Closed intramedullary nailing with percutaneous cement ...

 ONCOLOGY

Closed intramedullary nailing with percutaneous cement augmentation for long bone metastases Y-i. Kim, H. G. Kang, J. H. Kim, S-k. Kim, P. P. Lin, H. S. Kim From Orthopaedic Oncology Clinic, National Cancer Center, Gyeonggi-do, Republic of Korea

Aims The purpose of the study was to investigate whether closed intramedullary (IM) nailing with percutaneous cement augmentation is better than conventional closed nailing at relieving pain and suppressing tumours in patients with metastases of the femur and humerus.

Patients and Methods A total of 43 patients (27 men, 16 women, mean age 63.7 years, standard deviation (SD) 12.2; 21 to 84) underwent closed IM nailing with cement augmentation for long bone metastases. A further 27 patients, who underwent conventional closed IM nailing, served as controls. Pain was assessed using a visual analogue scale (VAS) score pre-operatively (pre-operative VAS), one week post-operatively (immediate post-operative VAS), and at six weeks postoperatively (follow-up post-operative VAS). Progression of the tumour was evaluated in subgroups of patients using F-18-fludeoxyglucose (F-18-FDG) positron emission tomography (PET)/computed tomography (CT) and/or bone scintigraphy (BS), at a mean of 8.8 and 7.2 months post-operatively, respectively.

Results

 Y-i. Kim, MD, PhD, Nuclear Medicine Specialist, Department of Nuclear Medicine  H. S. Kim, MD, PhD, Professor, Department of Orthopaedic Surgery Seoul National University Hospital, 101, Daehak-ro, Jongno-gu, Seoul, 03080, Republic of Korea.  H. G. Kang, MD, PhD, Orthopaedic Surgeon, Orthopaedic Oncology Clinic  J. H. Kim, MD, Orthopaedic Surgeon, Orthopaedic Oncology Clinic  S-k. Kim, MD, PhD, Nuclear Medicine Specialist, Department of Nuclear Medicine National Cancer Center, 323, Ilsan-ro, Ilsandong-gu, Goyangsi, Gyeonggi-do, 10408, Republic of Korea.  P. P. Lin, MD, PhD, Professor University of Texas MD Anderson Cancer Center, Department of Orthopaedic Oncology, 1400 Pressler Street, Houston, TX 77030, USA Correspondence should be sent to Dr. H. G. Kang; e-mail: [email protected] ©2016 The British Editorial Society of Bone & Joint Surgery doi:10.1302/0301-620X.98B5. 35312 $2.00 Bone Joint J 2016;98-B:703–9. Received 16 October 2014; Accepted after revision 2 November 2015

VOL. 98-B, No. 5, MAY 2016

The mean pain scores of patients who underwent closed nailing with cement augmentation were significantly lower than those of the control patients post-operatively (immediate post-operative VAS: 3.8, SD 0.9 versus 6.0, SD 0.9; follow-up post-operative VAS: 3.3, SD 2.5 versus 6.6, SD 2.2; all p < 0.001). The progression of the metastasis was suppressed in 50% (10/20) of patients who underwent closed nailing with augmentation, but in only 8% (1/13) of those in the control group.

Conclusion Percutaneous cement augmentation of closed IM nailing improves the relief of pain and limits the progression of the tumour in patients with metastases to the long bones. Take home message: Percutaneous cement augmentation while performing closed IM nailing has some advantages for long bone metastases. Cite this article: Bone Joint J 2016;98-B:703–9.

Pathological fractures occur in approximately 10% of patients with bone metastases and have a poor prognosis.1 Surgery for metastases in long bones with intramedullary (IM) fixation or prosthetic replacement can alleviate pain and allow patients to walk. Consequently, early surgical intervention for a pathological or impending fracture is indicated.2,3 IM nailing is widely used for metadiaphyseal lesions of the long bones and for trochanteric and subtrochanteric lesions of the femur in particular. Immediate bony stability and pain relief may be achieved with low morbidity.4-7 IM nailing may be undertaken using an open or closed technique. Closed IM nailing tends to be used when there is minimal bone destruction and displacement of

the fragments.8,9 It may be combined with percutaneous cement augmentation,10 however, until now there has been no large-scale study which compares closed IM nailing with and without augmentation with cement Augmentation in this way may be used as palliation for the pain of bone metastases.11,12 It has given good results in the treatment of spinal tumours as well as in flat bones such as the pelvis, scapula and sternum.13 However, in weight-bearing bones, stronger fixation is required. On its own, augmentation with cement in long bones runs a high risk of pathological fracture14 and has extremely limited indications in metastatic fractures of these bones.15 703

