ABSTRACT
Objective: The objective of the current study was to find the factors
affecting the activities of daily living, as evaluated by the Barthel Index, at the end of
rehabilitation after musculoskeletal tumour surgery. Further, we evaluated whether the
Barthel Index correlates with functional scores that are specific to musculoskeletal
tumours at final follow-up. Methods: The activities of daily living of 190
patients who underwent postoperative rehabilitation after surgery to treat musculoskeletal
tumours were evaluated at the end of the program using the Barthel Index. Functional
evaluation at the time of final follow-up observation was evaluated using the
Musculoskeletal Tumour Society Score and the Toronto Extremity Salvage Score.
Results: The post-rehabilitation Barthel Index was significantly lower in
elderly patients aged more than 60 years and in those with malignant tumours and tumours
larger than 10 cm. Malignancy and large tumour size were risk factors for a low Barthel
Index. There was significant correlation between the Musculoskeletal Tumour Society
Score/Toronto Extremity Salvage Score at final functional evaluation and the Barthel Index
at the end of rehabilitation. Conclusion: The Barthel Index is a simple
method to assess the activities of daily living and can potentially predict
disease-specific health-related quality of life at final functional evaluation after
musculoskeletal tumour surgery.
INTRODUCTION
“Musculoskeletal tumour” is a general term for bone tumours and soft tissue tumours. Such
tumours can occur in various locations in the body, with sites of origin including bony
tissues, fibrous connective tissues such as subcutaneous tissues and muscles, fibrous
tissues such as tendons and ligaments, adipose tissues, striated muscle tissues, smooth
muscle tissues, vascular and lymphatic tissues, tissues originating from the mesoderm such
as synovial membranes, and tissues originating from the ectoderm such as peripheral nerve
tissues. Among musculoskeletal tumours, the frequencies of benign tumours and malignant
tumours are reported to be approximately 1:100.1) Both conservative treatment and various surgical treatments
are performed, depending on the type of tissue, the tumour location, the diagnosis, the
level of malignancy, and subjective symptoms involving the tumour.1,2,3)
Although rehabilitation is implemented to ameliorate functional impairment after treatment,
the efficacy of rehabilitation has been described mostly for malignant tumours.4,5,6) As part of the rehabilitation procedures, evaluation of the
following items are recommended: functional impairment; deterioration in the performance of
activities of daily living (ADL); and social disadvantages evaluated using scales such as
the Performance Status, the Barthel Index, and the Functional Independence
Measure.7,8) Developed in 1965, the Barthel Index
has a track record of being used in numerous studies and is still widely used today as a
simple method to assess ADL for various diseases.9) However, in musculoskeletal tumours, disease-specific
methods for functional evaluation are widely used. These methods include the International
Symposium on Limb Salvage/Musculoskeletal Tumour Society Score and the Toronto Extremity
Salvage Score; few reports have described the use of the Barthel Index for the assessment of
ADL in patients with musculoskeletal tumours. Therefore, in this study, we used the Barthel
Index to evaluate the postoperative ADL in patients treated for musculoskeletal tumours. We
also examined the factors affecting the Barthel Index in these patients. Subsequently, we
examined the relationship between the Barthel Index at the end of rehabilitation and the
Musculoskeletal Tumour Society Score/Toronto Extremity Salvage Score at final functional
evaluation.
