Research ArticleClinical Studies

Sarcopenia Is an Independent Prognostic Factor for Squamous Cell Carcinoma of the Cervix Treated With Concurrent Chemoradiotherapy

SHINYU KISE, YOSHIHISA ARAKAKI, WATARU KUDAKA, TAKURO ARIGA, NAGISA KINJO, HIROSHI KOHATU and YOICHI AOKI
Anticancer Research October 2022, 42 (10) 4887-4893; DOI: https://doi.org/10.21873/anticanres.15994

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Abstract

Background/Aim: To investigate sarcopenia as a predictor of prognosis before concurrent chemoradiotherapy (CCRT) in patients with squamous cell carcinoma (SCC) of the cervix using the new psoas muscle index (PMI) cutoff value for sarcopenia in Japanese women. Patients and Methods: We included 134 patients with SCC of the cervix treated with CCRT. CT images were taken within one month before treatment. Measurements of PM and skeletal muscle (SM) area were taken at the L3 level using a CT image analysis system (Synapse Vincent). Whole-pelvic external beam radiotherapy (EBRT) with 50 Gy was performed. High-dose-rate intracavitary brachytherapy and boost EBRT doses were administered. The patients received 40 mg/m2 of cisplatin weekly during CCRT. Kaplan-Meier analysis and the log-rank test were used to compare survival rates. Results: The five-year overall survival (OS) and five-year progression-free survival of all 134 patients were 86.1% and 77.3%, respectively. Univariate analysis revealed that only PMI had a significant association with OS (PMI <3.92 cm2/m2 in the sarcopenia group vs. PMI ≥3.92 cm2/m2 in the non-sarcopenia group, p=0.0112), with no significant differences in age, advanced stage of disease, tumor size, lymph node enlargement, serum SCC, or SMI. Multivariate analysis revealed that PMI is the only independent prognostic factor for OS, but none of the factors were found to have a significant association with PFS. Conclusion: PMI as an indicator of sarcopenia was found to be an independent prognostic factor for patients with SCC of the cervix who underwent CCRT.

Key Words:

Cancer cachexia is a multifactorial syndrome characterized by progressive loss of skeletal muscle mass that cannot be completely reversed with conventional nutritional support, leading to progressive functional disability (1). Sarcopenia, a form of cancer cachexia, is divided according to its etiology into two categories: primary sarcopenia (i.e., loss of muscle mass associated with aging) and secondary sarcopenia (i.e., loss of muscle mass associated with disuse atrophy and undernutrition due to low levels of activity, organ failure, invasion, tumors, or other diseases) (2). With the aging of patients in recent years, preoperative sarcopenia has been severally reported to be a poor prognostic factor, especially for gastrointestinal diseases (3, 4). Further, a significant association was reported between sarcopenia and mortality due to respiratory diseases (5). Regarding gastroenterological cancers, it was reported that sarcopenia is a poor prognostic factor for overall survival in pancreatic (6) and rectal cancer (7). Skeletal muscle loss is reported to be associated with overall survival in patients with advanced ovarian cancer (8). In several studies on sarcopenia, computed tomography (CT) was used as a uniform assessment method to define and assess low skeletal muscle mass; for example, it was used to measure the area of the iliopsoas and skeletal muscles at the level of the third lumbar vertebra (L3) (9, 10). The values obtained were denoted as PM for the iliopsoas and SM for skeletal muscles. These values were further divided by the square of the height to eliminate the effect of body size, and the resulting values were denoted as PM index (PMI) and SM index (SMI) for the iliopsoas and skeletal muscles, respectively.

Regarding gynecological cancers, sarcopenia is reported to be a risk factor of surgical complications and early mortality in patients with endometrial and ovarian cancers (11), and it is associated with poor outcomes, including decreased survival in patients with metastatic breast cancer (12). Regarding the association between concurrent chemoradiotherapy (CCRT) for cervical cancer and sarcopenia, Kiyotoki et al. (13) and Lee et al. (14) reported that decrease in muscle mass during treatment reflects prognosis; however, since prognosis cannot be estimated before treatment, there are questions regarding the clinical usefulness of this association.

The aim of this study was to investigate sarcopenia as a predictor of prognosis before CCRT initiation in patients with squamous cell carcinoma (SCC) of the cervix using the new PMI cutoff value for sarcopenia in Japanese women (10).

