X Clinically Important Reductions in Physical.32

Clin Orthop Relat Res (2021) 479:2306-2319
DOI 10.1097/CORR.0000000000001797
Clinical Research
Clinically Important Reductions in Physical Function and Quality

of Life in Adults with Tumor Prostheses in the Hip and Knee: A
Cross-sectional Study
Linda Fernandes MSc, PhD1, Christina Enciso Holm MD, PhD2, Allan Villadsen MD, PhD2,
Michala Skovlund Sørensen MD, PhD2, Mette Kreutzfeldt Zebis MSc, PhD1,
Michael Mørk Petersen MD, DMSc2,3
Received: 4 November 2020 / Accepted: 9 April 2021 / Published online: 10 May 2021
Copyright © 2021 by the Association of Bone and Joint Surgeons
Abstract
Background Patients with a bone sarcoma who undergo evaluate and improve upon postoperative interventions,
limb-sparing surgery and reconstruction with a tumor data from objectively measured physical function have
prosthesis in the lower extremity have been shown to have been suggested.
reduced self-reported physical function and quality of life Questions/purposes We sought to explore different aspects
(QoL). To provide patients facing these operations with of physical function, using the International Classification of
better expectations of future physical function and to better Functioning, Disability, and Health (ICF) as a framework, by
asking: (1) What are the differences between patients 2 to 12
years after a bone resection and reconstruction surgery of the
hip and knee following resection of a bone sarcoma or giant
The institution of one or more of the authors (LF) has received, cell tumor of bone and age-matched controls without walking
during the study period, funding from Vissing Fonden, Aalborg,
limitations in ICF body functions (ROM, muscle strength,
Denmark (grant number 85969).
The institution of one or more of the authors (MMP) has received, pain), ICF activity and participation (walking, getting up
outside the study period, funding from Zimmer Biomet, Biomet, from a chair, daily tasks), and QoL? (2) Within the patient
Ethicon UK, and Lima. group, do ICF body functions and ICF activity and partici-
All ICMJE Conflict of Interest Forms for authors and Clinical pation outcome scores correlate with QoL?
Orthopaedics and Related Research® editors and board members
Methods Between 2006 and 2016, we treated 72 patients
are on file with the publication and can be viewed on request.
Ethical approval for this study was obtained from the Danish Data for bone sarcoma or giant cell tumor of bone resulting in
Protection Agency (VD-2018-20, 6594) and the Capital Regional bone resection and reconstruction with a tumor prosthesis
Committee on Health Research Ethics (H-18032141). of the hip or knee. At the timepoint for inclusion, 47 pa-
The work was performed at the Musculoskeletal Tumor Section, tients were alive. Of those, 6% (3 of 47) had undergone
University Hospital Rigshospitalet, Copenhagen, Denmark.
amputation in the lower limb and were excluded. A further
32% (14 of 44) were excluded because of being younger
1
Department of Midwifery, Physiotherapy, Occupational Therapy, than 18 years of age, pregnant, having long transportation,
and Psychomotor Therapy, University College Copenhagen, palliative care, or declining participation, leaving 68% (30
Copenhagen, Denmark
of 44) for analysis. Thus, 30 patients and 30 controls with a
2
Musculoskeletal Tumor Section, Department of Orthopedic Surgery, mean age of 51 6 18 years and 52 6 17 years, respectively,
University Hospital Rigshospitalet, Copenhagen, Denmark were included in this cross-sectional study. Included pa-
3
tients had been treated with either a proximal femoral (40%
Institute of Clinical Medicine, Faculty of Health and Medical [12 of 30]), distal femoral (47% [14 of 30]), or proximal
Sciences, University of Copenhagen, Denmark
tibia (13% [4 of 30]) reconstruction. The patients were
L. Fernandes ✉, University College Copenhagen, Sigurdsgade 26, assessed 2 to 12 years (mean 7 6 3 years) after the
2200 Copenhagen Denmark, Email: life@kp.dk resection-reconstruction. The controls were matched on
Copyright © 2021 by the Association of Bone and Joint Surgeons. Unauthorized reproduction of this article is prohibited.
Volume 479, Number 10 Physical Function after Tumor Prosthesis 2307
gender and age (6 4 years) and included if they considered Conclusion This patient group demonstrated clinically
their walking capacity to be normal and had no pain in the important muscle weaknesses not only in resected muscles
lower extremity. Included outcome measures were: passive but also in the contralateral limb. Many patients reported
ROM of hip flexion, extension, and abduction and knee pain, and they showed reductions in walking and chair-
flexion and extension; isometric muscle strength of knee stand capacity comparable to elderly people. The results
flexion, knee extension and hip abduction using a hand- are relevant for information before surgery, and assess-
