Research ArticleClinical Studies
Open Access

Association of Geriatric Nutritional Risk Index With Adverse Event and Treatment Duration in Adjuvant Chemotherapy for Patients With Colorectal Cancer

ATSUYA SHIMIZU, MIYU FUKASAWA, RYOSUKE ENDO, TAKUMI NAKAMURA, SHOGO YAMADA, RYO FUJIBAYASHI, KEN KIKUCHI, MASAOMI TANAKA, ISAO HASEGAWA and HIDEKI SATO
In Vivo January 2024, 38 (1) 453-459; DOI: https://doi.org/10.21873/invivo.13459

Abstract

Background/Aim: In recent years, the Geriatric Nutritional Risk Index (GNRI) has been reported as a predictor of prognosis in many patients with cancer. This study investigated the association of preoperative GNRI with the occurrence of adverse events and duration of treatment with capecitabine plus oxaliplatin (CAPOX), a postoperative adjuvant chemotherapy, in 59 patients with colorectal cancer from September 2019 to April 2022. Patients and Methods: A cut-off value of 100.9 was used to categorize patients into high and low GNRI groups. Results: The incidence of grade ≥2 leukopenia (p=0.03), and all grades peripheral neuropathy (p=0.04) were significantly more frequent in the low GNRI group. Analysis of factors influencing treatment duration by univariate and multivariate Cox regression proportional hazards models showed a significant difference in GNRI (p=0.0097). Conclusion: GNRI, a nutritional indicator assessed before the start of treatment, influences the occurrence of adverse events and duration of treatment with CAPOX as adjuvant chemotherapy. To complete CAPOX therapy, preoperatively, it is important to assess the patients’ nutritional status using the GNRI and to actively intervene in nutritional therapy.

Key Words:

In Japan, colorectal cancer was the leading cause of cancer incidence in 2019. In 2021, colorectal cancer ranked second in cancer-related deaths, but ranked first among women (1). Colorectal cancer is now treated with adjuvant chemotherapy to control recurrence after surgery; with oxaliplatin (OX) as the key drug and CAPOX [capecitabine 2,000 mg/m2/day on days 1-14; OX 130 mg/m2 on day 1, every 3 weeks (q3wks)] (2). Recently, preoperative nutritional status was reported to be associated with prognosis in patients with gastric cancer (3). Body weight loss prior to the start of cancer chemotherapy has also been reported to be associated with a lower median survival, and nutritional status before and during treatment is associated with resistance to treatment, incidence of adverse events, and other oncological outcomes (4, 5). Therefore, the assessment of nutritional status before postoperative chemotherapy is expected to ensure the safety and continuity of chemotherapy and improve the quality of life (QOL) and prognosis of patients with cancer. The Geriatric Nutritional Risk Index (GNRI) was developed by Bouillanne et al. (6) and has been reported to be a predictor of prognosis in many patients with cancer (7, 8). The nutritional status in the older adults should be assessed using a combination of blood test findings, such as serum albumin level (Alb) and anthropometric indicators (skeletal muscle mass and body fat mass). The GNRI also influences the outcomes of postoperative chemotherapy (4) and chemoradiotherapy in oncology. In the field of colorectal cancer, the association between preoperative GNRI and postoperative complications and prognosis has been investigated, with a lower preoperative GNRI reported to be associated with increased postoperative complications and poorer prognosis (9, 10). However, to date, no studies have investigated the association between the occurrence of adverse events, measured by the GNRI, and treatment duration, in postoperative adjuvant chemotherapy for colorectal cancer. This study investigated the association between preoperative GNRI, adverse event occurrence, and treatment duration in patients treated with CAPOX, a postoperative adjuvant chemotherapy for colorectal cancer.

Patients and Methods

From September 2019 to April 2022, 72 patients who underwent eight courses of CAPOX therapy as adjuvant chemotherapy for colorectal cancer at JR Sapporo Hospital, Hokkaido Gastroenterology Hospital, and Public Interest Association of Medical Service for Workers Kin-ikyo Chuo Hospital. Overall, 59 patients were included, excluding 13 patients who had missed two or more courses. A retrospective study of the patients’ background and occurrence of adverse events was conducted based on the electronic medical records of doctors, nurses, and pharmacists.