Patients and Methods

Patients. We included 134 patients with SCC of the cervix [stage IB to stage IVA, excluding stage IIIC2 with para-aortic lymph node enlargement, reclassified according to the International Federation of Gynecology and Obstetrics (FIGO) 2018 classification] who underwent CCRT as curative radiotherapy at our institution between January 2010 and December 2016. The treatment is briefly described below. Whole-pelvis external beam radiotherapy (EBRT) with 50 Gy (25 fractions) was performed using the anteroposterior–posteroanterior or four-field technique with a center shield at midline after delivering a 40-Gy dose. High-dose-rate intra-cavitary brachytherapy and boost EBRT doses were administered. The patients received 40 mg/m2 of cisplatin (CDDP) weekly over the course of the CCRT. Only patients who underwent CT within one month prior to the start of treatment were included.

The Common Terminology Criteria for Adverse Events version 5.0 was used to assess adverse events during the treatment period. The patient background characteristics included age, height, weight, FIGO stage, tumor diameter, presence of enlarged lymph nodes, serum SCC antigen level, total CDDP dose, and duration of CCRT.

Measurements of SM and PM area by CT images. CT images taken within one month prior to the start of treatment were used; CT images were standardized with a slice thickness of 5 mm. Measurements of SM and PM area were taken at the L3 level. Analysis was performed using a CT image analysis system (Synapse Vincent; Fujifilm Medical, Tokyo, Japan). Muscles were defined based on CT values of −29 to +150 Hounsfield units. We defined sarcopenia as SMI less than 38.5 cm2/m2, as proposed by Prado et al. (5), and PMI less than 3.92 cm2/m2, as proposed by Hamaguchi et al. (10). In addition, body mass index (BMI) less than 22 kg/m2, which is regarded as appropriate by the Japan Society for the Study of Obesity, was used in the determination of sarcopenia.

Statistical analyses. Regarding statistical analyses, continuous data were expressed as medians and ranges, and categorical data were expressed as numbers and percentages. The distribution of clinical characteristics was compared using Mann-Whitney U-test and χ2 test. Survival was measured from the date of treatment initiation to the date of death or last follow-up. Kaplan-Meier method was used to calculate actual rates, and log-rank test was used to compare survival rates between groups. Multivariate analysis of all variables was performed using Cox proportional hazards regression model. Data were analyzed using JMP version 15 (SAS Institute, Cary, NC, USA). p<0.05 was considered statistically significant.

Ethical issues. This retrospective study was conducted according to the principles stated in the 1964 Declaration of Helsinki and subsequent revisions and was approved by the Institutional Review Board of our university on June 25, 2018 (#2018-1304). We used the opt-out method to obtain consent from the patients.

Results

The clinicopathological background characteristics of the 134 patients are shown in Table I. The median age was 49 (range=22-72) years. Forty-eight patients had FIGO stage IB or stage II disease, and 86 patients had stage IIIB or a higher stage of disease. The median tumor diameter was 51.5 (range=23-112) mm. There were 68 patients with enlarged lymph nodes, and 66 patients without enlarged lymph nodes. The median serum SCC antigen level was 6.5 (range=0.7-168) ng/ml. The median BMI was 22.0 (range=13.3-36.2) kg/m2, the median SMI was 41.5 (range=30.1-59.0) cm2/m2, and the median PMI was 3.88 (range=1.39-6.95) cm2/m2. The median total CDDP dose was 306.9 (range=52.1-550.2) mg, and the median duration of CCRT was 49 (range=36-74) days. The prognosis was no evidence of disease (NED) in 106 patients, alive with disease (AWD) in nine patients, dead of disease in 18 patients, and dead of intercurrent disease in one patient. The median follow-up duration was 60 (range=2-124) months.

View this table:
Table I.

Patient characteristics (N=134).

Table II shows the overall survival (OS) and progression-free survival (PFS) for each clinicopathological factor. The five-year OS and five-year PFS of all 134 patients were 86.1% and 77.3%, respectively. Univariate analysis revealed that only PMI has a significant association with OS (PMI <3.92 cm2/m2 in the sarcopenia group versus PMI ≥3.92 cm2/m2 in the non-sarcopenia group, p=0.0112), with no significant differences in age, advanced stage of disease, tumor size, lymph node size, serum SCC antigen level, BMI, or SMI. Multivariate analysis revealed that PMI is the only independent prognostic factor for OS (p=0.0265), but none of the factors were found to have a significant association with PFS (Table III).

View this table:
Table II.

Univariate analysis for overall survival and progression-free survival.

View this table:
Table III.

Cox proportional hazard model for overall survival and progression-free survival.