held dynamometer; pain intensity (numeric rating scale; ments of objective physical function are advisable in
NRS) and distribution (pain drawing); the 6-minute walk postoperative monitoring. Prospective studies evaluating
test (6MWT); the 30-second chair-stand test (CST); the the course of physical function and which include assess-
Toronto Extremity Salvage Score (TESS), and the ments of objectively measured physical function are war-
European Organisation for Research and Treatment of ranted. Studies following this patient group with repetitive
Cancer Quality of Life Questionnaire (EORTC QLQ-C30). measures over about 5 years could provide information
The TESS and the EORTC QLQ-C30 were normalized to about the course of physical function, enable comparisons
0 to 100 points. Higher scoring represents better status for with population norms, and lead to better-designed, tar-
TESS and EORTC global health and physical functioning geted, and timely postoperative interventions.
scales. Minimum clinically important difference for muscle Level of Evidence Level III, therapeutic study.
strength is 20% to 25%, NRS 2 points, 6MWT 14 to 31
meters, CST 2 repetitions, TESS 12 to 15 points, and
EORTC QLQ-C30 5 to 20 points. Introduction
Results Compared with controls, the patients had less knee
extension and hip abduction strength in both the surgical and Standard treatment after diagnosis of a primary bone sar-
nonsurgical limbs and regardless of reconstruction site. coma is usually limb-sparing surgery often combined with
Mean knee extension strength in patients versus controls neoadjuvant and adjuvant chemotherapy [21]. The opera-
were: surgical limb 0.9 6 0.5 Nm/kg versus 2.1 6 0.6 tive procedure is extensive, with resection of the affected
Nm/kg (mean difference -1.3 Nm/kg [95% CI -1.5 to -1.0]; bone, muscle, and adjacent joint followed by re-
p < 0.001) and nonsurgical limb 1.7 6 0.6 Nm/kg versus 2.2 construction with either tumor prostheses, allografts, au-
6 0.6 Nm/kg (mean difference -0.5 Nm/kg [95% CI -0.8 to tografts, or a bone graft prosthetic composite. The muscles
-0.2]; p = 0.003). Mean hip abduction strength in patients may be partly attached to one another and partly to the
versus controls were: surgical limb 1.1 6 0.4 Nm/kg versus prosthesis but only seldom can those muscles integrate
1.9 6 0.5 Nm/kg (mean difference -0.7 Nm/kg [95% CI -1.0 with it. With the loss of natural bone insertion of sur-
to -0.5]; p < 0.001) and nonsurgical limb 1.5 6 0.4 Nm/kg rounding muscles, the biomechanics of the joint and
versus 1.9 6 0.5 Nm/kg (-0.4 Nm/kg [95% CI -0.6 to -0.2]; muscles change substantially. Because the patient group is
p = 0.001). Mean hip flexion ROM in patients with proximal often fairly young at diagnosis, and given that both 5- and
femoral reconstructions was 113° 6 18° compared with 10-year survival rates have been reported to be around 54%
controls 130° 6 11° (mean difference -17°; p = 0.006). to 62% [2, 53, 60], the patients may live many years with
Mean knee flexion ROM in patients with distal femoral re- the tumor prosthesis. Considering the extensive surgical
constructions was 113° 6 29° compared with patients in the procedure, one may assume that there is a high risk of
control group 146° 6 9° (mean difference -34°; p = 0.002). reduced physical function over time.
Eighty-seven percent (26 of 30) of the patients reported pain,
predominantly in the knee, anterior thigh, and gluteal area.
The patients showed poorer walking and chair-stand ca- Physical Function
pacity and had lower TESS scores than patients in the
control group. Mean 6MWT was 499 6 100 meters versus Prior studies describing physical function in this patient
607 6 68 meters (mean difference -108 meters; p < 0.001), group, however, are often limited to the disease-specific
mean CST was 12 6 5 repetitions versus 18 6 5 repetitions Toronto Extremity Salvage Score (TESS) and the
(mean difference -7 repetitions; p < 0.001), and median Musculoskeletal Tumor Society Score (MSTS). When
(interquartile range) TESS score was 78 (21) points versus compared with the International Classification of
100 (10) points (p < 0.001) in patients and controls, re- Functioning, Disability, and Health (ICF), the TESS and
spectively. Higher pain scores correlated to lower physical MSTS measure some aspects of physical function, but they
functioning of the EORTC QLQ-C30 (Rho -0.40 to -0.54; do not provide a complete clinical picture [19, 46, 61]. It
all p values < 0.05). Less muscle strength in knee extension, has been suggested that objective measures of physical
knee flexion, and hip abduction correlated to lower physical function such as gait, balance, physical activity, ROM, and
functioning of the EORTC QLQ-C30 (Rho 0.40 to 0.51; all muscle strength should serve as important supplements
p values < 0.05). [19, 39, 40]. Patients going through limb-sparing surgery
2308 Fernandes et al. Clinical Orthopaedics and Related Research®
with faster stair climbing, walking speed, and a higher QoL