Patient characteristics included: sex, age, performance status (PS), height, body weight, body surface area (BSA), body mass index (BMI), serum creatine level (Scr), creatinine clearance (Ccr), estimated glomerular filtration rate (eGFR)/1.73 m2 corrected for BSA, uncorrected BSA eGFR, preoperative serum Alb levels, preoperative GNRI, OX dose, white blood cell count, neutrophil count, hemoglobin level, and platelet count in the immediate pre-dose period; adverse events included hematologic toxicity, nausea, vomiting, constipation, diarrhea, chemotherapy-induced peripheral neuropathy (CIPN), fatigue, and hand-foot syndrome (HFS). PS was assessed using the Eastern Cooperative Oncology Group (ECOG) rating scale (11).

Adverse events were assessed using the Common Terminology Criteria for AEs (CTCAE) ver 5.0. The onset of hematological toxicity was defined as the lowest toxicity during the treatment period. BMI was calculated as body weight in kilograms divided by height in meters squared. GNRI was calculated using the following formula:

Embedded Image

The study period was from the start date of CAPOX therapy to the end date of treatment.

This study was conducted in accordance with the “Ethical Guidelines for Medical Research Involving Human Subjects” and was approved by the Ethics Committee of Hokkaido University of Science (Approval No: 22-11). Owing to its retrospective nature, no written or oral consent was obtained from the research subjects. Information about the study was made available to the research subjects (posted in the hospital or on the hospital website), and the research subjects were guaranteed the opportunity to opt-out from participating in this study. We ensured that all patient confidential information were protected. The data were anonymized prior to handling.

Statistical analysis. Patients were divided into two groups, a high GNRI group and a low GNRI group, for comparison of quantitative data (including patient background, minimum hematologic toxicity, and grade of adverse event) using Student’s t-test, Mann-Whitney’s U-test, and Welch’s t-test, as appropriate. Welch’s t-test was used for comparisons of quantitative data for independence. Chi-square and Fisher’s exact probability test were used for comparisons of qualitative data. A p-value <0.05 was considered statistically significant. Treatment duration was analyzed using the Kaplan-Meier method, and differences were assessed using the log-rank test. In addition, confounders between factors, were eliminated if factors showed significant differences in the univariate analysis and were analyzed using the Cox proportional hazards model to obtain hazard ratios (HRs) and 95% confidence intervals (CIs); factors for treatment duration were also examined. In all cases, the significance level was set at less than 5%. For continuous variables, the cutoff values calculated from the receiver operating characteristic (ROC) curve were used. Excel Statistics ver. 4.04 (Social Information Service, Tokyo, Japan) was used for the statistical analysis.

Results

Table I presents the patient backgrounds. The area under the ROC curve for the GNRI was 0.5908, with a cut-off value of 100.9. Based on this cutoff value, the patients were classified into two groups, with 30 patients each in the high and low GNRI groups, respectively. Of the 59 patients, men (n=40) were significantly more (p=0.003). The mean age was 59.7±10.4 years in the high GNRI group and 64.8±10.6 years in the low GNRI group. PS was available only for patients with scores of 0 and 1. Body weight (p=0.01), BMI (p=0.02), and preoperative Alb level (p=0.01), were significantly lower in the low-GNRI group. Among the renal function-related laboratory values, the Scr showed no difference between groups; whereas eGFR/1.73 m2 (p=0.008) and eGFR (p=0.04) were significantly higher in the low GNRI group.

View this table:
Table I.

Characteristics of the study population.

There were no significant differences in the occurrence of nausea, vomiting, constipation, diarrhea, general malaise, or HFS between groups in any CAPOX therapy (Table II). In all grades of CIPN, the low GNRI group was significantly more prevalent (p=0.04). There were no significant differences in the occurrence of leukopenia, neutropenia, hemoglobin, or thrombocytopenia between the groups (Table III). There was a significant difference in grade ≥2 leukemia in the low GNRI group compared to the high GNRI group (p=0.03).

View this table:
Table II.

Hematologic toxicity.

View this table:
Table III.

Non-hematologic toxicity.

