Received: 27 June 2017
|
Revised: 9 August 2017
|
Accepted: 19 September 2017
DOI: 10.1002/jso.24880
RESEARCH ARTICLE
Factors associated with local recurrence after surgery for bone metastasis to the extremities Chandra Kumar Krishnan MS1,2 | Han-Soo Kim MD, PhD1 | Ji Yeon Yun BS1 | Hwan Seong Cho MD, PhD3 | Jong Woong Park MD1 | Ilkyu Han MD, PhD1 1 Department
of Orthopaedic Surgery, Seoul National University Hospital, Seoul, Korea
Background and Objectives: With increasing life expectancy of patients with bone
2 Department
metastasis, durable surgical stabilization of bone metastasis is necessary. Local
of Surgical Oncology, Cancer Institute (WIA), Adyar, Chennai, India
recurrence (LR) can compromise surgical stabilization and necessitate retreatment. We
3 Department
of Orthopedic Surgery, Seoul National University Bundang Hospital, Bundang-gu, Seongnam, Korea
analyzed LR rate and factors associated with LR in patients undergoing surgery for bone metastasis. Methods: Patients (n = 301) who underwent surgery for bone metastasis to the
Correspondence Ilkyu Han, MD, PhD, Department of Orthopaedic Surgery, Seoul National University Hospital, 101 Daehak-ro Jongnogu, Seoul 03080, Korea. Email:
[email protected]
extremities were reviewed. Possible factors that might be associated with LR were investigated. Results: LR rate was 16% (49/301). Surgical margin was associated with LR, as patients with en-bloc resection had significantly less LR than patients who underwent curettage (5/66 vs 44/235, P = 0.03). Prostate cancer had lowest rate (0%) of LR and colon cancer had highest rate (31%). Interval from surgery to LR differed among primary cancer types (4.5 ± 3.9 months [lung cancer], vs 12.3 ± 12.9 months [other cancers], P = 0.041). In multivariate analysis, en-bloc surgical margins (HR = 0.372, P = 0.036) and primary cancers of breast or prostate (HR = 0.391, P = 0.049) were independent factors associated with longer LR-free survival. Conclusions: LR after surgery for bone metastasis to extremities is affected by surgical margin and primary cancer type. These factors, along with expected patient survival, need to be considered when planning surgery for bone metastasis to extremities. KEYWORDS
bones of lower extremity, bone neoplasms, bones of upper extremity, neoplasm metastasis
1 | INTRODUCTION
of patients with bone metastases.3–5 Given the increasing life expectancy of patients with bone metastases, durable surgical
Although most patients with bone metastases to the extremities have a
stabilization of bone metastases, which provides lifelong pain relief
limited life expectancy of only a few months, a considerable proportion
and functional recovery, is necessary.6 Durability of surgical stabiliza-
1,2
of patients live longer, even a few years.
Moreover, ongoing
tion is determined not only by the adequacy of the surgical
improvements in systemic therapy are prolonging the life expectancy
construction, such as the choice of implant or the length of the fixation, but also by the effectiveness of local tumor control. Local
Investigation performed at Department of Orthopaedic Surgery, Seoul National University Hospital, 101 Daehak-ro Jongno-gu, Seoul 03080, Korea.
J Surg Oncol. 2017;1–8.
tumor recurrence can compromise surgical stabilization and necessitate re-treatment.7,8 Although there are many reports in the orthopedic
wileyonlinelibrary.com/journal/jso
© 2017 Wiley Periodicals, Inc.
|
1
2
KRISHNAN
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literature regarding adequate surgical construction, few studies have
TABLE 1
been published on local tumor control after surgical stabilization of bone
Variable
metastasis to the extremities.7–15
Previous radiotherapy
To provide durable surgical stabilization and select optimal surgical options with regard to resection and reconstruction, identification of the risks of local recurrence (LR) and its associated factors is needed. Therefore, this study sought to identify the LR rate and to analyze the clinicopathologic factors associated with LR in patients undergoing surgery for bone metastasis to the extremities.
