Abstract
Background/Aim: Malignant bone tumors (MBT) and soft tissue sarcomas (STS) require wide excision. Although the number of elderly patients is increasing, wide excision may decrease limb function and quality of life (QOL) for elderly patients. However, no detailed evaluation of the functional prognosis or QOL of elderly patients with sarcoma has been reported. This study evaluated postoperative limb function and QOL in elderly patients with MBT and STS. Patients and Methods: This retrospective study included 67 patients aged >70 years with MBT or STS who underwent surgery at a single institution. The Toronto Extremity Salvage Score (TESS), EuroQoL 5-dimension 5-level (EQ-5D-5L) questionnaire, Musculoskeletal Tumor Society (MSTS) score, and psoas muscle index (PMI) were evaluated. We also assessed factors associated with the postoperative TESS and EQ-5D-5L index. Results: Detailed examination of the MSTS items perioperatively revealed significant decline in manual dexterity/walking ability and support but significant improvement in pain and emotional acceptance. The mean PMI decreased significantly from 4.7 to 4.23 perioperatively. The postoperative mean TESS and EQ-5D-5L index was 76.9 and 0.74, respectively. Patients with good performance status and clinical frailty scale scores preoperatively had better postoperative TESS and EQ-5D-5L scores. Conclusion: The current study strongly suggests the possibility of maintaining postoperative limb function, satisfaction, and QOL in patients with MBT and STS by choosing patients in good condition and the appropriate procedure that the patient desires. However, perioperative progression of sarcopenia should be noted.
Malignant bone tumors (MBT) and soft tissue sarcomas (STS) are rare tumors that occur from children to the elderly (1). With the ageing population, the number of elderly patients with MBT and STS is expected to increase (2). Treatment of MBT and STS involves wide excision, chemotherapy, and radiotherapy. Distant metastasis of sarcomas is also common, and its prognosis is extremely poor due to distant metastasis. Although the treatment of sarcomas has focused on prognosis, the importance of postoperative limb function and quality of life (QOL) has also been reported in recent years.
The Toronto Extremity Salvage Score (TESS) and Musculoskeletal Tumor Society (MSTS) scores are useful for evaluating postoperative limb function in patients with cancer and sarcoma (3, 4). Some reports have shown that postoperative limb function is compromised in young patients undergoing MBT and STS with a wide excision (5). On the other hand, the EuroQoL 5-dimension 5-level (EQ-5D-5L) questionnaire is frequently used for the perioperative evaluation of QOL in patients with MBT and STS (6).
Wide excision may lead to decreased limb function and QOL in elderly patients with MBT and STS compared to young patients because of the original low muscle mass and reduced activity. Muscle resection in elderly patients can contribute to sarcopenia and frailty. Although there are many reports on prognosis of elderly patients with sarcoma after multidisciplinary treatment (7), no detailed evaluation of the functional prognosis or QOL of elderly patients with MBT and STS has been reported.
Therefore, the objective of the current study was to evaluate postoperative limb function and QOL in elderly patients with MBT and STS by assessing MSTS scores, TESS, EQ-5D-5L, and sarcopenia. We also evaluated factors associated with TESS and the EQ-5D-5L index postoperatively.
Patients and Methods
Study design and patients. Approval was obtained from the review board of the Chiba Cancer Center, and informed consent was obtained from each patient. We retrospectively reviewed our Institution’s database of 310 patients with MBT and STS aged >70 years who underwent surgery between April 2006 and March 2022. Among them, patients who were unable to answer the TESS and EQ-5D-5L questionnaires and were under the 6 months follow-up period were excluded. Ultimately, 67 patients were included in this study.
Clinical characteristics and parameters for investigation. We investigated the following: sex, age at operation, follow-up period after surgery, type of sarcoma, tumor site, histology, surgical technique, surgical margin, use of chemotherapy and radiotherapy, local recurrence, distant metastasis, performance status, and clinical frailty scale score at operation. The surgical margin was microscopically categorized. A negative margin (R0 resection) was defined as the absence of tumor cells at the margin, and a positive margin (R1 resection) was defined as the presence of tumor cells at the closest margin. Macroscopic residual tumor after surgery was defined as an R2 resection. The objective perioperative function was evaluated using the MSTS score preoperative and 6 months postoperatively. The MSTS consists of six items: pain, function, emotional acceptance, hand positioning (upper limb)/support (lower limb), manual dexterity (upper limb)/walking ability (lower limb), and lifting ability (upper limb)/gait (lower limb) (1). Skeletal muscle volume was calculated using the psoas muscle index (PMI) based on CT images taken preoperatively and 6 months postoperatively, according to previously described methods (8). The sum of the L3 level cross-sectional area of the right and left psoas muscles was calculated, and the value was divided by the height squared (cm2/m2).