score in 10- to 26-year-old patients [40]. This would in-
dicate that ROM could be an important element to include
in exercise interventions. Likewise, other components of
physical function (such as pain, muscle strength, walking
capacity, and daily tasks) could be correlated with QoL and
thereby inform us about potentially important elements for
the exercise intervention. In summary, the knowledge
about different impairments and their severity, as well as
the relationship to QoL, is limited in this patient group.
Research Questions
In this study we sought to explore different aspects of

physical function, using the ICF as a framework, by asking:
Fig. 1. Flowchart of enrollment of patients. (1) What are the differences between patients 2 to 12 years
after a bone resection and reconstruction surgery of the hip
are obliged to know what short- and long-term post- and knee following resection of a bone sarcoma or giant
operative physical status they can expect. Combining re- cell tumor of bone and age-matched controls without
sults from self-reported and objectively measured physical walking limitation in ICF body functions (ROM, muscle
function might provide a more complete and tangible im- strength, pain), ICF activity and participation (walking,
age of expectations. Moreover, objectively measured getting up from a chair, daily tasks), and QoL? (2) Within
physical function is often of generic nature, enabling the patient group, do ICF body functions and ICF activity
comparisons between different treatment modalities, and participation outcome scores correlate with QoL?
techniques, and samples, which is important in research
and clinical settings. Muscle strength is one example of a
generic physical function measure often used in musculo- Patients and Methods
skeletal research. Five studies assessed muscle strength in
patients who underwent limb-sparing surgery due to bone Study Design, Setting
sarcoma [4, 7, 8, 12, 16]. One of these studies was a case
report of four patients [4], two of whom used manual The patients were compared with matched controls in a
muscle testing (that is, they did not objectively measure cross-sectional study. Recruitment and assessments took
muscle strength) [7, 16], compromising the quality of re- place between September 2018 and October 2019 in the
sults. Two studies used dynamometers to measure muscle Musculoskeletal Tumor Section of University Hospital
strength and showed less knee extension, knee flexion, and Rigshospitalet in Denmark. Patient recruitment was ad-
hip abduction peak torques compared with the nonsurgical ministered by a physical therapist (LF), an orthopedic
limb, but they did not include comparisons to a reference resident (CEH), and a consultant orthopaedic surgeon
group [9, 12]. Although ROM, pain, balance, and walking (AV). Recruitment of controls was administered by one
capacity are other important generic outcomes of physical author (LF) and four physical therapy students.
function, the prior reports are sparse and comparisons to
reference norms are almost nonexistent [19].
Participants
Physical Function in Relation to Quality of Life Patients were enrolled if they had been diagnosed with
bone sarcoma or giant cell tumor of bone resulting in bone
Quality of life (QoL) is an outcome that is important to resection and reconstruction with a tumor prosthesis of the
patients, and improved QoL often serves as a long-term hip or knee at the Musculoskeletal Tumor Section,
goal in medicine and rehabilitation [18, 31]. Both children University Hospital Rigshospitalet, between January 2006
and adults with bone sarcomas have reported inferior QoL and December 2016 (n = 72). At start of recruitment in
compared with population norms [15, 47, 54]. To better September 2018, 47 of the initial 72 patients were alive and
target exercise interventions to improve QoL, it is valuable thus eligible for physical evaluation (Fig. 1). Exclusion
to know what physical function components influence criteria were (1) age younger than 18 years, (2) amputation
QoL. One study found that greater knee ROM correlated in the lower limb, (3) less than 2 years since initial surgery,
Table 1. Participant demographics (Stryker), 27% (8 of 30) were the Segmental (Zimmer
Patients Controls Biomet), and 7% (2 of 30) were the Mega C (Link),
Characteristics (n = 30) (n = 30) p value depending in part on surgeon choice and the prostheses that
Men 53 (16) 53 (16) 0.99
were generally being used at the time of the
resection. Twenty percent (6 of 30) of patients underwent
Age in years 51 6 18 52 6 17 0.61
revision, and 3% (1 of 30) had two revisions. Forty percent
BMI in kg/m2 26 6 4 26 6 4 0.94
(12 of 30) had received chemotherapy (neoadjuvant and
Comorbidity, % yes (n) 43 (13) 33 (10) 0.43 adjuvant [n = 11] and only neoadjuvant [n = 1]), and 3% (1
Histology of 30) underwent postoperative radiation therapy. In gen-
Chondrosarcoma 47 (14) N/A eral, chemotherapy (neoadjuvant and adjuvant) was used
Osteosarcoma 30 (9) for the treatment of osteosarcoma and Ewing sarcoma and
Giant cell tumor 10 (3) postoperative external radiation therapy was used in the
Other 13 (4) treatment of Ewing sarcoma in case of poor chemotherapy
response and/or only marginal tumor removal. Three pa-
Data are presented as % (n) or mean 6 SD; N/A = not
tients used crutches daily and four used them from time to
applicable.
time.
(4) pregnancy, and (5) not understanding Danish. Three Description of Experiment, Procedure
patients were excluded based on hospital records of am-
putation. The remaining 44 patients were informed about All participants were assessed by a physical therapist who was
the study by phone or during outpatient visits at the hos- not involved in their initial surgical or postoperative care (LF),
pital. A total of 68% (30 patients) were included (Fig. 1). with assistance of students, at the Musculoskeletal Tumor
Excluded patients were younger than 18 years (n = 1), Section, University Hospital Rigshospitalet. The question-
pregnant (n = 1), did not understand Danish (n = 1), de- naires had been sent to the participants beforehand to be filled
clined participation for various reasons (n = 7), or did not out the same day as the appointment or one day ahead. The
return calls (n = 4) (Fig. 1). test session lasted one hour, and tests were carried out in the
Patients in the control group were recruited from post- following order: 6-minute walk test (6MWT), 30 second
ings at the hospital, university college, and social media. chair-stand test (CST), ROM, isometric muscle strength, and
We matched patients in the control group on age 6 4 years body weight. Body weight was recorded on a scale (MT32, no
and gender, as the two variables have a strong relationship 0299, BISCO Vægte A/S). One patient declined the test
to performance-based tests [24]. We applied a matching session at the hospital because of long distance but filled in
factor of 1:1. To reach 30 matched controls, a total of 53 and returned the questionnaires. No adverse effects were seen
patients in the control group were considered. Exclusion from the tests.
criteria were current and/or long-lasting pain in the lower
limb, known diseases that interfered with walking capacity
or stair walking, and the use of a walking aid. Although Variables, Outcome Measures, Data Sources, and Bias
not a reason for exclusion, none of the patients in the
control group had had a hip or knee replacement. It was not possible to blind the test personnel to the re-
construction site or whether the participant was a patient
or a control. To minimize observer bias, standardized test
Participant Demographics procedures were applied and information such as prosthe-
sis used, time from surgery, whether the patient had un-
Included patients had a mean age of 51 6 18 years and dergone any revision surgery, or postoperative care was
controls 52 6 17 years (Table 1). The patients were seen 2 kept from test personnel. We used the ICF as a framework
to 12 years (mean 7 6 3 years) after initial surgery. Tumor to list the outcome measures of physical function into the
subtypes were 47% (14 of 30) chondrosarcoma and 30% (9 two domains: (1) body function and (2) activity and par-
of 30) osteosarcoma (Table 1). Forty percent (12 of 30) ticipation. Developed by the World Health Organization,
underwent proximal femoral, 47% (14 of 30) distal femo- the ICF is used to standardize and code functioning and
ral, and 13% (4 of 30) proximal tibia resection and re- disability associated with health conditions [61]. The ICD-
construction surgery. Mean bone resection length for the 10 and the ICF are complementary; together, they provide
proximal femur was 15 6 3 cm, for the distal femur it was information on diagnosis plus functioning, giving a
15 6 4 cm, and for the proximal tibia it was 14 6 3 cm. Of broader and more meaningful picture of the health of
the tumor prostheses used, 67% (20 of 30) were the GMRS populations.
ICF Body Function counting the maximum amount of complete chair-stand