Comparison of background characteristics between the two groups is shown in Table IV. Tumor stage III/IV (FIGO 2018) was found to be significantly more common in the sarcopenia group (50 out of 68 patients) than in the non-sarcopenia group (36 out of 66 patients) (p=0.030). Further, between the sarcopenia and the non-sarcopenia groups, there were no significant differences in median tumor diameter [53 (range=23-110) mm vs. 50 (range: 25-112) mm, p=0.070], frequency of enlarged lymph nodes (54.4% vs. 47.0%, p=0.490), and serum SCC antigen level (7.25 ng/ml versus 5.6 ng/ml, p=0.347). Regarding treatment intensity, between the sarcopenia and non-sarcopenia groups, there were no significant differences in total CDDP dose (309.9 mg vs. 303 mg, p=0.977) and duration of CCRT [47 (range=36-65) days vs. 48.5 (range=40-74) days, p=0.352); in contrast, there were significant differences in BMI, SMI, and PMI (p=0.0049, p<0.0001 and p<0.0001, respectively).

View this table:
Table IV.

Patient characteristics by psoas muscle mass index (PMI).

Table V shows the frequency of grade 3 or higher adverse events in the two groups, with no significant differences between the groups. The most common adverse event was neutropenia, which occurred in 17 patients (25%) in the sarcopenia group and in 20 patients (30.3%) in the non-sarcopenia group.

View this table:
Table V.

Grade 3, 4 adverse events.

Furthermore, there was no significant difference in the number of patients with post-treatment residual/recurrent disease between the sarcopenia and non-sarcopenia groups (18 patients vs. 13 patients, p=0.415). However, the number of patients with NED and AWD after post-recurrent treatment was significantly lower in the sarcopenia group than in the non-sarcopenia group (4 patients vs. 9 patients, p=0.013). Kaplan-Meier curves were used to analyze OS and PFS in the two groups. Five-year OS was 78.8% in the sarcopenia group and 93.8% in the non-sarcopenia group (p=0.011) (Figure 1a), and five-year PFS was 73.3% in the sarcopenia group and 79.9% in the non-sarcopenia group (p=0.389) (Figure 1b). Although there were no differences in treatment intensity or adverse events between the two groups, the course of treatment after recurrence was thought to be the cause of the significant difference in OS between the groups.

Figure 1.
Figure 1.

(A) Kaplan-Meier curves showing that five-year overall survival is significantly lower in the sarcopenia group compared to the non-sarcopenia group (78.8% vs. 93.8%, p=0.011). (B) Kaplan-Meier curves showing no significant difference in five-year progression-free survival between the sarcopenia and non-sarcopenia group (73.3% vs. 79.9%, p=0.389).

Discussion

In this study, PMI as an indicator of sarcopenia was found to be an independent prognostic factor for patients with SCC of the cervix who underwent CCRT. In previous studies, the association between sarcopenia and prognosis of patients with cervical cancer who underwent CCRT was investigated, but there was bias in the patient background characteristics, including histological type of cancer and irradiation range (15, 16). Since patients with enlarged para-aortic lymph nodes (17) and non-squamous carcinoma (18) are considered to have a poor prognosis, in this study, we focused on patients with SCC as the only histological type, anterior total pelvis irradiation as the only irradiation range, and CDDP as the only chemotherapy regimen, as we consider these characteristics appropriate for prognostic evaluation in relation to sarcopenia.

To determine sarcopenia, it is necessary to evaluate three factors: muscle mass, muscle strength and physical function. Muscle strength is assessed using grip strength, and physical function is assessed using walking speed. In contrast, muscle mass is assessed using CT scan, which guarantees high objectivity regardless of the measurer or the time of measurement. Regarding criteria for low skeletal muscle mass using CT scan, SMI, which is the total skeletal muscle mass at the L3 level divided by the square of height (38.5 cm2/m2 in women), is an indicator of sarcopenia, as reported in the study by Prado et al. (5). However, since the study involved Canadian subjects and patients with respiratory and gastrointestinal cancers, it is necessary to determine whether SMI is an appropriate criterion for Japanese patients with cervical cancer. Given that there was no standard indicator of low skeletal muscle mass on CT scan in the Japanese population, Hamaguchi et al. (10) developed and proposed a PMI cutoff value of 3.92 cm2/m2 for healthy adult Japanese women. In the prognostic analysis of BMI of 22 kg/m2, SMI of 38.5 cm2/m2, and PMI of 3.92 cm2/m2 before CCRT initiation in this study, only PMI was found to be an independent prognostic factor of sarcopenia. This finding suggests that PMI is a useful indicator of low skeletal muscle mass and sarcopenia in patients with SCC of the cervix who underwent CCRT.