Furthermore, the subjective QOL and limb function after surgery were evaluated using the EQ-5D-5L and TESS questionnaires at the final follow-up. The descriptive system of EQ-5D-5L for QOL evaluation comprises five dimensions: mobility, self-care, usual activities, pain/discomfort, and anxiety/depression, each with five levels: no problems, slight problems, moderate problems, severe problems, and extreme problems (9). The TESS, a self-administered questionnaire, is widely used for the functional assessment of patients after surgery for musculoskeletal tumors (3, 4). The clinical frailty scale proposed by Rockwood et al. is shown in Table I (10, 11). Furthermore, we evaluated Eastern Cooperative Oncology Group (ECOG) performance status, as indicated in previous literature (12).
Clinical frailty scale.
Statistical analysis. Patient data were entered into a database. All data with rejected normality were evaluated using the Mann–Whitney U-test, whereas those with accepted normality were analyzed using an independent t-test and analysis of variance (ANOVA). Differences were considered statistically significant when the p-values were less than 0.05. All analyses were performed using the SAS software, version 14.2 (SAS Institute, Inc., Cary, NC, USA).
Results
Patients. Data regarding the patient and tumor characteristics are presented in Table II. There were 34 males and 33 females. The mean age at surgery and follow-up period after surgery was 78 years (range=70-95 years) and 38 months (range=6-120 months), respectively. A total of 8 and 59 patients were diagnosed with MBT and STS, respectively. The tumors were located in the upper limbs (13 patients), lower limbs (39 patients), and trunk (15 patients). Histological tumor subtypes included undifferentiated pleomorphic sarcoma (n=18), myxofibrosarcoma (n=16), liposarcoma (n=10), and chondrosarcoma (n=8). Wide excision (64 cases), wide excision with a prosthesis (1 case), shoulder girdle dissection (1 case), and above-knee amputation (1 case) were performed. The surgical margins were R0, R1, and R2 in 45, 18, and 4 patients, respectively. Perioperative chemotherapy and radiotherapy were administered in 15 and 23 patients, respectively. Local recurrence and distant metastasis occurred in 8 and 11 patients, respectively. The performance status at surgery was grade 0, 1, 2, and 3 in 12, 33, 20, and 2 cases, respectively, not including grades 4 and 5. The clinical frailty scale scores at operation were 1, 2, 3, and 4 in 4, 30, 23, and 10 cases, respectively, excluding grade >5.
Patient demographics and disease characteristics.
Perioperative MSTS score and PMI. The mean MSTS scores preoperatively and postoperatively were 76.3 (range=33-96) and 75.5 (range=43-100), respectively. There was no significant difference between them (Figure 1). Detailed examination of the MSTS items revealed significant declines in manual dexterity/walking ability and support but significant improvements in pain and emotional acceptance. Next, psoas muscle mass was assessed during the perioperative period. The mean preoperative and postoperative PMI of all cases were 4.7 (range=2.03-7.94) and 4.23 (range=1.72-7.32), respectively. There was a significant difference among them (Figure 2). Among men, the mean preoperative and postoperative PMI were 5.43 (range=3.68-7.94) and 4.82 (range=2.77-7.32), respectively. Furthermore, among women, the mean preoperative and postoperative PMI were 4.1 (range=2.03-7.09) and 3.57 (range=1.72-6.74), respectively. Both groups showed significant perioperative differences. This study did not include patients who underwent psoas muscle resection.
Perioperative MSTS score. Overall, the MSTS scores did not change postoperatively. Although manual dexterity, walking ability, and support worsened, pain and emotional acceptance improved. MSTS: Musculoskeletal Tumor Society; ns: not significant.
Perioperative PMI. The mean total, male and female PMI significantly worsened postoperatively. PMI: Psoas muscle index.
Factors associated with the postoperative TESS and EQ-5D-5L index. The postoperative mean TESS and EQ-5D-5L index were 76.9 (range=23.1-100) and 0.74 (range=0.04-1), respectively (Table III). We evaluated the factors associated with postoperative TESS and EQ-5D-5L, including age, tumor location, chemotherapy, radiotherapy, local recurrence, distant metastasis, preoperative performance status, and clinical frailty scale. Among them, patients with good scores on the preoperative performance status (score 0-1) and clinical frailty scale (score 1-2) had significantly better postoperative TESS, suggesting good postoperative limb function. Similarly, although there was no significant difference, patients with good preoperative performance status (score 0-1) and clinical frailty scale (score 1-2) had better postoperative EQ-5D-5L indexes, suggesting the possibility of good postoperative QOL.
Factors associated with the postoperative TESS and EQ-5D-5L index.
Discussion
The current study evaluated postoperative limb function and QOL in elderly patients with MBT and STS who underwent wide excision using the MSTS, TESS, and EQ-5D-5L questionnaires. Overall, the MSTS scores did not change postoperatively. Although manual dexterity, walking ability, and support worsened, pain and emotional acceptance improved. Furthermore, patients in good general condition preoperatively had a better postoperative functional prognosis and QOL. However, muscle atrophy progressed perioperatively.
There are limited reports on postoperative limb function and QOL for MBT and STS with MSTS and TESS evaluations. Table IV shows the comparative data from other studies (13-18). In a systematic literature review, Gilber et al. reported that the mean TESS and MSTS scores of patients with lower-extremity STS treated with surgery were 83.3 and 86.2, respectively (19). Although postoperative function is expected to be worse in older adults, the results of the current study were comparable to previous MSTS and TESS results at various ages. Regarding the MSTS items, elderly patients still showed a marked deterioration in postoperative limb ability, increasing orthotics and support. However, pain and emotional acceptance improved, and removing the MBT and STS improved satisfaction. Removing the MBT and STS with a wide excision should be an option, even for elderly patients.