movements during 30 seconds. MCID for the 30-second
We measured ROM using a full-circle 1°-increment CST has been estimated to two repetitions [14].
plastic goniometer with a moveable arm. Hip extension, The TESS is a disease-specific self-administered
flexion, and abduction were assessed bilaterally in pa- questionnaire measuring physical function [13, 51]. It
tients with proximal femur reconstruction and their contains 30 questions answered on 0 to 5 Likert scale. A
matched individual in the control group. Knee extension standardized summary score is calculated ranging from
and flexion were assessed bilaterally in patients with 0 to 100, where higher scores indicate better physical
distal femur or proximal tibia reconstructions and their function [13]. In a Danish sample, the TESS showed
matched individual in the control group. All motion di- lower and upper limits of agreement of -12 and 15 points,
rections, except for hip extension, were measured with respectively [51].
the patient in a supine position, with the opposite thigh
fixed in neutral position [29, 30]. The nonsurgical limb
was assessed first. Compound Outcome Measure
We tested maximum voluntary isometric muscle strength
of (1) knee extension, (2) hip abduction, and (3) knee flexion The European Organisation for Research and Treatment of
bilaterally using a hand-held dynamometer (Hoggan Cancer Quality of Life Questionnaire (EORTC QLQ-C30)
microFET2, Hoggan Scientific LLC). The nonsurgical limb is a QoL questionnaire developed to cover content relevant
was tested first. The tests were performed using a stan- and important to cancer patients with items pertaining to
dardized protocol for test positions, fixation, and instructions both ICF body function and activity and participation [35,
during the test [41]. We recorded three maximal intensity 50]. It consists of 30 items answered by the patient on
trials. Data was normalized to body weight (Nm/kg), and Likert scales ranging from 1 to 4 or 1 to 7. Subscale scores
percent muscle deficits were expressed as relative to refer- for general health, functional scales, and symptom scales

were calculated using a scoring algorithm [1]. MCIDs for
ence 1 2 reference value p100 . Minimum clinical
target value
improvement and deterioration for the functional scales
important differences (MCIDs) for isometric knee extension have been estimated within the range of 5 to 20 points [48].
and hip abduction strength were estimated between 20% to For the correlational analyses, we selected the subscales for
25% [41, 42, 49]. general health and physical functioning. Our rationale for
We assessed pain intensity with the commonly used 11- this was that general health represented an overall score of
point numeric rating scale (NRS), where 0 equaled “no pain” QoL and physical functioning represented the same con-
and 10 equaled “worst pain imaginable” [26]. Three NRS struct as the included outcome measures of physical
ratings were applied: (1) current pain, (2) worst pain during function described above. Moderate-to-high correlations
the past week, and (3) mean pain during the past week. MCID were expected for physical functioning and low-to-
for the NRS pain scale has been reported at 2 points [23]. moderate for general health [38, 56].
A pain drawing was used to illustrate pain distribution.
The participants were asked to mark the area where they
felt pain on a paper silhouette illustration of the human Ethical Approval
body, including anterior and posterior views. A transparent
template with 42 body regions was placed on the pain Ethical approval for this study was obtained from the
drawing [34, 37]. Any mark within a body region was Danish Data Protection Agency (VD-2018-20, 6594) and
scored as “pain present.” the Capital Regional Committee on Health Research Ethics
(H-18032141).
ICF Activity and Participation