ET AL.
Treatment of bone metastasis N
%
Not received
247
83
Received
49
17
En-bloc resection
66
22
Curettage
235
78
Intramedullary nail
154
52
Bipolar hip hemiarthroplasty
52
17
Megaprosthesis
51
17
Surgical Margin
Reconstruction used
2 | M ATERIA LS AN D METH ODS A retrospective review of a prospectively collected institutional database was performed and identified 437 patients who underwent surgery for bone metastasis to the extremities between January 2001 and December 2015. The institutional review board of the hospital approved this study. For the purpose of analysis, the following exclusion criteria were applied: 1) patients with hematolymphoid malignancy of the bone
Plate
24
8
Cement with screws and pins
16
5
No reconstruction
4
1
Not received
174
59
Received
121
41
Postoperative radiotherapy
(n = 64), 2) patients who had undergone operation on the small bones of the hands or feet (n = 11), 3) patients whose tumors were not surgically removed (n = 41), and 4) patients who underwent amputa-
applied to the main lesion. Stems of endoprostheses were fixed with
tion (n = 1). Of the remaining 320 patients, 19 patients with less than
methylmethacrylate cement. Forty-nine (17%) patients had undergone
1 month of follow up for LR were excluded, which left us with 301
previous radiation therapy for the main lesion. When postoperative
patients for analysis. For patients with multiple surgeries on the same
radiation therapy was administered, the entire bone was included in the
lesion, only the index surgery was counted (n = 28). Among the 301
field.
patients, 249 (83%) died during the follow-up period. The actuarial
In general, postoperative follow-up evaluations were performed at
survival rate calculated through Kaplan-Meier analysis at 6 months,
2 weeks and then at 3-6 month intervals. For LR surveillance, imaging
1 year, and 2 years was 62.1 ± 2.8%, 40.0 ± 2.9%, and 22.2 ± 2.6%,
such as plain radiographs, MRI scans, CT scans, PET scans, or bone
respectively. The mean follow-up period of the entire cohort was
scans were examined. The follow-up schedule and modality varied
14 months (range, 1-130 months).The median follow-up time in
according to each patient's condition.
survivors was 14 months (range, 1-130 months).
LR-free survival was the endpoint of the study. LR was defined as
Surgery was performed for impending or existing pathologic
radiological identification of recurrence in the operated tumor bed.
fractures. All surgeries were performed by two senior orthopedic
Tumor progression in a separate lesion where the tumor had not been
oncologists (HSK and IH). Surgical options regarding resection and
removed was not regarded as LR. Patients with no signs of LR at the
reconstruction were determined by (1) location of the main lesion in the
last imaging were considered censored, meaning that the outcome did
bone; (2) degree of cortical destruction; (3) radiological pattern of the
not occur by the last imaging. LR-free survival was defined as the
lesion (lytic vs sclerotic); (4) presence of separate lesions in the operated
period between the date of surgery and the date of LR or date of last
bone; (5) response to adjuvant radiation therapy or chemotherapy; (6)
imaging. We only considered the first identification of LR in our time-
expected survival time; and (7) patient preference. Resection was
to-event analysis. We obtained data on the following variables for
performed as en-bloc resection or curettage (Table 1). En-bloc resection
association with LR: (1) patient demographics, (2) primary cancer type,
was done by resecting the lesion as a whole with surrounding normal
(3) cancer burden, (4) characteristics of the bone metastatic lesion
tissue. Curettage was performed under direct vision to remove all
operated on, and (5) treatment of the bone metastasis.
grossly visible tumors. Electrocauterization or high-speed burrs were
For patient demographics, patients’ sex and age were retrieved.
used to remove possible remaining tumor when possible. Reconstruc-
One hundred and ninety-five patients were men (65%) (Table 2). The
tion was performed using osteosynthetic devices or endoprostheses.