In a previous study by Kiyotoki et al. (13) that evaluated patients with cervical cancer who underwent CCRT, sarcopenia was defined as muscle loss of at least 15% of PM from baseline before CCRT, and they reported that sarcopenia is a poor prognostic factor for OS and PFS in patients undergoing CCRT. Lee et al. (14) reported that sarcopenia is defined as SMI less than 41.0 cm2/m2, citing a weak correlation between PM and total lumbar muscle area as rationale for using SMI instead of PMI. However, SMI was not considered a prognostic factor, and patients whose SMI decreased by more than 10% at 150 days after the start of treatment had poor prognosis. The rationale for defining sarcopenia as SMI less than 41.0 cm2/m2 was reported in the study by Rutten et al. (19), but it is difficult to judge the appropriateness of this criterion in Japanese patients with cervical cancer since the study evaluated Dutch patients with ovarian cancer. Our study is the first study to report PMI less than 3.92 cm2/m2 before CCRT in patients with SCC of the cervix as an indicator of sarcopenia and a poor prognostic factor.

However, comparison of the clinical background characteristics of the groups revealed significantly higher cases of stages IIIB and IVA disease in the sarcopenia group than in the non-sarcopenia group; however, when the sarcopenia criterion was divided into two groups based on BMI of 22 kg/m2 and SMI of 38.5 cm2/m2, distribution was not significantly different (p=0.280 and 0.854, respectively). The sarcopenia criterion based on PMI tends to concentrate more advanced cases in the sarcopenia group and is therefore considered an index of interest. In this study, there was no difference in prognosis between advanced stages IB and II and stages IIIB and IVA, with OS of 87.3% and 85.5%, respectively (p=0.735) and PFS of 85.3% and 72.8%, respectively (p=0.124) (Table II). Furthermore, multivariate analysis revealed that FIGO stage is not a significant prognostic factor, and that PMI is the only independent prognostic factor for OS (Table II).

Multivariate analysis also revealed that PMI is not a significant prognostic factor for PFS, even though it is a significant prognostic factor for OS. This finding is explained by the non-significant difference in the number of patients with post-treatment residual/recurrent disease between the sarcopenia and non-sarcopenia groups [18 patients (26.4%) and 13 patients (19.7%), respectively, p=0.415] and the significantly higher number of patients with NED and AWD after post-recurrent treatment in the non-sarcopenia group compared to the sarcopenia group [four patients (22.2%) vs. nine patients (69.2%), p=0.013]. These findings may be because more patients did not respond to post-recurrent treatment and had an inadequate course of post-recurrent treatment in the sarcopenia group than in the non-sarcopenia group. Although there were no differences in the intensity of initial treatment or in adverse events between the two groups, sarcopenia may have affected the implementation and effectiveness of post-recurrent treatment, resulting in a significant difference in OS between the groups.

The strengths of this study are that the patient sample size is larger than in previous studies and the study was conducted in the same population, with SCC as the only histological type, whole-pelvic irradiation as the only irradiation field, and CDDP as the only chemotherapy regimen. In addition, we showed PMI of less than 3.92 cm2/m2 to be a new sarcopenia index and demonstrated its usefulness. The limitation of this study is its retrospective design.

If PMI is used to diagnose sarcopenia, nutrition and rehabilitation interventions should be considered for the patients. Many intervention studies on exercise or nutrition for sarcopenia have been conducted, and meta-analyses have shown that exercise, especially resistance exercise, is effective (20). The NEXTAC-TWO randomized trial by a collaborative research group evaluating patients with non-small cell lung or pancreatic cancer who are at least 70 years old and undergoing first-line chemotherapy is currently underway and is attracting attention (21). In the study, patients were randomized to a chemotherapy group or a treatment group that adds nutritional therapy and exercise therapy to chemotherapy (21). In the future, sarcopenia should be evaluated in patients with cancer, and a holistic approach of care administered by different healthcare professionals should be considered.

Acknowledgements

The authors would like to thank Enago (www.enago.jp) for the English language review of this article.

Footnotes

  • Authors’ Contributions

    The work presented herein was carried out in collaboration among all Authors. SK, YA, and YA made substantial contribution to the conception, designed methods, interpreted the results, and wrote the manuscript. KS, YA, WK, TA, NK, HK, and YA engaged in data acquisition and analyzed the data. SK, YA, and YA substantively revised the manuscript. All Authors have read the manuscript and have approved this submission.

  • Conflicts of Interest

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

  • Received July 8, 2022.
  • Revision received July 25, 2022.
  • Accepted August 8, 2022.

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Sarcopenia Is an Independent Prognostic Factor for Squamous Cell Carcinoma of the Cervix Treated With Concurrent Chemoradiotherapy
SHINYU KISE, YOSHIHISA ARAKAKI, WATARU KUDAKA, TAKURO ARIGA, NAGISA KINJO, HIROSHI KOHATU, YOICHI AOKI
Anticancer Research Oct 2022, 42 (10) 4887-4893; DOI: 10.21873/anticanres.15994
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