704

Y-I. KIM, H. G. KANG, J. H. KIM, S-K. KIM, P. P. LIN, H. S. KIM

Table I. Primary tumour and pathological features of fracture Surgery

Primary tumour

Pathological fracture

Closed IM nailing with PC (n = 43)

Lung (22)

PH (14) and DH (2) of femur, PH (5) and DH (1) of humerus PH (4) DH (1) of femur, PH (2) and DH (1) of humerus PH (1) of femur, PH (2) of humerus PH (4) of femur, PH (2) of humerus PH (3) of femur, PH (1) of humerus PH (10) and DH (1) of femur, PH (4) and DH (1) of humerus PH (5) and DH (1) of femur, PH (2) of humerus PH (1) of femur, PH (2) of humerus

Liver/kidney (4)

Conventional closed IM nailing (n = 27)

Breast (3) Multiple myeloma/Oesophagus/Meningioma (2) Prostate/Thyroid/Sarcoma/Unknown (1) Lung (16) Breast/Lidney/Cholangiocarcinoma/Sarcoma (2) Multiple myeloma/Kidney/Endometrium (1)

IM, intramedullary; PC, percutaneous cementoplasty; PH, proximal half; DH, distal half

The percutaneous IM injection of cement has been used in conjunction with flexible (Ender) nails to stabilise metastases of the humerus16 and femur.17 We hypothesised that closed IM nailing and augmentation with cement could be used to treat pathological or impending fractures of long bones. The purpose of the study was to investigate whether this form of treatment is better than conventional closed nailing using clinical evaluation and imaging F-18-fludeoxyglucose (F-18-FDG) positron emission tomography (PET), computed tomography (CT) and bone scintigraphy (BS)).

Patients and Methods Patients. We prospectively studied 43 patients who were to undergo closed IM nailing with cement augmentation for long bone metastases between July 2007 and June 2013. There were 27 men and 16 women with a mean age of 63.7 (standard deviation (SD) 12.2; 21 to 84). There were 29 metastases in the femur and 14 in the humerus. Each patient had an impending or established pathological fracture with a Mirels score > 9 points.18,19 The indication for surgery was the need for pain relief and mechanical stability. Those who underwent closed nailing for osteoporosis or trauma were excluded. Pre-operative decisions were made using a multidisciplinary approach, which included haematologists, radiologists, anaesthetists, radiotherapists, and orthopaedic surgeons. The site of the primary tumours was: lung (22 patients), liver/kidney (four), breast (three), multiple myeloma/ oesophagus/meningioma (two), prostate/thyroid/sarcoma/ unknown (one). The site of fracture was: proximal half of the femur (26); distal half of the femur (three); proximal half of the humerus (12) and distal half of the humerus (two) (Table I). As a control group, 27 patients who only underwent closed nailing were enrolled. Control patients were in the same condition as the study group and had an impending or established fracture with a Mirels score > 9 points but had

refused closed IM nailing with percutaneous cementoplasty (PC). The study had ethical approval and all patients gave informed consent. Surgical technique for closed IM nailing with cement augmentation. Regional anaesthesia was used in most cases.

Spinal anaesthesia was used for those with a femoral fracture and an interscalene or axillary nerve block for those with a humeral fracture. Patients were placed in the lateral decubitus position for femoral nailing and in the deckchair position for humeral nailing. Various different nails were used. A small diameter nail was used to limit reaming and to allow more space around the nail into which to inject the cement. Only proximal reaming and minimal diaphyseal reaming were undertaken. Proximal locking screws were used in all patients: distal locking screws were optional. A distal locking screw was not used if the lesion was in the proximal half of the bone. A percutaneous vertebroplasty (PV) needle (11 gauge, 11 cm poverty needle; Kyungwon Medical, Seoul, Korea) was introduced directly into the metastasis or beside the IM nail. Either two or three needles were used to allow the injection of sufficient cement. Once the location of the needle had been confirmed fluoroscopically, low viscosity polymethylmethacrylate cement (DePuy International Ltd., Blackpool, United Kingdom) was injected into the fracture. The cement was mixed and transferred to a 30 ml syringe. In order to facilitate injection using low finger pressure, it was divided and transferred to several 1 ml syringes. It was injected two to three minutes after mixing. Care was taken to avoid drainage into the venous system or leakage into the surrounding soft tissues. If injection was difficult, a stilette was used to push cement through the lumen of the needle. The cement started to harden after eight minutes and the surgeon tried to complete the injection within ten minutes. The needle was removed after 15 minutes. The anaesthetist monitored the patient’s blood pressure and pulse rate during injection due to the potential toxicity of cement. In order to avoid THE BONE & JOINT JOURNAL