METHODS
This study was approved by the Institutional Review Board of our hospital, and all patients
provided informed consent prior to their study enrolment. From 2013 to 2016, 464 patients
with musculoskeletal tumours underwent orthopaedic surgery (amputation, wide resection,
marginal resection, curettage, or corrective osteotomy) at our hospital. If the ADL
performance was adversely affected after surgery, a therapist intervened with rehabilitation
and made assessments using the Barthel Index. The patient was discharged from the hospital
when able to perform daily life activities such as walking without assistance, climbing
stairs, and bathing. Rehabilitation was considered complete at the time of hospital
discharge, and the Barthel Index was subsequently evaluated by a physical therapist. If a
patient exhibited no impairments in their postoperative ADL, rehabilitation procedures were
not carried out. Patients who underwent rehabilitation and had malignant tumours that
originated in the extremities were evaluated using the Musculoskeletal Tumour Society Score
and the Toronto Extremity Salvage Score. When the functional improvement plateaued during
follow-up observation, the final functional evaluation was conducted using the
Musculoskeletal Tumour Society Score and the Toronto Extremity Salvage Score. Of the 464
patients with musculoskeletal tumours who underwent orthopaedic surgery, we excluded the 274
patients who did not undergo postoperative rehabilitation; this left a study population of
190 patients with musculoskeletal tumours who underwent rehabilitation. Based on information
from medical records, we analysed the following factors: age at surgery, sex, histologic
diagnosis and grade of the tumour, tumour location, tumour size, rehabilitation period, the
Barthel Index at the end of rehabilitation, and the Musculoskeletal Tumour Society Score and
the Toronto Extremity Salvage Score at final functional evaluation. In accordance with the
United Nations report on population dynamics10) and previous studies on musculoskeletal tumors,11) patients were divided into two
groups based on age: below age 60 years and age 60 years and above. Patients with mild to
moderate disabilities reportedly can achieve a Barthel Index score of 100; this implies that
the Barthel Index exhibits a ceiling effect.12,13) Because we also anticipated that many patients in our study
would exhibit a Barthel Index of 100, we conducted our analysis by separating the patients
into two groups: those with a Barthel Index of 100 points and those with a Barthel Index
<100 points. All histopathological specimens were classified by two or more pathologists
from the Department of Laboratory Medicine. The tumour stage was calculated using the
American Joint Committee on Cancer and International Union Against Cancer systems, 6th
edition.14) The follow-up
period was defined as the time from surgery to the last follow-up.
Univariate analyses were performed, comparing patient-, tumour-, and treatment-related
factors according to the two age categories using the Mann–Whitney U test for continuous
variables and the chi-squared test for categorical variables. Factors that were found to be
associated with a low Barthel Index were analysed using multivariate logistic regression
analysis. Spearman correlation analyses were performed to evaluate associations between the
Barthel Index and the Musculoskeletal Tumour Society Score and between the Barthel Index and
the Toronto Extremity Salvage Score. Statistical analyses were performed using statistical
analysis software (IBM Corp.; IBM SPSS Statistics for Windows, Version 25.0.). In all
analyses, P <0.05 indicated statistical significance.
RESULTS
The median age at surgery was 56 years (range, 6–91). One hundred and two patients were
under 60 years old, and 88 patients were over 60 years old. There were 97 male and 93 female
patients. One hundred and eighteen cases of soft tissue tumour and 72 cases of bone tumour
were included in the study. The locations of the tumours were 23 in the upper extremities,
137 in the lower extremities, and 30 in the trunk. In 131 patients, the tumour was smaller
than 10 cm and in 59 patients the tumour was larger than 10 cm. Benign tumours (including
the intermediary group) were present in 88 patients, and malignant tumours were present in
102 patients. In order of frequency, the benign tumours included 12 atypical lipomatous
tumours, 10 osteochondromas, and 10 lipomas. Likewise, malignant tumours included 16
undifferentiated pleomorphic sarcomas, 16 liposarcomas, and 15 myxofibrosarcomas. In total,
47 of 102 patients with malignant tumours were less than 60 years old, whereas 55 such
patients were more than 60 years old. Sixty-four malignant tumours were smaller than 10 cm
and 38 were larger than 10 cm. Further details on patient characteristics in relation to
Barthel Index are given in Table 1.
Table 1.