Statistical Analysis, Study Size
Walking capacity was assessed using the 6MWT [3]. The
participants were instructed to walk back and forth as Data were analyzed in SPSS version 25 (SPSS Inc).
quickly as possible for 6 minutes on a 20-meter walking Results were regarded as statistically significant at p <
track. The 6MWT has been widely used in numerous pa- 0.05. Normality of variables was tested by visual in-
tient groups [17]. MCIDs for the 6MWT have been spection (histograms, probability plots) and the Shapiro-
reported to be between 14 and 31 meters [10]. Wilk test. For normally distributed data, the paired t-test
The CST aims to record functional muscle strength and was used to evaluate differences between groups
power by evaluating the activity “sit-to-stand” in both along with presentation of mean differences (95% confi-
younger and older populations [22, 45, 57]. It is scored by dence interval). For nonnormally distributed data,
Table 2. Hip and knee passive ROM (in degrees) in the patient and control groups
Patient Control Patient Control
group group group group
ROM by Between-group Between-group
reconstruction Surgical Matched to mean difference p Nonsurgical Matched to mean difference p
site limb surgical limb (95% CI) value limb nonsurgical limb (95% CI) value
Proximal femur
Hip Flexion 113 6 18 130 6 11 -17 (-29 to -6) 0.006 131 6 9 1316 11 0 (-10 to 11) 0.98
Extension 865 15 6 8 -8 (-13 to -2) 0.01 967 14 6 7 -6 (-11 to 0) 0.047
Abduction 34 6 10 38 6 5 -4 (-11 to 3) 0.24 33 6 9 41 6 7 -8 (-15 to -1) 0.03
Distal femur
Knee Flexion 113 6 29 146 6 9 -34 (-53 to -14) 0.002 140 6 9 146 6 9 -6 (-14 to 2) 0.10
Extension 364 364 0 (-3 to 3) 0.86 463 363 0 (-2 to 3) 0.71
Proximal tibia
Knee Flexion 108 6 14 151 6 2 -43 (-66 to -20) 0.009 141 6 8 151 6 3 -10 (-22 to 2) 0.07
Extension 162 463 -3 (-7 to 0) 0.06 365 463 -2 (-6 to 3) 0.32
Data are presented as mean 6 SD and mean difference (95% CI); hip ROM in patients with proximal femoral reconstructions (n = 11/
group); knee ROM in patients with distal femoral (n = 14/group) and proximal tibia (n = 4/group) reconstructions.
between-group differences were analyzed using the controls (Table 2). Mean hip flexion ROM in patients with
Wilcoxon signed rank test. To compare muscle strength proximal femoral reconstructions was 113° 6 18° and in
data to a previously published study, we performed a controls was 130° 6 11° (mean difference -17° [95% CI
subgroup analysis based on reconstruction site [8], where -29° to -6°]; p = 0.006). Mean knee flexion ROM in pa-
paired t-tests were used despite violating the assumption tients with distal femoral reconstructions was 113° 6 29°
of normal distribution. We used the Spearman rank cor- and in controls was 146° 6 9° (mean difference -34° [95%
relation coefficient (Rho) to analyze correlations. CI -53° to -14°]; p = 0.002).
Because a substantial number of various parameters were Compared with controls, the patients had less knee
examined and tested statistically without any pre- extension and hip abduction strength in both the surgical
determined primary outcome measure (and with no sam- and nonsurgical limbs. Mean knee extension strength in
ple size calculations performed), the results of this study the patients’ surgical limb was 0.9 6 0.5 Nm/kg versus
cannot be considered confirmatory but are of an explor- those in the control group 2.1 6 0.6 Nm/kg (mean dif-
atory nature. This is also the reason why we did not per- ference -1.3 Nm/kg [95% CI -1.5 to -1.0]; p < 0.001) and
form any correction for the multiple testing. To justify in patients’ nonsurgical limb it was 1.7 6 0.6 Nm/kg
pooling of patients with different age and time since versus the control group 2.2 6 0.6 Nm/kg (mean dif-
surgery, correlations between TESS scores and age (r = ference -0.5 Nm/kg [95% CI -0.8 to -0.2]; p = 0.003)
-0.07; p = 0.70) and time since surgery (r = 0.25; p = 0.18) (Table 3). Mean hip abduction strength in the patients’
were performed. In addition, no differences in TESS surgical limb was 1.1 6 0.4 Nm/kg versus the control
scores depending on the three sites of surgery were found group 1.9 6 0.5 Nm/kg (mean difference -0.7 Nm/kg
using the Kruskal-Wallis test (p = 0.73). One patient de- [95% CI -1.0 to -0.5]; p < 0.001) and in patients’ non-
clined assessments at the hospital (ROM, muscle strength, surgical limb it was 1.5 6 0.4 Nm/kg versus the control
6MWT, CST) but filled in the self-reported outcomes. group 1.9 6 0.5 Nm/kg (-0.4 Nm/kg [95% CI -0.6 to
Missing observations from this patient were not replaced. -0.2]; p = 0.001). Using the limbs of the control group as
reference values, muscle strength deficits in the surgical
limbs ranged from 28% to 66% (Fig. 2A-C). Muscle
Results strength in patients’ nonsurgical limbs ranged from no
deficit to 27% deficit (Fig. 2A-C).
Differences Between Patients and Controls Pain intensity ratings differed between groups for “worst