CLOSED INTRAMEDULLARY NAILING WITH PERCUTANEOUS CEMENT AUGMENTATION FOR LONG BONE METASTASES

Fig. 1b

Fig. 1a

Fig. 1d

705

Fig. 1c

Fig. 1e

Closed intramedullary nailing with cement augmentation, radiographs of a) a 64 year-old woman with cancer of the lung and a pathological fracture of the shaft of the left femur with extensive osteolysis proximally including the head and neck; post-operatively, b) anteroposterior and c) lateral radiographs show cement at the site of the lesions and around the nail; d) an injection screw with several holes can be used instead of one proximal locking screw to allow the injection of cement; e) an intraoperative image shows cement injected into the femoral head and neck.

leakage of cement in patients with a pathological fracture, it was injected as far distally as possible from the fracture site. For patients who had concomitant involvement of the femoral head and neck, cement was injected through a hollow perforated screw (HPS, Multihole Injection Screw; Solco Inc., Gyeonggido, Korea) which was introduced between the two proximal locking screws (Fig. 1).16 The mean volume of cement injected at each site was 19.1 ml (SD 7.9 ml; 8.8 to 37.0). Post-operatively, a compression dressing was applied without splint immobilisation. The complications of surgery were evaluated by two orthopaedic surgeons (HGK and JHK), including symptoms and signs of arrhythmia, hypotension, embolism, pneumonia, delilium, heart/lung failure, and failure of fixation. Additional therapy. In the augmentation group, radiotherapy was used in 28 patients (65%); six pre-operatively, 19 post-operatively and three both pre-and post-operatively. A total of 38 patients (88%) had chemotherapy; 14 preVOL. 98-B, No. 5, MAY 2016

operatively, four post-operatively and 20 both pre-and post-operatively. The assessment of pain. Pain was evaluated using a visual analogue scale (VAS) with a range from 0 (no pain) to 10 (worst pain imaginable).20 The pain score was recorded one day pre-operatively (pre-operative), one week post-operatively (immediate post-operative), and at six weeks postoperatively (follow-up post-operative). F-18-FDG PET/CT and BS acquisition and evaluation. In order to identify progression of disease, PET/CT and BS were carried out pre- and post-operatively. Ten patients in the augmentation group and six controls underwent PET/ CT (Discovery VCT; General Electric, Waukesha, Wisconsin) pre- and post-operatively. Pre-operative PET/CT was carried out a mean 2.7 months pre-operatively (SD 1.1; 0.3 to 3.6) and 8.8 months (SD 2.6; 4.2 to 12.6) postoperatively. The images were assessed using a dedicated workstation with intrinsic software (AW Volumeshare;

706


Table II. Patient characteristics

Mean age (yrs) (SD, range) Gender (M:F) Closed IM nailing site (femur:humerus) Mean injected cement amount (ml) (SD) Combined radiation therapy rate (pre- and/or post-operative) (n, %) Mean radiation therapy dose (cGy) (SD) Combined chemotherapy rate (pre- and/or post-operative) (n, %) Mean tumour progression evaluation interval (mths) (SD) Post-operative complication rate (n, %)

Closed IM nailing with PC (n = 43)

Conventional closed IM nailing (n = 27)

p-value

63.7 (12.2) (21 to 84) 27:16 29:14 19.1 (7.9) 28 (65) 3468.5 (719.4) 38 (88) 8.5 (3.8) 4 (9)

68.1 (10.7) (44 to 83) 13:14 16:11 0.0 (0.0) 18 (67) 3008.9 (326.6) 23 (85) 6.3 (2.7) 4 (15)