Patient characteristics and the post-rehabilitation Barthel Index
|
Total
(n) |
Median
rehabilitation period
(days) |
P value |
Median Barthel Index |
Mean Barthel Index
±standard error |
P value |
| All patients |
190 |
16 (3−389) |
|
100 (5−100) |
93.84 ± 0.896 |
|
| Age (years) |
|
|
<0.001*** |
|
|
0.004** |
| <60 years old |
102 |
13 (3–129) |
|
100 (30–100) |
95.29 ± 1.099 |
|
| ≥60 years old |
88 |
23 (4–389) |
|
95 (5–100) |
92.12 ± 1.443 |
|
| Sex |
|
|
0.074 |
|
|
0.683 |
| Male |
97 |
19 (3–389) |
|
100 (60–100) |
94.85 ± 0.872 |
|
| Female |
93 |
14 (3–120) |
|
100 (5–100) |
92.80 ± 1.588 |
|
| Tissue |
|
|
0.014* |
|
|
0.476 |
| Soft tissue |
118 |
18.5 (3–389) |
|
100 (5–100) |
94.75 ± 1.039 |
|
| Bone |
72 |
13 (3–129) |
|
100 (30–100) |
92.36 ± 1.637 |
|
| Tumour site |
|
|
0.093 |
|
|
0.353 |
| Upper extremity |
23 |
24 (4–40) |
|
95 (65–100) |
94.57 ± 1.631 |
|
| Lower extremity |
137 |
14 (3–389) |
|
100 (5 − 100) |
93.80 ± 1.092 |
|
| Trunk |
30 |
22.5 (7–129) |
|
95 (30–100) |
93.50 ± 2.458 |
|
| Tumour size |
|
|
<0.001*** |
|
|
0.005** |
| <10 cm |
131 |
13 (3–135) |
|
100 (30–100) |
95.27 ± 0.864 |
|
| ≥10 cm |
59 |
22 (7–389) |
|
95 (5–100) |
90.68 ± 2.113 |
|
| Diagnosis |
|
|
<0.001*** |
|
|
<0.001*** |
| Benign & intermediate |
88 |
10.5 (3–41) |
|
100 (60–100) |
98.01 ± 0.629 |
|
| Atypical lipomatous tumour |
12 |
15.5 (7–36) |
|
100 (70–100) |
97.08 ± 2.497 |
|
| Osteochondroma |
10 |
5 (3–18) |
|
100 (90–100) |
98.00 ± 1.106 |
|
| Lipoma |
7 |
10 (6–27) |
|
100 (95–100) |
98.57 ± 0.922 |
|
| Malignant |
102 |
25 (3–389) |
|
95 (5–100) |
90.25 ± 1.493 |
|
Undifferentiated
pleomorphic sarcoma |
16 |
26.5 (3–135) |
|
95 (55–100) |
91.88 ± 2.846 |
|
| Liposarcoma |
16 |
26 (5–70) |
|
95 (65–100) |
90.63 ± 2.695 |
|
| Myxofibrosarcoma |
15 |
30 (7–389) |
|
95 (70–100) |
91.67 ± 2.789 |
|
The median duration of postoperative rehabilitation was 16 days (range, 3–389). The
duration was significantly longer in patients aged 60 years or more (P <0.001). There was
no significant difference in rehabilitation duration in terms of gender (P=0.074). For
patients with tumours that originated in the soft tissues, the rehabilitation duration was
significantly longer (P=0.014). There was no significant difference between sites of
occurrence (P=0.093). Patients with a tumour size greater than 10 cm exhibited a
significantly longer rehabilitation period (P <0.001). Moreover, malignant tumours
resulted in a significantly longer duration (P <0.001). The duration of rehabilitation
and the Barthel Index at the end of rehabilitation were significantly negatively correlated
(Fig. 1a). In patients with a Barthel Index
below 95 points, the rehabilitation period was significantly longer (Fig. 1b).
There were 83 patients with a post-rehabilitation Barthel Index of 95 or less and 107
patients with a Barthel Index of 100. The median score was 100 (range, 5–100) and the mean
score was 93.84 ± 0.896. The Barthel Index was significantly lower in patients over 60 years
of age compared to those under 60 years of age (P <0.001), with a larger proportion of
patients with a Barthel Index below 95 points (under 60 years old, 35 cases; over 60 years
old, 48 cases; P=0.004). There was no significant difference in the Barthel Index between
male and female patients (P=0.683), or for the type of tissue (P=0.476), or site of
occurrence (P=0.353). In patients with tumours larger than 10 cm, the post-rehabilitation
Barthel Index was significantly lower than for those with a tumour smaller than 10 cm
(P=0.005). A larger proportion of patients with tumours larger than 10 cm had a Barthel
Index below 95 points (smaller than 10 cm, 48 cases; larger than 10 cm, 35 cases; P=0.003).