pain” and “mean pain,” but not for “current pain” (Table 4).
ICF Body Function “Worst pain” showed a median (interquartile range) of 5 (5)
and 0 (2) points (p = 0.001), “mean pain” 3 (3) and 0 (1) points
The patients showed less hip and knee flexion ROM but (p = 0.002), and “current pain” 1 (3) and 0 (1) points (p = 0.07)
similar hip and knee extension ROM compared with in patients and controls, respectively (Table 4). Eighty-seven
Table 3. Isometric muscle strength (in Nm/kg) in patients (n = 29) and controls (n = 29)a
Patients Controls Patients Controls
Between- Between-
Matched to group mean Matched to group mean
Muscle Surgical surgical difference p % Nonsurgical nonsurgical difference p %
group limb limb (95% CI) value deficit limb limb (95% CI) value deficit
Knee 0.9 6 0.5 2.1 6 0.6 -1.3 (-1.5 to -1.0) < 0.001 57% 1.7 6 0.6 2.2 6 0.6 -0.5 (-0.8 to -0.2) 0.003 34%
extension
Knee 0.7 6 0.2 1.1 6 0.3 -0.5 (-0.6 to -0.4) < 0.001 42% 1.0 6 0.4 1.1 6 0.3 -0.12 (-0.3 to 0.1) 0.16 11%
flexion
Hip 1.1 6 0.4 1.9 6 0.5 -0.7 (-1.0 to -0.5) < 0.001 40% 1.5 6 0.4 1.9 6 0.5 -0.4 (-0.6 to -0.2) 0.001 20%
abduction
Data are presented as mean 6 SD and mean differences (95% CI); p value when obtained from paired samples t-test.
a
One of 30 patients did not attend muscle strength tests, leaving 29 pairs for this analysis.
percent (26 of 30) of patients marked pain in at least one of 42 functioning of the EOTRC QLQ-C30 correlated to less
body regions on the pain drawing. The patients reported a muscle strength in knee extension (Rho 0.40; p = 0.034), knee
median (IQR) of 2.5 (4) painful body regions on the pain flexion (Rho 0.40; p = 0.038), and hip abduction (Rho 0.51;
drawings (Table 4), with knee, thigh, and gluteal area as the p = 0.006) of the surgical limb and hip abduction (Rho 0.38;
most frequent painful body regions (Fig. 3). p = 0.046) of the nonsurgical limb (Table 7). Worse physical
functioning also correlated with higher pain scores (current
pain, Rho -0.54; p = 0.002; worst pain, Rho -0.51; p = 0.004;
ICF Activity and Participation mean pain, Rho -0.40; p = 0.03; and painful body regions,
Rho -0.53; p = 0.003) (Table 7). Better scorings of the sub-
Group differences were found for the 6MWT, 30-second scale physical functioning correlated with better scorings of
CST, and TESS (Table 5). Mean 6MWT was 499 6 100 the TESS (Rho 0.79; p < 0.001) (Table 7).
meters versus 607 6 68 meters (mean difference -108
meters; p < 0.001), mean CST was 12 6 5 repetitions
versus 18 6 5 repetitions (mean difference -7 repetitions; Discussion
p < 0.001), and median (IQR) TESS scores were 78 (21)
points versus 100 (10) points (p < 0.001) in patients and Limb-sparing bone tumor resection and reconstruction
controls, respectively (Table 5). with a tumor prosthesis is an extensive surgical procedure.
In the postoperative period, limitations in self-reported
physical function and inferior QoL have been reported
Quality of Life [54]. Objectively measured physical function has been
suggested to serve as an important supplement to provide a
There were differences between groups in the EORTC more complete image of physical status after surgery [19].
QLQ-C30 subscales global health (median [IQR] 79 [16] Moreover, evaluating the relationship between different
versus 92 [17]; p < 0.001), physical functioning (median aspects of physical function and QoL can help health
[IQR] 80 [30] versus 100 [0]; p < 0.001), role functioning professionals involved in rehabilitation to target in-
(median [IQR] 83 [50] versus 100 [0]; p < 0.001), fatigue tervention to improve QoL. In this study, we found that the
(median [IQR] 22 [33] versus 11 [14]; p = 0.01), and pain patients who had undergone limb-sparing surgery 2 to 12
(median [IQR] 25 [33] versus 0 [17]; p < 0.001) (Table 6). years earlier had bilateral muscle deficits in knee extension
and hip abduction and less walking and chair-stand ca-
pacity. The patients reported weekly pain most frequently
Correlation between ICF Body Function, Activity and located in thigh, knee, and gluteal area. To give tangible
Participation Outcomes, and QoL expectations about future physical status, information
about frequent pain, reduced muscle strength, and mobility
Overall, muscle strength, pain, and TESS correlated to QoL capacity should be provided to patients who face this sur-
scores (Table 7). Worse global health status correlated to less gery. In addition, this study showed that muscle strength
hip abduction muscle strength in both surgical (Rho 0.43; p = and pain were related to QoL, thus indicating that these two
0.02) and nonsurgical limbs (Rho 0.39; p = 0.04) and higher aspects of physical function are important for the percep-
current pain (Rho -0.60; p < 0.001) (Table 7). Worse physical tion of QoL and can be targeted in rehabilitation.
Fig. 2. A-C Subgroup analysis, based on reconstruction site (proximal femur, n