0.135 0.228 0.487 < 0.001* 0.941 0.152 0.698 0.465 0.701

IM, intramedullary; PC, percutaneous cement augmentation *Statistically significant (p < 0.05)

General Electric). In order to confirm the effect of closed nailing with cement augmentation, we evaluated two metastatic sites in each patient, the operated lesion and an unoperated lesion. Qualitative evaluation was divided into ‘improved’ or ‘worsened’ by two nuclear medicine physicians (YK and SK) blinded to the clinical condition of the patient. ‘Improved’ was defined as reduced extent and intensity of uptake by the lesion, and ‘worsened’ as increased extent and intensity of uptake or a new metastatic lesion. In addition, ten patients in the cement augmentation group and seven controls underwent BS using a doublehead gamma camera (Ecam; Siemens Medical Solutions, Hoffman Estates, Illinois) pre- and post-operatively. The pre-operative scans were carried out 3.5 months preoperatively (SD 1.2; 0.2 to 5.1), and 7.2 months postoperatively (SD 2.9; 3.1 to 11.7) Qualitative evaluation of the scans was carried out in a similar manner to that of PET/CT and the results merged. The metastases were also divided into ‘operated’ and ‘unoperated’ in each patient and evaluation of the lesion was again categorised either as ‘improved’ or ‘worsened’ by the same observers in a blinded fashion. Statistical analysis. The patients’ pre- and post-operative conditions were compared using the t-test for age, amount of cement that was injected, the dose of radiotherapy and the progression of the tumour. The chi-square test was used for gender, the site of closed nailing, combined rate of radiotherapy and chemotherapy. Fisher’s exact test was used for post-operative rate of complications. The mean VAS in the two groups was compared using the repeated-measures analysis of variance (ANOVA). In order to assess the effect of closed nailing with cement augmentation in a homogenous group, the repeated-measure ANOVA of the pain score was assessed in a subgroup of patients with cancer of the lung who had undergone surgery for femoral metastases. Progression of the tumour was assessed from the PET-CT and BS using Fisher’s exact test. A p-value of < 0.05 was considered statistically significant. Statistical analyses were performed using the software package SPSS 18.0 (IBM, Chicago, Illinois) and MedCalc (Ver. 12.2; MedCalc Inc., Mariakerke, Belgium).

Results Evaluation of patients’ pre- and post-operative condition. There was no statistically significant difference between the two groups in terms of age, gender, site of nailing, combined radio- and chemotherapy, dose of radiation, progression of disease and rate of complications three months postoperatively (Table II). Complications of nailing with augmentation (4/43; 9%) were one transient arrhythmia during surgery; one case of pneumonia; one case of delirium, and one death from post-operative heart/lung failure two months after surgery. Complications of conventional nailing (4/27; 15%) were two cases of hypotension during surgery; one case of atelectasis and one death from multiple organ failure due to metastatic disease two months postoperatively. There was no failure of fixation using either technique. The minimum follow-up was 15 months. Of the 43 patients who underwent closed nailing with augmentation, two were lost to follow-up. The mean survivorship of the remaining 41 was 10.1 months (one to 50). Of the 27 who underwent closed nailing alone, two were also lost to follow-up: the mean survivorship of the remaining 25 was 9.2 months (one to 51). The assessment of pain. The mean pre-operative VAS score for pain was 9.5 (7 to 10). No statistically significant difference was found between the two groups (9.5, SD 0.7 vs 9.5, SD 1.0; p = 0.886). Pain was relieved post-operatively in both groups. However, there was a significant difference in pain score between the groups one week post-operatively (mean immediate post-operative VAS: 3.8, SD 0.9 (with augmentation) versus 6.0, SD 0.9 (without augmentation); p < 0.001): this difference persisted until the final review (mean follow-up VAS: 3.3, SD 2.5 (with augmentation) versus 6.6, SD 2.2 (without augmentation); p < 0.001) (Fig. 2a). Subgroup analysis of patients with cancer of the lung and femoral metastases. We studied 15 patients with cancer of

the lung who underwent closed nailing with augmentation for femoral metastases and five who underwent closed nailing alone. The mean pre-operative pain score was not significantly different between the two groups (9.4, SD 0.8 versus 9.0, SD 1.3; p = 0.424). However, there was a THE BONE & JOINT JOURNAL