mean age was 60 years (range, 19-91). For the purpose of analysis,
Osteosynthetic devices were predominantly used after curettage and
patients were dichotomized as ≤60 years (n = 150, 50%) and >60 years
endoprosthetic reconstruction after en-bloc excision. The most
(n = 151, 50%). The most common primary cancers in the study group
common reconstruction methods used were intramedullary nails
were lung cancer (n = 73, 24%), hepatocellular carcinoma (n = 68, 23%),
(n = 154, 52%), bipolar hemiarthroplasty of the hip (n = 52, 17%), and
renal cell carcinoma (n = 51, 17%), and breast cancer (n = 35, 11%). For
megaprosthesis (n = 51, 17%). When osteosynthetic devices were used
the purpose of analysis, patients were grouped into the breast or
after curettage, methylmethacrylate cement augmentation was also was
prostate cancer group, which respond well to the medical treatment, and
KRISHNAN
ET AL.
TABLE 2
| TABLE 2
Patient characteristics N
%
≤60
150
50
>60
151
50
Variable
3
(Continued) N
%
≤6.8
178
59
>6.8
123
41
Variable Size, cm
Age, years
Time from cancer diagnosis to bone metastasis, months
Sex Male
195
65
≤8
152
51
Female
106
35
>8
148
49
Lung cancer
73
24
Hepatocellular carcinoma
68
23
other cancers group.16 Histological confirmation was obtained in all
Renal cell carcinoma
51
17
cases. For cancer burden, time from cancer diagnosis to bone metastasis,
Breast cancer
35
11
Colon cancer
13
4
Prostate
8
3
Sarcoma
6
2
patients (10%) presented with solitary bone metastases at the time of
Bladder cancer
5
2
surgery, defined as metastasis to a single bone without metastasis to
Gastric cancer
5
2
other bones or organs. For characteristics of the bone metastatic lesion
Metastasis of unknown origin
4
1
operated on, the bone operated on, the location of the metastasis within
Others
33
11
the bone, the presence of pathological fractures, and the size of the bone
Primary cancer type
presence of visceral metastases, and presence of solitary metastases were investigated. The median time from the diagnosis of the cancer to the diagnosis of bone metastasis was 8 months (range, 0-248). At the time of surgery, 220 patients (73%) had visceral metastases. Thirty
metastasis were investigated. The femur (n = 208, 70%) and humerus
Involvement of other bones
(n = 70, 23%) were the most common bones operated on. The ends of
Not present
62
21
Present
239
79
Not present
80
27
as the largest diameter on preoperative imaging or pathology report, was
Present
220
73
6.8 cm (range, 2.0-36.0). For treatment of the bone metastasis, surgical
No
270
90
administration of postoperative radiation were investigated. The
Yes
30
10
surgical margin was categorized into en-bloc resection or curettage
the bone were involved in 209 patients (70%) and the shafts in 89 Visceral metastasis
patients (30%). One hundred and forty-six patients (49%) presented with pathological fractures. The mean size of the metastasis, measured
margin, previous radiation to the bone metastatic lesion, and the
Solitary bone metastasis
(Table 1). En-bloc resection was performed in 66 patients (22%) and
Bone operated on
curettage in 235 patients (78%). All patients with en-bloc resection had
Femur
208
70
Humerus
70
23
Tibia
16
5
(range, 8-60 Gy). Postoperative radiation therapy was considered in