= 11; distal femur, n = 14; proximal tibia, n = 4), of isometric muscle strength
(Nm/kg) in (A) knee extension; (B) knee flexion; and (C) hip abduction. Muscle
deficits (that is, percent decrease in muscle strength) in nonsurgical and sur-
gical limb compared with controls (above bars) and in surgical limb compared
with nonsurgical limb (below bars). Error bars represent mean (95% CI).
a
Statistical significance (p < 0.05), bstatistical significance (p < 0.001), when
obtained from paired sample t-test.
Table 4. Between-group comparison of pain intensity and number of painful body regions (of maximum 42 body regions)
Pain Patients (n = 30) Controls (n = 30) p value
Intensity (NRS) Current pain 1 (3) 0 (1) 0.07
Worst pain during the past week 5 (5) 0 (2) 0.001
Mean pain during the past week 3 (3) 0 (1) 0.002
Distribution Number of painful body regions 2.5 (4) 0 (3) 0.01
Data are presented as median (interquartile range); NRS = numeric rating scale (0 = no pain to 10 = worst pain imaginable).
Limitations instructions, and encouragement, and conducted training

sessions before the study started. Because they showed
This study has several limitations. First, the sample size was clinically important reductions, we believe the risk of
small; however, because bone sarcoma is a rare disease, this overestimating patients’ results did not affect the in-
was expected [60]. Of the 44 eligible patients 32% (14 of 44) terpretation of between-group differences. Despite limita-
were not included. Reasons for not participating varied: Two tions in study design and a possible skewness toward
patients were in late-stage palliative care, and two patients overestimating outcome scores, we believe these results are
thought the transportation to the study location was too important. One reason is to give the most accurate in-
challenging. With the exclusion of these four patients, a formation possible to patients before their consent to limb-
possible selection bias toward better outcomes was in- sparing surgery. Each patient has different needs for in-
troduced. The seven patients who declined or did not return formation, and health professionals should be prepared to
calls we assumed were less motivated to attend. The results supplement standard information with personal advice to
would therefore be generalizable to survivors of bone sar- suit the individual’s situation [25]. Another reason is that the
coma after limb-sparing surgery with the motivation and use of objectively measured physical function of a generic
overall physical status to attend outpatient clinics and endure
physical testing. The attendance rate of 68% gives surgeons
an idea of the percentage of patients who regain mobility and
the motivation to participate in physical activity at a rea-
sonable level. Second, a heterogenous sample of patients
with different sites of surgery, resection length, histology,
(neo-) adjuvant treatment, assessment points between 2 and
12 years after surgery, and ages ranging from 19 to 83 years
was included. However, we decided to pool data from these
patients based on the pre-analyses, which showed no dif-
ferences in TESS scores between the three sites of surgery
and no correlations between the TESS scores and time from
surgery or age. The absence of correlation between the TESS
scores and time from surgery is further supported by a study
that followed children after limb-sparing surgery who
showed no improvements in TESS between 2 and 7 years
postoperatively [59]. Furthermore, a study assessing TESS
and QoL in adults at a mean 4 years after surgery found no
correlations between time since surgery and score ratings
[33]. We therefore considered pooled analyses for this
sample to be legitimate. Third, the study was cross-sectional
in design because we only assessed patients at one point.
Therefore, we cannot draw any conclusions about the tem- Fig. 3. Painful body regions marked by two or more of 30
patients after limb-sparing surgery with reconstruction of
poral relationship of time of surgery and onset of the im-
proximal femur (n = 12), distal femur (n = 14), and proximal
pairments and disabilities found in this study. Forth, tibia (n = 4). We modified a template from a previous paper
blinding test personnel to the operated surgical joint was not (Adapted with permission from Wolters Kluwer Health Inc:
possible. This may have encouraged patients to perform Lacey RJ, Lewis M, Jordan K, et al. Interrater reliability of scoring
better so as to demonstrate good surgical results. To mini- of pain drawings in a self-report health survey. Spine (Phila Pa
mize observation bias, we used standardized information, 1976). 2005;30:455-458.)
Table 5. Between-group comparison of the 6MWT, CST, and TESS

Patients Controls Between groups p value
6MWT, m 499 6 100 607 6 68 -108 (-146 to -70) < 0.001
CST, n 12 6 5 18 6 5 -7 (-9 to -4) < 0.001
TESS 78 (21) 100 (10) -14 (-26 to -5) < 0.001
Data are presented as mean 6 SD for 6MWT and CST, median (interquartile range) for TESS, and as between-group mean
differences (95% CI); 6MWT = 6-minute walk test; CST = 30-second chair-stand test; TESS = Toronto Extremity Salvage Score (range
0-100). CST measures complete chair-stand movements.
nature enables comparison to population norms and between rehabilitation. Our results showed that, in accordance
different treatment modalities. The assessments used in this with expectations, resected muscles were weaker, but in
study can be easily implemented in clinical practice. A third contrast to expectations, intact muscles were also weaker
reason is to contribute to research. Considering the chal- compared with controls. The deficits in hip abduction
lenges of conducting prospective studies in a rare disease and knee extension in both surgical and nonsurgical
with 5-year survival rates of about 60%, the cross-sectional limbs are clinically important [41, 42, 49], and they are
design has its place. However, to evaluate the course of larger than in patients with primary knee replacements
function over time, prospective studies are needed. [27, 43, 58]. We cannot draw any conclusion about the
temporal relationship of time of surgery and onset of
muscular weakness in the nonsurgical limb. The find-
Differences Between Patients and Controls ings, however, suggest that it would be advisable to as-
sess muscle strength bilaterally, comparing them with
ICF Body Function reference groups and where muscle deficits are found, to
consider strengthening exercises. Hip and knee flexion
The surgical limb showed muscle strength deficits in all ROM in this sample was less versus controls but com-
three muscles groups tested regardless of the target joint pared with the mechanical abilities of the tumor pros-
of surgery. Reduced muscle strength is expected in thesis, we would consider mean hip flexion of 113° 6
resected muscles at short- and long-term [8, 12], and 18° and mean knee flexion of 113° 6 29° acceptable. Our
normalized muscle strength is generally expected in in- results are similar to one study in children after limb-
tact muscles after completing postoperative sparing surgery in the hip and knee [40].
Table 6. Between-group comparison of the EORTC QLQ-C30 subscales