Table IV shows the results of univariate and multivariate Cox regression proportional hazard analyses of the factors influencing treatment duration. HRs and 95%CIs were determined using Cox proportional hazards regression analysis, with cutoff values from the ROC curves. The areas under the ROC curve for age, height, body weight, BSA, Scr, Ccr, eGFR/1.73 m2, eGFR, GNRI, and the first dose of OX were 0.5132, 0.6213, 0.5339, 0.5839, 0.5741, 0.5667, 0.5103, 0.5414, 0.5908, and 0. 5736; and the cut-off values were 63 years, 1.62 m, 55.9 kg, 1.63 kg/m2, 0.73 g/dl, 94.86 ml/min, 80.0 ml/min, 75.76 ml/min, 100.9, and 190 mg, respectively. The multivariate analysis was performed using variables with p<0.1 in the univariate analysis, including sex, height, body weight, GNRI, and first dose of OX. Significant differences were found in GNRI (HR=2.43, 95%CI=1.16-5.10, p=0.0097).

View this table:
Table IV.

Univariate and multivariate analyses using Cox proportional hazards models of time to treatment completion in colorectal cancer patients treated with adjuvant CAPOX.

When comparing the high and low GNRI groups, the treatment time required to complete eight courses of CAPOX was significantly longer in the low GNRI group (p=0.016) (Figure 1).

Figure 1.
Figure 1.

There were 30 patients who completed treatment. 23 patients were off medication for more than one week, of which 17 patients (74%) were in the low GNRI group and 6 patients (26%) in the high GNRI group, with a higher proportion in the low GNRI group.

Discussion

In the present study, we investigated the association between the occurrence of adverse events and duration of treatment with preoperative GNRI and CAPOX (a postoperative adjuvant chemotherapy regimen), in patients with colorectal cancer.

The GNRI was initially used for benign diseases and in the elderly, but is now also used in younger people, as it can be calculated simply from Alb level, height, and weight (12). Patients with colorectal cancer not only include older but also younger people; in this study, about half of the patients were in their 40s-50s; therefore, they could be assessed using the GNRI as well. The cutoff value for GNRI in this study was 100.9. According to the GNRI score interpretation by Bouillanne et al. (8), 98≤GNRI; 92≤GNRI<98; 82≤GNRI<92; and GNRI <82 refers to no, mild, moderate, and high nutritional risks, respectively. In a study predicting GNRI and cancer prognosis in patients with locally advanced rectal cancer undergoing radical surgery after chemoradiotherapy, Ide et al. (13) found a cut-off value of 104.25. Considering these factors, the GNRI cut-off value of 100.9 in this study is considered reasonable for use as a nutritional indicator.

The GNRI is a useful method for assessing nutritional status based on Alb and BMI. In this study, the high GNRI group had significantly higher BMI and preoperative Alb (p<0.001). Preoperative Alb in elderly patients undergoing gastrectomy has been reported to be an independent risk factor for postoperative pneumonia (14). Since malnutrition and cachexia are reflected in hypoalbuminemia in patients with cancer and hypoalbuminemia is reported to be correlated with a reduced immune response (15), Alb is considered a useful indicator of nutritional status. High Alb also contributes to improved survival of patients with cancer (16). Preoperative BMI has been reported as a predictor of outcomes after cancer resection in patients with lung cancer, with significantly higher survival rates in patients with a higher BMI than in those with a lower BMI (17, 18). GNRI has been shown to be an independent prognostic factor in postoperative patients with locally advanced rectal cancer who underwent curative surgery after preoperative chemoradiotherapy (13). In this study, the GNRI was also shown to be a factor influencing the duration of treatment, and a significant difference in the GNRI was observed in multivariate Cox regression proportional hazards analysis (p=0.0097). This indicates that GNRI before treatment initiation is a factor influencing treatment duration. This suggests that those in the high GNRI group had a good completion rate within a defined period of CAPOX therapy.

In terms of renal function, eGFR and eGFR/1.73 m2 were significantly higher in the low GNRI group (eGFR/1.73 m2: p=0.008, eGFR: p=0.04), but both the high and low GNRI groups had an eGFR/1.73 m2 between 60 and 90, and both were classified as having normal to mildly reduced renal function (19). Further data are needed to determine whether renal function has an impact on the continuation of treatment.