Radius
4
1
patients with longer life expectancy, radiation-sensitive primary cancer
Fibula
3
1
or whose tumors were removed with curettage. However, no
bone was undertaken in 121 patients (41%) with a median dose of 30 Gy
prospective criteria was used to administer postoperative radiation
Part of bone Proximal
200
67
Shaft
89
30
Distal
negative margins. Postoperative radiation therapy covering the entire
9
3
therapy. We presented continuous variables as a mean with SD and categorical variables as frequencies with percentages. We used a Chisquare test for categorical variables and analysis of variance for
Pathological fracture
continuous variables. Various clinicopathological factors were analyzed
Absent
155
51
Present
146
49
271
90
variables, multivariate analysis was performed using the variables with P
Sclerotic
19
6
values of 60
91
81
73
55 0.052a
Primary cancer type Lung cancer
82
78
74
74
Hepatocellular carcinoma
90
78
59
29
Renal cell carcinoma
95
85
74
51
Breast cancer
94
85
85
85
Colon cancer
69
35
35
0
Prostate cancer
100
100
100
100
Sarcoma
80
80
80
NA
Bladder cancer
80
80
NA
NA
Gastric cancer
100
NA
NA
NA
Absent
90
86
80
71
Present
88
77
72
62
Visceral metastasis
0.228
Solitary bone metastasis
0.135
No
89
80
73
60
Yes
90
85
85
85
Time from cancer diagnosis to bone metastasis, months
0.375
≤8
88
77
72
59
>8
90
85
78
73
Pathological fracture
0.933
Absent
89
81
74
69
Present
88
80
76
58
Size, cm
0.606
≤6.8
91
83
75
64
>6.8
85
78
74
67
Previous radiotherapy
0.347
Not received
87
82
75
64
Received
100
72
72
72
En-bloc resection
96
87
87
74
Curettage
87
79
72
63
Not received
86
78
70
70
Received
91
84
79
63
Surgical margin
0.037
Postoperative radiotherapy
NA, not available. Breast or prostate cancer vs. others.
a
P-value
0.512
5
6
KRISHNAN
|
ET AL.
(4.5 ± 1.1 months vs 12.2 ± 2.1 months, P = 0.006) (Table 4). On Kaplan-Meier analysis of factors associated with the development of LR, primary cancer type showed a trend toward significance, as patients with prostate cancer or breast cancer had a longer LR-free survival than patients with other cancers (101.7 ± 13.7 months vs 72.2 ± 7.5 months, P = 0.052) (Figure 1) (Table 3). The actuarial local control rate of prostate cancer or breast cancer was higher than that of other cancers (at 1 year, 88.4 ± 5.5% vs 78.8 ± 3.5%; at 2 year, 88.4 ± 5.5% vs 70.8 ± 4.7%, respectively, P = 0.052).
3.3 | Multivariate analysis On multivariate analysis of variables associated with LR-free survival, en-bloc surgical margin (HR = 0.372, P = 0.036) and primary cancers of the breast or prostate (HR = 0.391, P = 0.049) were independent factors associated with a lower likelihood of LR (Table 5). None of the factors related to patient demographics, cancer burden, or characterFIGURE 3 Kaplan-Meier analysis of local recurrence-free survival according to the surgical margin. Patients with en-bloc resection had significantly better local recurrence-free survival rates than patients with curettage (P = 0.037, log rank test)
istics of the bone metastatic lesion were associated with LR-free survival.
4 | DISCUSSION after en-bloc resection was higher than that after curettage (at 1 year, 86.6 ± 6.6% vs 78.9 ± 3.4%; at 2 years, 86.6 ± 6.6% vs 71.1 ± 4.4%, respectively).