EORTC QLQ-C30 Patients (n = 30) Controls (n = 30) p value
Global health status 79 (16) 92 (17) < 0.001
Functional scales Physical functioning 80 (30) 100 (0) < 0.001
Role functioning 83 (50) 100 (0) < 0.001
Emotional functioning 92 (25) 96 (17) 0.37
Cognitive functioning 100 (17) 100 (17) 0.63
Social functioning 100 (33) 100 (0) 0.001
Symptom scales Fatigue 22 (33) 11 (14) 0.01
Nausea and vomiting 0 (0) 0 (0) 0.18
Pain 25 (33) 0 (17) < 0.001
Item scales Dyspnea 0 (33) 0 (0) 0.22
Insomnia 0 (33) 0 (33) 0.31
Appetite loss 0 (0) 0 (0) 1.0
Constipation 0 (0) 0 (0) 0.66
Diarrhea 0 (0) 0 (0) 0.06
Financial difficulties 0 (33) 0 (0) 0.003
Data are presented as median (interquartile range); the EORTC QLQ-C30 scales range from 0 to 100 points; higher scoring represents
better status for Global health status and Functional scales; higher scoring represents worse status for Symptom and Item scales;
EORTC QLQ-C30 = European Organisation for Research and Treatment of Cancer Quality of Life Questionnaire.
Table 7. Relationship between quality of life and variables of ICF body function and ICF activity and participation (n = 29)
EORTC QLQ-C30
Global health p value Physical functioning p value
ICF body function
ROM Hip flexion (n = 11)a 0.16 0.64 0.03 0.92
Hip extension (n = 11) -0.21 0.53 0.15 0.67
Hip abduction (n = 11) -0.29 0.40 0.46 0.16
Knee flexion (n = 18) -0.31 0.21 -0.28 0.28
Knee extension (n = 18) -0.18 0.48 -0.37 0.14
Muscle strength in surgical limb Knee extension 0.15 0.43 0.40 0.034
Knee flexion 0.16 0.42 0.40 0.038
Hip abduction 0.43 0.02 0.51 0.006
Muscle strength in nonsurgical limb Knee extension 0.31 0.10 0.31 0.11
Knee flexion 0.39 0.04 0.35 0.07
Hip abduction 0.39 0.04 0.38 0.046
Pain intensity (NRS) Current pain -0.60 < 0.001 -0.54 0.002
Worst pain -0.36 0.05 -0.51 0.004
Mean pain -0.31 0.09 -0.40 0.03
Pain distribution Painful body regions -0.38 0.04 -0.53 0.003
ICF activity and participation
6MWT 0.01 0.98 0.20 0.32
CST 0.19 0.32 0.29 0.14
TESS 0.38 0.046 0.79 < 0.001
Data are presented as correlation coefficients (Rho). The CST measures complete chair-stand movements; EORTC QLQ-C30 =
European Organisation for Research and Treatment of Cancer Quality of Life Questionnaire; NRS = numeric rating scale; 6MWT = 6-
minute walk test; CST = 30-second chair-stand test; TESS = Toronto Extremity Salvage Score.
ICF Activity and Participation item scores (dyspnea, insomnia, appetite loss, con-
stipation, diarrhea). This may be due to initial treatment
We found clinically important reductions in 6MWT, CST, and being completed before inclusion in this study and side-
TESS, and when comparing our patients (mean age 51 6 18 effects from treatment, such as chemotherapy, were no
years) to population-based norms, mean walking and chair- longer an issue. Comparing our results with population-
stand capacity were equal to levels of 80-year-old men and based references, patients’ scores for global health were
women [6, 10, 42, 44, 52, 55]. Further deterioration of walking at equal levels and physical functioning were at levels
and chair-standing capacity may have consequences on self- of 70- to 79-year-old patients, despite having a mean
sufficiency, and it has been found to be related to increased risk age of 51 6 18 years [32]. This demonstrates the im-
of falling, disabilities, and mortality in older people [11, 36]. It portance of clinicians paying attention to physical
is unrealistic to think that walking and chair-standing capacity function and the ability to participate in social settings 2
could be as good as age-related references after this extensive years or more postoperatively. Among patients who
surgery. The walking capacity of children and adolescents was express difficulties, supportive interventions might be
demonstrated to improve during the first 2 postoperative years of value.
and to level out between 2 and 7 years, but it was still inferior
to age-related peers [5, 59]. This may also be the case for
adults, but there are no prospective studies to confirm this. Correlation Between ICF Body Function, Activity and
Bear in mind that with a capacity of an 80-year-old, it might be Participation Outcomes, and QoL
advisable to promote exercise to minimize deterioration of
these activities over time. We found that poorer QoL correlated to muscle strength
deficits, pain, and lower TESS scores but not to ROM,
Quality of Life 6MWT, or CST. This indicates that, for the purpose of
improving QoL, elements of strengthening exercises and
The patients showed poorer QoL in functioning sub- pain management may be useful but need to be evaluated in
scales, fatigue, and pain but not in the cancer-specific prospective studies. A lack of correlation between QoL and
ROM, 6MWT, and CST was unexpected since previous 3. ATS Board of Directors. American Thoracic Society ATS
studies have found correlations in cancer and knee re- statement: guidelines for the six-minute walk test. Am J Resp Crit
Care Med. 2002;166:111-117.
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4. Beebe K, Song KJ, Ross E, et al. Functional outcomes after limb-
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of the same construct. For example, the reporting of being pandable prosthesis: a report of 4 cases. Arch Phys Med Rehabil.
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to a metric system. Lack of a demonstrated correlation with prospective study on quality of life and functional outcome in
children and adolescents after malignant bone tumor surgery.
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Our study showed that patients with bone sarcoma or allograft-prosthetic composite reconstruction and modular pros-
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muscles around the reconstructed joint but also in the
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Clin Orthop Relat Res (2021) 479:2306-2319

Clinically Important Reductions in Physical Function and Quality

with faster stair climbing, walking speed, and a higher QoL

In this study we sought to explore different aspects of

ICF Body Function counting the maximum amount of complete chair-stand

ICF Activity and Participation

Fig. 2. A-C Subgroup analysis, based on reconstruction site (proximal femur, n

Limitations instructions, and encouragement, and conducted training

Table 5. Between-group comparison of the 6MWT, CST, and TESS

Table 6. Between-group comparison of the EORTC QLQ-C30 subscales

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