In patients with tumours larger than 10 cm, the post-rehabilitation Barthel Index was
significantly lower than for those with a tumour smaller than 10 cm (P=0.005).Compared to
patients with benign tumours, a larger proportion of patients with malignant tumours had a
Barthel Index below 95 points (benign, 17; malignant, 66; P <0.001). Patients with
malignant tumours also had a significantly lower Barthel Index (P <0.001). Multivariate
analysis revealed that malignancy and tumour size were risk factors for a lower
post-rehabilitation Barthel Index, as described in Table 2. In order of frequency, the Barthel Index items for which points were
deducted included STAIRS (58 cases), BATHING (54 cases), and MOBILITY (24 cases).
Table 2.
Risk factors for a low post-rehabilitation Barthel Index
| Factors |
Hazard ratio |
95% Confidence interval |
P value |
| Age ≥60 years |
0.536 |
0.277 − 1.037 |
0.064 |
| Malignancy |
0.143 |
0.072 − 0.283 |
<0.001*** |
| Tumour size ≥10 cm |
0.472 |
0.234 − 0.949 |
0.035* |
Of the patients with malignant tumours present in the extremities, 58 were evaluated using
the Musculoskeletal Tumour Society Score and 28 were evaluated using the Toronto Extremity
Salvage Score. The median follow-up period was 24.4 months (range, 4.7–60.1). The Barthel
Index at the end of rehabilitation correlated significantly with the Musculoskeletal Tumour
Society Score at final evaluation (Fig. 1c), and
patients with a Barthel Index below 95 had a significantly lower Musculoskeletal Tumour
Society Score (Fig. 1d). The Barthel Index at the
end of rehabilitation also significantly correlated with the Toronto Extremity Salvage Score
at final evaluation (Fig. 1e), and the Toronto
Extremity Salvage Score was significantly lower in patients with a Barthel Index below 95
points (Fig. 1f).
DISCUSSION
In this study, by using the Barthel Index, we evaluated the postoperative ADL of patients
who had undergone surgery for musculoskeletal tumours. We also investigated factors
affecting the post-rehabilitation Barthel Index score. The Barthel Index is applied to
evaluate 10 items of ADL in two to four stages; its efficacy is widely accepted.15,16,17) The Barthel Index is used to assess functional impairment
resulting from stroke, neurological disorders, and many other diseases.18,19) Rehabilitation for cancer patients is known to
improve the Barthel Index and Performance Status, and the efficacy of the Barthel Index for
estimating the survival rate of cancer patients has been reported in the
literature.6,20,21) However, there are few reports that have evaluated
postoperative impairment resulting from musculoskeletal tumours using the Barthel Index. In
the current study, we found that the impairment of ADL after musculoskeletal tumour surgery
is related to the need for long-term rehabilitation, which implies an extension of the
hospitalization period. Moreover, patients aged 60 years or older, patients with tumours
larger than 10 cm, and patients with malignant tumours required a longer rehabilitation
period; these results were consistent with past reports on cancers other than
musculoskeletal tumours.21,22)
Although soft tissue tumours required a longer rehabilitation period than bone tumours,
there was no reduction in the Barthel Index at the end of rehabilitation. One reason for
this result may be complications, such as the necessity for functional reconstruction during
surgery, failure of sutures, or infection. Risk factors for a low post-rehabilitation
Barthel Index were malignant tumours and tumours larger than 10 cm; these findings were also
consistent with past reports on other types of cancers.21,22)
In the current study, we also examined the relationship between the post-rehabilitation
Barthel Index and the Musculoskeletal Tumour Society Score/Toronto Extremity Salvage Score
at the final functional evaluation. The Musculoskeletal Tumour Society Score and the Toronto
Extremity Salvage Score were developed as disease-specific postoperative functional
evaluation scales for musculoskeletal tumours.23,24) The Musculoskeletal Tumour Society Score is an easily
applied, highly reproducible, and versatile scale that is aimed at evaluating functional
impairment and decreased functional ability after treatment of musculoskeletal tumours.