Comparative data from other published studies on postoperative limb function and QOL for MBT and STS with MSTS, TESS, and EQ-5D-5L evaluations.
However, few reports have examined the EQ-5D-5L in the MBT and STS (Table IV). Tanaka et al. reported that the median EQ-5D score after extensive resection of STS of the thigh at various ages was 0.782 (17). Izawa et al. investigated the psychological and physical states of elderly patients who underwent outpatient rehabilitation at a geriatric health service facility using the EQ-5D-5L. The mean EQ-5D-5L was 0.69 for males (mean 82.3 years) and 0.77 for females (mean 84.6 years) without cancer and surgery at a geriatric health services facility (20). These reports suggest that the 0.74 points of EQ-5D-5L scores in the current study of the elderly were comparable to the results of various ages. However, there are other QOL evaluations, such as the SF-36, and further evaluations using various modalities are required.
In univariate analysis, patients with better postoperative functional prognosis had a preoperative performance status of 0-1 and clinical frailty scale of 1-2, i.e., they had a good preoperative general condition. In contrast, patients in good preoperative general condition had a better postoperative QOL, although the difference was insignificant. Based on these results, we believe that preoperative evaluation of a patient’s general condition is indispensable when considering the indications for surgery.
However, the choice of surgical technique for elderly patients is difficult. In elderly patients, the functional prognosis may take precedence over survival prognosis, and marginal excision, rather than wide excision, may be performed if the tumor is close to a major nerve or blood vessel. In the current study, the surgical margins of R0, R1, and R2 were 45, 18, and 4 cases, respectively, and R1 and R2 were relatively common. However, although we proposed marginal excision with priority given to functional prognosis, some elderly patients preferred amputation to achieve a local radical cure.
An 86-year-old woman desired shoulder girdle dissection and was continuously disease-free for 20 months postoperatively. Although her postoperative function was poor, with an MSTS score of 46% and TESS of 44%, her EQ-5D-5L score was relatively good at 0.729. Furthermore, a 77-year-old woman who wanted an above-knee amputation had no local recurrence or metastasis for 40 months postoperatively. Although her postoperative MSTS score (57%) and TESS (61%) were low, her postoperative QOL was relatively good, with an EQ-5D-5L score of 0.78. Postoperative satisfaction and QOL can be maintained even in elderly patients by definitive radical surgery. The optimal surgical technique should be selected after informed consent is obtained from the patient.
However, sarcopenia was significantly more advanced in elderly patients in the current study. Hamaguchi et al. determined the sex-specific cutoff values for low skeletal muscle mass of PMI as 6.36 cm2/m2 for men and 3.92 cm2/m2 for women (21). In the current study, the mean preoperative and postoperative PMI decreased from 5.43 cm2/m2 to 4.82 cm2/m2. Similarly, among women, mean PMI decreased perioperatively from 4.1 cm2/m2 to 3.57 cm2/m2. Based on Hamaguchi et al. criteria, both men and women in the current study were considered to have worsened, leading to sarcopenia. These results suggest that aggressive rehabilitation is necessary to prevent sarcopenia and frailty in elderly patients undergoing MBT and STS.
The current study had certain limitations. First, it was a retrospective study. Second, the EQ-5D-5L and TESS scores were not evaluated preoperatively, and changes over time could not be assessed. Finally, only the surviving patients were selected because the postoperative questions were patient-reported outcomes. The mean 6 months postoperative MSTS score of patients who were unable to answer the TESS and EQ-5D-5L questionnaires with MBT and STS aged >70 years who underwent surgery our institution was similar to those of 67 patients included in the current study, with no significant differences. However, more detailed investigation is needed by prospective studies including patient-reported outcomes in the future.
In conclusion, we evaluated the postoperative limb function and QOL in elderly patients with MBT and STS who underwent wide excision. The current study strongly suggests the possibility of maintaining postoperative limb function, satisfaction, and QOL in patients with MBT and STS by choosing patients in good condition and the appropriate procedure that the patient desires. However, active postoperative rehabilitation interventions are important because of the possibility of rapid progression of sarcopenia in elderly patients.
Acknowledgements
This work was supported by JSPS KAKENHI grants (19K16760), the Kato Memorial Bioscience Foundation, and the Mother and Child Health Foundation. We would like to thank Editage (www.editage.com) for English language editing.
Footnotes
Authors’ Contributions
H. K. designed and performed the experiments, analyzed the data, and wrote the article. S. K., Y. H., H. K., S. O., and T. Y. provided technical support and conceptual advice.
Conflicts of Interest
The Authors declare no conflicts of interest directly relevant to the content of this article.
- Received April 19, 2023.
- Revision received May 14, 2023.
- Accepted May 29, 2023.
- Copyright © 2023 International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.