In terms of adverse events, hematologic toxicity did not differ significantly across all grades. However, grade ≥2 leukopenia was significantly more frequent in the low GNRI group (p=0.03). As leukopenia is one of the threshold values for the initiation of CAPOX therapy, more attention should be paid to leukopenia values during treatment. Non-hematologic toxicity was significantly more prevalent in the low GNRI group for CIPN in all grades (p=0.04). The aggravation of CIPN symptoms may reduce a patient’s QOL by producing sensory, motor, and autonomic neuropathy (20), thereby affecting the performance of CAPOX therapy. Reports of the efficacy of duloxetine and pregabalin in improving the symptoms of CIPN (21) exist (22). However, the efficacy is insufficient, and no treatment method has yet been established. This also suggests that early intervention and careful monitoring are needed to prevent CIPN deterioration, especially in patients with a low GNRI score.

The duration of CAPOX therapy was eight courses over 168 days. The time taken to complete treatment in the low GNRI group was significantly longer than 168 days when compared to the high GNRI group (p=0.016). This may be due to the fact that the low GNRI group had more leukopenia and CIPN adverse events, which prolonged the duration of treatment.

CIPN significantly reduces the patients’ QOL and is a dose-regulatory factor in OX (20), which may have affected the duration of treatment. As the GNRI before treatment initiation is an important factor for continuation without treatment discontinuation, an early response to CIPN and hematological toxicity are important for completion without withdrawal during treatment in the low GNRI group. In gastric cancer, it has been reported that improved preoperative nutritional status contributes to fewer postoperative complications and shorter hospital stays (3, 23). In colorectal cancer and liver metastases of colorectal cancer, preoperative nutritional status has also been reported to influence postoperative complications and survival (24-27), and to be a predictor of recurrence and poor prognosis in elderly patients with rectal cancer undergoing radical resection after preoperative chemotherapy (neoadjuvant chemotherapy) (28). Therefore, we believe that GNRI, a useful method of assessing nutritional status, is a factor that influences the duration of surgery and cancer chemotherapy treatment in gastric and colorectal cancer.

Similarly, in the present study, assessment of the nutritional status of patients using the GNRI preoperatively and the active nutritional therapy intervention were important for the completion of the postoperative adjuvant chemotherapy in colorectal cancer, using CAPOX therapy, without any withdrawal.

One limitation of this study was that it was a retrospective study with a small sample size (59 patients). In the future, more patients should be accumulated to investigate the association between GNRI and adverse events and the duration of treatment.

Conclusion

In patients with colorectal cancer, the preoperative GNRI has been suggested as a possible indicator of the occurrence of adverse events in postoperative adjuvant chemotherapy. There was also a statistically significant difference in the duration of treatment between the high- and low-GNRI groups, suggesting that it is a factor influencing the completion of CAPOX and postoperative adjuvant chemotherapy.

Footnotes

  • Authors’ Contributions

    Atsuya Shimizu conceived the study and drafted the original manuscript. Miyu Fukasawa, Shogo Yamada, Ryo Fujibayashi, and Ken Kikuchi made significant contributions to the design of the study and interpretation of the data. Ryosuke Endo, Takumi Nakamura, Maomi Tanaka, and Isao Hasegawa contributed to interpretation of the results. Hideki Sato supervised this study. Hideki Sato and other Authors contributed substantially to manuscript revision. All Authors have approved the submitted version of the manuscript and agreed to be accountable for any part of the study.

  • Conflicts of Interest

    The Authors have no conflicts of interest to declare in relation to this study.

  • Received August 29, 2023.
  • Revision received September 18, 2023.
  • Accepted September 19, 2023.

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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Association of Geriatric Nutritional Risk Index With Adverse Event and Treatment Duration in Adjuvant Chemotherapy for Patients With Colorectal Cancer
ATSUYA SHIMIZU, MIYU FUKASAWA, RYOSUKE ENDO, TAKUMI NAKAMURA, SHOGO YAMADA, RYO FUJIBAYASHI, KEN KIKUCHI, MASAOMI TANAKA, ISAO HASEGAWA, HIDEKI SATO
In Vivo Jan 2024, 38 (1) 453-459; DOI: 10.21873/invivo.13459
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