Although it was originally developed for the functional evaluation of patients undergoing
limb-sparing surgery, the scale can also be used for the functional evaluation of patients
after amputation. The scoring system of the Musculoskeletal Tumour Society Score is the most
standard method of evaluation in assessing the function of the affected limb. It has also
been reported that a moderate correlation was found between physical role functioning,
social role functioning, and physical functioning in SF-36, a comprehensive health-related
quality of life health survey. Although the Toronto Extremity Salvage Score is a
patient-reported measure to assess physical function of patients after limb-salvage surgery
for musculoskeletal tumours, the measure can also be used for evaluating physical function
after amputation. It is the sole patient-reported measure that can be used for
musculoskeletal tumours. The only methods generally used for evaluating health-related
quality of life that are specific to musculoskeletal tumours are the Musculoskeletal Tumour
Society Score and the Toronto Extremity Salvage Score, and the combined use of the two
scoring systems is recommended to evaluate disease-specific health-related quality of life,
including the physical functioning of the patient. Although their efficacy has been
reported,25,26,27,28,29) these methods of evaluation are limited to musculoskeletal
tumours of the extremities, underscoring a flaw in that they can neither be adapted for
tumours of the head, neck, and trunk, nor used for comparison with other diseases. In
addition to the Musculoskeletal Tumour Society Score and the Toronto Extremity Salvage
Score, several new evaluation scales have been developed in recent years, and some have also
been used for musculoskeletal tumours.30,31,32,33,34) However, these methods of evaluation are disease-specific,
and a generalized evaluation method remains to be developed for future evaluations. Davis et
al. reported that the Musculoskeletal Tumour Society Score and the Toronto Extremity Salvage
Score demonstrate a significant correlation.24) However, there are few reports that evaluate the relationship
between the Barthel Index and the Musculoskeletal Tumour Society Score/Toronto Extremity
Salvage Score. We found that the Barthel Index, which is a widely used and simple method for
assessing ADL, shows a significant correlation with the Musculoskeletal Tumour Society
Score/Toronto Extremity Salvage Score at final functional evaluation and can potentially be
used to predict health-related quality of life following the treatment of musculoskeletal
tumours.
There are several limitations to this study. First, there is the potential for bias because
some patients, often those with small benign tumours, suffered no postoperative impairment.
For these patients, we neither intervened with postoperative rehabilitation nor evaluated
ADL using the Barthel Index (although a Barthel Index score of 100 could be assumed).
Second, multiple evaluators, including surgeons and therapists, assessed the Barthel Index
and the Musculoskeletal Tumour Society Score/Toronto Extremity Salvage Score, and we did not
evaluate their reproducibility. Third, because this was a retrospective study, there were
variations in the time at which the Musculoskeletal Tumour Society score and the Toronto
Extremity Salvage Score were evaluated at the final follow-up observation. Furthermore,
because this was a one-time-point assessment, we were unable to evaluate changes over time.
Finally, this research was conducted at a single institution only.
The postoperative and post-rehabilitation ADL for patients with musculoskeletal tumours
were evaluated using the Barthel Index. Multivariate analysis revealed that a tumour larger
than 10 cm and malignant tumours were risk factors for a low Barthel Index at the end of
rehabilitation. The Barthel Index at the end of rehabilitation and the Musculoskeletal
Tumour Society Score/Toronto Extremity Salvage Score at final functional evaluation were
significantly correlated. We believe that the Barthel Index at the end of rehabilitation
could potentially predict the disease-specific health-related quality of life at the final
functional evaluation. Patients with musculoskeletal tumours comprise a highly heterogeneous
population, and we believe that higher sensitivity and better outcomes may be achieved in
evaluating the validity and effectiveness of treatments through the combined use of the
Musculoskeletal Tumour Society Score/Toronto Extremity Salvage Score with a much simpler ADL
assessment, such as the Barthel Index.
CONFLICTS OF INTEREST
The authors report no conflicts of interest.
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