the worse oncological prognosis in patients with EC.

A third possible mechanism is that the mALI-low group had a higher rate of hematogenous metastasis than the mALI-high group. Hematogenous metastasis refers to the spread of cancer cells from the primary tumor site to the bloodstream and then to other organs. The prognosis of patients with EC is extremely poor when the tumor recurs or metastasizes (3, 4). The impact of neoadjuvant chemotherapy (NAC) and adjuvant chemotherapy on the postoperative clinical course and the improvement of the oncological prognosis of patients with EC has been demonstrated in multicenter, randomized trials, including JCOG9907 (24) and CheckMate577 (25). In this study, it is highly possible that NAC and adjuvant chemotherapy had an impact and led to a significant difference in hematogenous metastasis between the two groups. In this study, there was no significant difference in the rate of NAC or adjuvant use between the mALI-low and mALI-high groups (NAC: mALI-low group vs. mALI-high group, 52.4% vs. 47.3%, p=0.483; adjuvant: mALI-low group vs. mALI-high group, 36.9% vs. 33.9%, p=0.666). Therefore, further large-scale, multicenter cohort studies are needed in the future.

Study limitations. First, this was a retrospective study conducted at a single institution, and it was impossible to eliminate selection bias. In addition, the patients with EC included in this study were treated between 2000 and 2020, and there were various changes in the standard treatment during this period. For example, the treatment of esophageal cancer has changed significantly, with changes in the drug regimen for adjuvant and NAC and the addition of thoracoscopy, mediastinoscopy, and robotics to surgical approaches. In addition, there are now more treatment options for patients with recurrent EC and metastasis of EC, which may have affected the oncological prognosis of patients with EC in this study. Third, the optimal cutoff value for mALI is unclear. In this study, the cutoff value for mALI was set at 10 for males and 12 for females based on our analysis of OS. However, depending on the multidisciplinary treatment for esophageal cancer, number of patients, and patient background, the optimal cutoff value may differ from the value in this study. In future studies, it will be necessary to conduct further large-scale, multicenter cohort studies, considering the above limitations.

Conclusion

In conclusion, mALI may be a useful prognostic factor for the oncological outcomes of patients with EC who have undergone radical resection via mechanisms such as preoperative anemia, perioperative blood transfusions, salvage surgery, and hematogenous metastasis.

Acknowledgements

This study was supported in part by a nonprofit organization (YSRG).

Footnotes

  • Authors’ Contributions

    SY and TA contributed substantially to study design. TA, YM, IH, TI, SN, KO, KS, SY, RE, KK, KN, MU, and RH 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 March 9, 2025.
  • Revision received March 24, 2025.
  • Accepted March 26, 2025.

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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The Usefulness of the Modified Advanced Lung Cancer Inflammation Index (mALI) as a Prognostic Factor in Patients With Esophageal Cancer who Have Undergone Curative Resection
SOSUKE YAMAMOTO, TORU AOYAMA, YUKIO MAEZAWA, ITARU HASHIMOTO, RYUKI ESASHI, KAZUKI OTANI, SUGURU NUKADA, TETSUSHI ISHIGURO, KIYOKO SHIMADA, KEISUKE KAZAMA, KOJI NUMATA, MAMORU UCHIYAMA, REI HATAYAMA, AYAKO TAMAGAWA, AYA SAITO, NORIO YUKAWA
In Vivo Jul 2025, 39 (4) 2176-2185; DOI: 10.21873/invivo.14013
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