The prevalence of bone metastasis is rising due to a higher rate of diagnosis, better systemic treatment, patients with cancer living longer, and a higher disease burden rate.3,17,18 With advances in treatment, patients with cancer are living longer, and thus there is a greater responsibility on the orthopedic surgeon to preserve the
3.2 | Primary cancer type
quality of life by preventing and managing problems related to bone
LR rate varied according to the primary cancer type. The lowest LR rate
metastasis. Surgery for bone metastasis should not fail to outlive the
was observed in patients with prostate cancer (0%, 0/8), followed by
patient, since retreatment may not be possible or safe with advancing
breast cancer (14%, 5/35), and the highest LR rate was observed in
disease.3,7 Causes of failure after bone metastasis surgery can be
patients with colon cancer (31%, 4/13) (Table 4). In addition, the
categorized into either non-oncologic reasons or oncologic reasons,
interval from surgery to LR differed among primary cancer types, as
that is, local recurrence or tumor progression. Most existing literature
lung cancer had significantly a shorter interval than other cancers
on failure after bone metastasis surgery has reported non-oncologic
TABLE 4
Comparison of local recurrence and survival among primary cancer types
Primary cancer type
Number
Number with LR
LR rate
Interval to LRa, months (range)
Lung cancer
73
13
18%
5
Postoperative survivalb, months (95%CI) (1-14)
8
(6-10)
Hepatocellular carcinoma
68
10
15%
11
(2-27)
7
(5-9)
Renal cell carcinoma
51
9
18%
14
(1-34)
9
(7-19)
Breast cancer
35
5
14%
15
(2-52)
16
(8-26)
(1-36)
4
(2-6)
17
(0-43)
Colon cancer
13
4
31%
14
Prostate cancer
8
0
0%
NA
Sarcoma
6
1
17%
NA
14
(3-27)
Bladder cancer
5
1
20%
NA
4
(3-5)
LR, local recurrence; CI, confidence interval; NA, not applicable. a Mean interval from surgery to LR. b Estimated median post-operative survival.
KRISHNAN
ET AL.
TABLE 5 recurrence
|
Multivariate analysis of prognostic factors of local
Prognostic factor
7
renal cell carcinoma.4,21,22 Of note, time to LR showed a trend toward significance as being shorter in the curettage group than in the en-bloc
Risk ratio
P-value
95%CI
group (8.9 ± 10.7 months vs 15.5 ± 14.8 months, P = 0.113). However, we found no difference between the curettage group and the en-bloc
Primary cancer type Breast or prostate
0.391
Others
1
0.154-0.995
0.049
group in terms of the rate of re-treatment (54% [21/39] vs 44% [4/9], respectively, P = 0.933) or re-operation (26% [10/39] vs 22% [2/9], respectively, P = 0.711). This is similar to the observation made by
Surgical margin
Langerhuizen et al.21 No difference in complication rates between the
En-bloc resection
0.372
Curettage
1
0.147-0.939
0.036
two groups was seen; 18% (12/66) of patients who underwent wide resection developed complications compared to 13% (30/235) of patients who underwent curettage.
CI, confidence interval.
LR was affected by the primary cancer type. The LR rate differed according to the primary cancer type, as colon cancer showed the reasons such as implant breakage or infection,8,9,19 and little literature
highest LR rate (31%), while prostate and gastric cancers showed
has focused on oncologic reasons for failure.8 Identification of
lowest LR rate (0%) (Table 4). Moreover, the time to LR differed
associated factors of LR after bone metastasis surgery would be
according to the primary cancer type, as lung cancer showed the
helpful in planning surgery. Although there are studies reporting LR
shortest interval to LR (Table 4). These findings, along with the known
after surgery for bone metastasis to the extremities, they have
prognostic impact of the primary cancer type23 highlight the
included fewer patients and are most pertaining to a single primary
importance of primary cancer type when planning surgery for bone
cancer type or a single bone or a part of a bone. The authors believe
metastasis.
that this study is the first to focus on LR after surgery for bone
No significant difference in LR rate was found between the
metastasis to the extremities in a large cohort of patients with various
patients who received postoperative radiation therapy and those who
primary cancer types. This study investigated a variety of possible
did not (22/121 vs 27/174, respectively, P = 0.545). This finding was
associated factors with respect to LR after surgery for bone metastasis
consistent across all primary cancer types. These findings may be due
to the extremities and identified the surgical margin and the primary
to selection bias, as postoperative radiation could have been
cancer type as independent factors associated with LR.
administered preferentially in patients with a high risk of LR, such as
This study had several limitations to be noted. First, the relatively
an insufficient surgical margin or a larger extent of the tumor. Whether
small number of patients limits the interpretation of our results. Given
or not the administration of postoperative radiation therapy reduces
the different LR patterns observed according the primary cancer types,
LR in bone metastasis to the extremities needs to be validated in larger
a larger number of patients is needed to address the impact of each
cohort, possibly in a prospective setting.