10

10

9

9

8

8

7

7

6

6 VAS

VAS


5

707

5

4

4

3

3 2

2 Closed IM nailing with PC Closed IM nailing (control)

1

Closed IM nailing with PC (subgroup) Closed IM nailing (subgroup)

1 0

0 Pre-op. VAS

Immediate post-op. VAS

Pre-op. VAS

Follow-up post-op. VAS

Immediate post-op. VAS

Follow-up post-op. VAS

Fig. 2b

Fig. 2a

Visual analogue scale (VAS) pain scores pre- and post-operatively; a) in whole series, pre-operative VAS showed no difference between groups (9.5 0.7 vs. 9.5 SD 1.0; p = 0.886), however, immediate post-operative mean VAS (3.8 SD 0.9 vs. 6.0 SD 0.9; p < 0.001) showed significantly lower scores with closed nailing and augmentation than in controls: this difference persisted until the final (3.3 SD 2.5 vs. 6.6 SD 2.2; p < 0.001); b) in the subgroup of patients with cancer of the lung, the mean pre-operative VAS showed no difference between groups, (9.4 SD 0.8 vs. 9.0 SD 1.3; p = 0.424); however, the mean immediate post-operative score (3.6 SD 1.1 vs. 6.2 SD 1.2; p < 0.001) and follow-up post-operative score (3.3 SD 2.7 vs. 8.2 SD 1.5; p < 0.001) showed significantly lower scores after closed nailing with augmentation. SD

Table III. Tumour progression vs intramedullary (IM) nailing technique Closed IM nailing with cement augmentation (n = 20) (%) Improved (operative site) Worsened (operative site) Worsened (other metastases)

10 (50) 10 (50) 20 (100)

Conventional closed IM nailing (n = 13) (%) 1 (8) 12 (92) 13 (100)

p-value *

0.022

Odds ratio 12.0

* Statistically significant (p < 0.05)

significant difference in the immediate post-operative mean pain score between the two groups (3.6, SD 1.1 versus 6.2, SD 1.2; p < 0.001): this difference persisted during the follow-up period (mean follow-up VAS: 3.3, SD 2.7 (with augmentation) versus 8.2, SD 1.5 (without augmentation); p < 0.001) (Fig. 2b). The evaluation of progression of disease by F-18-FDG PET/ CT and BS. Closed nailing with augmentation showed

improvement in the status of the tumour in 10/20 (50%) of the operated sites, while conventional nailing showed improvement in 1/13 (8%). This was statistically significant (odds ratio = 12.0; p = 0.022) (Table III). All the untreated metastases worsened, with an increase in the extent of the metastasis and/or new metastases both in 20/ 20 (100%) of closed nailing with augmentation and 13/13 (100%) of those without augmentation.

Discussion These results show that closed IM nailing with cement augmentation is better than conventional closed IM nailing. By VOL. 98-B, No. 5, MAY 2016

adding cement, we were able to achieve better relief of pain and reduced progression of the tumour in pathological or impending fractures of the femur and humerus. Recently, augmentation with cement has been widely used for the treatment of metastatic bone tumours, and studied in combination with other surgical techniques. Thus, augmentation as an adjunct to the placement of screws in the neck of the femur,21 and fixation with a flexible nail in non-weight-bearing long bones16,22 have been studied and both gave good clinical outcomes. In our study, we achieved significant relief of pain in the patients who underwent closed nailing with cement augmentation. Moreover, similar results were seen in a homogenous subgroup of patients with cancer of the lung and femoral metastases. Closed nailing with cement augmentataion has many advantages over conventional closed nailing. First, intraand post-operative bleeding is reduced as the cement fills the space around the nail. Secondly, the cement gives early mechanical stability by preventing further destruction of