primary cancer type on LR after surgery for bone metastasis. Second,
Factors representing the cancer burden were not associated with
treatment for bone metastasis may not have been standardized, as this
LR. The presence of solitary metastasis (P = 0.135), time from cancer
study was performed over a relatively long period of time. Moreover,
diagnosis to bone metastasis (P = 0.375), and the presence of visceral
medical management of bone metastases, such as chemotherapy, anti-
metastasis (P = 0.228) were not associated with LR. These findings may
bone resorbing drugs, and hormone therapy was not considered.
imply that local control after surgery for bone metastasis is affected
However, our treatment paradigm did remain largely unchanged over
more by local factors, such as the surgical margin, than systemic
the study period. Third, the treatment of the primary cancer and
factors.
metastases to other organs were not considered. Fourth, the testing of
As expected, patients with a longer postoperative survival time
multiple (ie, 11) variables might have increased the chance of finding a
had a higher rate of LR. Twenty-six percent of patients who survived
statistically significant association. Finally, the surveillance protocol for
more than one year after surgery for bone metastasis developed LR as
LR was not uniform. Majority of the patients had only plain radiographs
compared to 4% and 16% of patients who survived for 3 months and
for follow up, which might have led to the underestimation of LR of
12 months, respectively. This is in line with previous studies, where
osteosclerotic metastases such as the metastasis of prostate cancer.
failure after surgery for bone metastasis increased with sur-
The LR rate of this study was 16%, similar to the LR rate of two
vival.3,8,24,25 Of note, the association between survival time and LR
9,20
previous studies, which reported LR rates of 12% and 17%.
Of note,
rate was dependent upon the primary cancer type, as this association
for the purpose of analysis, we counted only the LR in the original
was not evident with lung cancer, possibly due to the shorter interval
tumor bed. There were patients in whom tumor progression was seen
to LR.
in a nearby lesion, which had not been treated. We found a significant difference in the LR rate based on surgical
Of the 49 patients who developed LR, 26 (53%) were symptomatic and had either pain or instability which necessitated retreatment in the
margin, as the LR rate was significantly higher in the curettage group
form of repeat surgery (n = 12), radiation (n = 12), or systemic therapy
than in the en-bloc group (P = 0.03). This finding was consistent across
(n = 2), while 23 (47%) patients received no intervention for their LR.
the various primary cancer types in this study. The importance of
The mean survival time of patients who underwent retreatment for
surgical margin on LR after bone metastasis surgery has been shown in
their LR was significantly longer than that of patients who were not
8
KRISHNAN
|
treated (25.6 ± 20.2 months vs 12.5 ± 13 months, P = 0.020). Patients with a better general condition and lower oncological burden underwent retreatment, giving rise to this significant difference in the survival time between these groups.
5 | C ONC LU SI ON S In conclusion, LR after surgery for bone metastasis to the extremities is affected by the surgical margin and the primary cancer type. These factors, along with the expected patient survival, need to be considered when planning surgery for bone metastasis to the extremities.
ACKNOWLEDGMENTS This work was not supported by any fund.
ORCID Ilkyu Han
http://orcid.org/0000-0001-9841-3775
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How to cite this article: Krishnan CK, Kim H-S, Yun JY, Cho HS, Park JW, Han I. Factors associated with local recurrence after surgery for bone metastasis to the extremities. J Surg Oncol. 2017;1–8. https://doi.org/10.1002/jso.24880
SYNOPSIS There are many reports in the orthopedic literature regarding adequate surgical construction, few studies have been published on local tumor control after surgical stabilization of bone metastasis to the extremities. Therefore, this study sought to identify the local recurrence (LR) rate and to analyze the clinicopathologic factors associated with LR in patients undergoing surgery for bone metastasis to the extremities. LR after surgery for bone metastasis to extremities is affected by surgical margin and primary cancer type.