708


bone and supporting the bone that remains: this results in further relief of pain.14 A previous study of closed nailing with cement augmentation suggested that it relieved pain in patients with a pathological fracture of the humerus.23 Thirdly, filling the canal with cement at the time of nailing may limit the intramedullary spread of tumour. One previous study suggested that the heat generated by the cement during closed nailing could interfere with the blood supply to the tumour thereby reducing progression of disease and its IM dissemination.24 Other authors have reported that the injection of cement induced tumour necrosis and a reduction in its volume.25,26 PET/CT and BS are complementary procedures: both are good imaging modalities for the assessment of bone metastases.27 PET/CT is better than BS for the detection of metastases in bone,28,29 and may be used to assess the effect of treatment on metastatic bone disease.30 In our study, patients who had undergone closed nailing with augmentation were more likely (6/10; 60%) to show a significantly decreased uptake of glucose, indicating suppression of the tumour, than those who had undergone conventional nailing (1/6; 17%, 1/6; p = 0.145).31 BS is a useful initial imaging modality when an aggressive lesion is detected in bone by plain radiography and CT. It can be used to assess skeletal metastases3 and monitor the response to treatment.32 In our study, BS showed an improvement in the extent of the tumour after nailing with cement augmentation in 4/10 patients (40%), while conventional nailing showed no improvement in seven patients (0%). Of the ten patients whose tumour progression was suppressed by closed nailing with augmentation, four did not have radiotherapy. Our study had limitations. First, we could not study the effect of closed nailing with cement augmentation in a primary tumour other than cancer of the lung and operative site (proximal versus distal) due to the relatively small number of patients. Secondly, radiotherapy or chemotherapy, which is essential for treatment, may affect the progression of the tumour. Thirdly, the possible complications of cement augmentation such as extravasation of cement and pulmonary embolism, should be taken into consideration, although these may be prevented by the appropriate preparation of the cement and technique of introduction.33 We can conclude, however, that the addition of cement when undertaking closed IM nailing for long bone metastases gives better relief of pain and less progression of disease than conventional closed nailing. Author contribuitions: Y-i. Kim: Data collection, Data analysis, Writing the paper. H. G. Kang: Study concepts and design, Data collection, Data analysis, Performed surgeries, Writing the paper, Manuscript review. J. H. Kim: Data analysis, Performed surgeries. S-k. Kim: Data analysis, Manuscript review. P. P. Lin: Data analysis, Manuscript review. H. S. Kim: Data analysis, Manuscript review. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. This article was primary edited by A. C. Ross and first proof edited by J. Scott.

References 1. Chow S, McDonald R, Yee A, et al. A multidisciplinary bone metastases clinic at Sunnybrook Odette Cancer Centre: A review of the experience from 2009-2014. Journal of Pain Management 2015;8:117–121. 2. Sarahrudi K, Hora K, Heinz T, Millington S, Vécsei V. Treatment results of pathological fractures of the long bones: a retrospective analysis of 88 patients. Int Orthop 2006;30:519–524. 3. Bickels J, Dadia S, Lidar Z. Surgical management of metastatic bone disease. J Bone Joint Surg [Am] 2009;91-A:1503–1516. 4. Moore RE, Lackman RD. Metastatic bone disease. U Penn Orthopaed J 2010;20:117–120. 5. Piccioli A, Maccauro G, Rossi B, et al. Surgical treatment of pathologic fractures of humerus. Injury 2010;41:1112–1116. 6. Ruggieri P, Mavrogenis AF, Casadei R, et al. Protocol of surgical treatment of long bone pathological fractures. Injury 2010;41:1161–1167. 7. Sharma H, Bhagat S, McCaul J, et al. Intramedullary nailing for pathological femoral fractures. J Orthop Surg (Hong Kong) 2007;15:291–294. 8. Arvinius C, Parra JLC, Mateo LS, et al. Benefits of early intramedullary nailing in femoral metastases. Int Orthop 2014;38:129–132. 9. Weber KL, Randall RL, Grossman S, Parvizi J. Management of lower-extremity bone metastasis. J Bone Joint Surg [Am] 2006;88-A(suppl 4):11–19. 10. Piccioli A, Rossi B, Scaramuzzo L, et al. Intramedullary nailing for treatment of pathologic femoral fractures due to metastases. Injury 2014;45:412–417. 11. Sun G, Jin P, Liu XW, Li M, Li L. Cementoplasty for managing painful bone metastases outside the spine. Eur Radiol 2014;24:731–737. 12. Iannessi A, Amoretti N, Marcy P- Y, Sedat J. Percutaneous cementoplasty for the treatment of extraspinal painful bone lesion, a prospective study. Diagn Interv Imaging 2012;93:859–870. 13. Anselmetti GC. Osteoplasty: percutaneous bone cement injection beyond the spine. Semin Intervent Radiol 2010;27:199–208. 14. Botton E, Edeline J, Rolland Y, et al. Cementoplasty for painful bone metastases: a series of 42 cases. Med Oncol 2012;29:1378–1383. 15. Deschamps F, Farouil G, Hakime A, et al. Cementoplasty of metastases of the proximal femur: is it a safe palliative option? J Vasc Interv Radiol 2012;23:1311–1316. 16. Kim JH, Kang HG, Kim JR, Lin PP, Kim HS. Minimally invasive surgery of humeral metastasis using flexible nails and cement in high-risk patients with advanced cancer. Surg Oncol 2011;20:32–37. 17. Kim YI, Kang HG, Kim TS, et al. Palliative percutaneous stabilization of lower extremity for bone metastasis using flexible nails and bone cement. Surg Oncol 2014;23:192–198. 18. Du ZY, Zang J, Tang XD, Guo W; Chinese Orthopaedic Association Bone Oncology Group. Experts’ agreement on therapy for bone metastases. Orthop Surg 2010;2:241–253. 19. Mirels H. Metastatic disease in long bones. A proposed scoring system for diagnosing impending pathologic fractures. Clin Orthop Relat Res 1989;249:256–264. 20. Kim YI, Kang HG, Kim SK, Kim JH, Kim HS. Clinical outcome prediction of percutaneous cementoplasty for metastatic bone tumor using (18)F-FDG PET-CT. Ann Nucl Med 2013;27:916–923. 21. Deschamps F, Farouil G, Hakime A, et al. Percutaneous stabilization of impending pathological fracture of the proximal femur. Cardiovasc Intervent Radiol 2012;35:1428–1432. 22. Nakata K, Kawai N, Sato M, et al. Percutaneous osteoplasty with a bone marrow nail for fractures of long bones: experimental study. J Vasc Interv Radiol 2010;21:1436–1441. 23. Laitinen M, Nieminen J, Pakarinen T- K. Treatment of pathological humerus shaft fractures with intramedullary nails with or without cement fixation. Arch Orthop Trauma Surg 2011;131:503–508. 24. Kang HG, Roh YW, Kim HS. The treatment of metastasis to the femoral neck using percutaneous hollow perforated screws with cement augmentation. J Bone Joint Surg [Br] 2009;91-B:1078–1082. 25. Uemura A, Matsusako M, Numaguchi Y, et al. Percutaneous sacroplasty for hemorrhagic metastases from hepatocellular carcinoma. AJNR Am J Neuroradiol 2005;26:493–495. 26. San Millán Ruíz D, Burkhardt K, Jean B, et al. Pathology findings with acrylic implants. Bone 1999;25(2 suppl):85S–90S. 27. Meirelles GS, Schöder H, Ravizzini GC, et al. Prognostic value of baseline [18F] fluorodeoxyglucose positron emission tomography and 99mTc-MDP bone scan in progressing metastatic prostate cancer. Clin Cancer Res 2010;16:6093–6099. THE BONE & JOINT JOURNAL


28. Liu T, Xu J- Y, Xu W, et al. Fluorine-18 deoxyglucose positron emission tomography, magnetic resonance imaging and bone scintigraphy for the diagnosis of bone metastases in patients with lung cancer: which one is the best?--a meta-analysis. Clin Oncol (R Coll Radiol) 2011;23:350–358. 29. Song JW, Oh Y- M, Shim T- S, et al. Efficacy comparison between (18)F-FDG PET/ CT and bone scintigraphy in detecting bony metastases of non-small-cell lung cancer. Lung Cancer 2009;65:333–338. 30. Masala S, Schillaci O, Bartolucci AD, et al. Metabolic and clinical assessment of efficacy of cryoablation therapy on skeletal masses by 18F-FDG positron emission tomography/computed tomography (PET/CT) and visual analogue scale (VAS): initial experience. Skeletal Radiol 2011;40:159–165.

VOL. 98-B, No. 5, MAY 2016

709

31. Tateishi U, Gamez C, Dawood S, et al. Bone metastases in patients with metastatic breast cancer: morphologic and metabolic monitoring of response to systemic therapy with integrated PET/CT. Radiology 2008;247:189–196. 32. Tryciecky EW, Gottschalk A, Ludema K. Oncologic imaging: interactions of nuclear medicine with CT and MRI using the bone scan as a model. Semin Nucl Med 1997;27:142–151. 33. Laredo J- D, Hamze B. Complications of percutaneous vertebroplasty and their prevention. Seminars in Ultrasound. CT and MRI 2005;26:65–80.