Pathological fractures caused by metastatic malignant disease have been the subject of increasing interest in recent years. This article describes our experience with the treatment of metastatic bone disease of the upper extremity and our attempt to clarify the indications for different surgical procedures. Of 53 patients with metastatic lesions to the upper extremity, 20 who had been surgically treated were analyzed retrospectively. These comprised 13 men and 7 women with a mean patient age of 62 years. The most common primary tumors to metastasize were lung and liver, with the humerus involved in 12 cases and the scapula and forearm in 4 cases each. Four patients with scapula and forearm involvement underwent tumor resection due to uncontrollable tumor size, while 3 were successfully treated by selective arterial embolization. Three metastases to the humeral head were reconstructed with endoprosthesis, but functional restriction was noted. Five cases with metastases to the humeral shaft were treated with tumor curettage, internal fixation using intramedullary nailing, adjuvant cryosurgery, and cementing. This achieved good results for pain relief and functional restoration with minimal complications. Two metastases to the humeral condyle were unable to be stabilized with plate and locking screws.
Metastatic lesions to the scapula and forearm are commonly treated nonsurgically, but some patients with uncontrollable tumor mass require surgical resection. Endoprosthetic replacement is recommended if the lesion involves the humeral head or condyle. Most patients with the humeral shaft lesion are likely to benefit from tumor curettage, intramedullary nailing with locking screw, and cementing.
Improvement in the treatment of primary cancers has led to increased survival times and an increasing number of patients with bone metastasis.1,2 Although it has received relatively little attention, the humerus is the second most involved bone in cancer patients, accounting for 16% to 39% of cases with actual or impending pathological fractures of the long bones.2-4 Pathologic fractures due to metastatic tumors usually occur late in the course of metastatic disease and are accompanied by severe pain and acute loss of function. To date, most work has focused on the surgical treatment of metastatic lesions of the lower limbs.5,6 Surgical stabilization of the pathological fracture has been recommended, since pathological fractures of weight-bearing bones directly influence the activities of daily living and the quality of life of cancer patients.4,7 Upper-extremity metastasis can result in significant functional loss that hinders personal hygiene and general activities of daily living. However, few reports have focused on metastatic lesions of the upper extremity.8-11
Adequate treatment of metastatic skeletal disease provides immediate pain reduction, stability, increased mobility, and local tumor control, thus easing nurse care as quickly as possible. Conservative treatments, such as casting or splinting, rarely provide sufficient pain relief or the return of extremity function.12 Because of the poor results from conservative treatment, surgical stabilization has become the recommended therapy for pathologic fracture of long bones. The surgical indication and appropriate procedure for metastatic fracture of the upper extremity remain controversial. Patients with a short life expectancy, inoperable condition, or radiosensitive tumors are not suitable candidates for surgery.13 Because of advances in adjuvant treatment and the increased survival of patients with metastatic bone disease, surgeons have been motivated to practice more aggressive treatments. This has led to the application of surgical techniques used for the treatment of primary sarcoma of bone, such as curative resection and megaprosthesis.14
A review of the literature reveals a lack of published data that give clear indications for surgery and recommendations for adequate surgical procedures.15 This article describes our experience with the treatment of metastatic bone disease of the scapula, humerus, and forearm. We also suggest a treatment algorithm for the selection of different modalities and surgical procedures.
Materials and Methods
Between 1999 and 2008 in the outpatient clinic of our institution, we experienced 54 consecutive cases with metastatic lesions (involving lymphoma) of the upper extremity involving the scapula, humerus, or forearm. The diagnoses were made using clinical history, radiographs, bone scintigrams, other imaging modalities, and biopsy. Among these cases, 21 patients were treated in our department for metastatic lesion. Mean patient age was 62 years (range, 37-80 years), and there were 14 men and 7 women. Metastatic lesions were present in the scapula (4), humerus (12), and forearm (5). The primary tumors were located in the lung (7), liver (7), kidney (4), prostate (1), lymphoma (1), and skin (1). All patients were followed up for at least 6 months or until death (Table 1).
The surgical indications used in this study for metastatic bone disease were:
- Pain relief could not be controlled even with opioid drugs.
- Tumor progression was rapid and the tumor size had become uncontrollable.
- Instability of the fracture site could not be controlled by cast or splint.
If at least 1 of these conditions was met, the doctor in charge was consulted for the next 2 points:
- Prognosis was estimated at >3 months.
- General condition allowed surgical intervention.
If both of these conditions were met, surgical treatment was recommended to the patient (Figures 1, 2).
|Figure 1: Treatment options for metastatic bone disease of the scapula and forearm. |
|Figure 2: Treatment options for metastatic bone disease of the humerus. Abbreviations: ADR, adriamycin; w/o, without. |
Preoperative local imaging studies included plain radiograph, computed tomography, and magnetic resonance imaging. Careful attention was paid to the extent of tumor involvement, cortical breakthrough, soft tissue extension, and relationship with the axillary nerve and brachial artery. In 6 patients, selective arterial embolization of the metastatic lesion was performed 1 day preoperatively to decrease intraoperative blood loss.
Different surgical procedures were used for the humerus depending on the site of the metastatic lesion. According to the classification of Bickels et al,8 type I metastasis extended into the humeral head and across the anatomical neck. Type II metastasis involved the humeral diaphysis between the anatomic neck and the supracondylar ridges. Type III metastasis extended to the humeral condyle below the supracondylar ridges.
Surgery was performed in the beach-chair supine position. For type I metastasis, the anterior deltopectolaris approach was used, while for shaft metastasis in type II, the anterolateral approach was used. The site of metastasis was exposed prior to tumor resection. Type I metastases were removed by intra-articular resection of the humeral ends, and type II and III metastases by curettage of the tumor cavity. Cryosurgery was performed as an adjuvant in patients with type II and III metastasis, in which the cortex remained after tumor resection and allowed the containment of liquid nitrogen. It involved freezing the tumor cavity by direct pouring of liquid nitrogen followed by thawing with warm saline. This was repeated 3 times.
After type I resection, an endoprosthesis was inserted into the intramedullary cavity and fixed with polymethylmethacrylate (PMMA) containing gentamicin and adriamycin. An antegrade intramedullary nail with locking screw was used for reconstruction of type II metastasis. After stabilization of the humeral fracture, PMMA was applied to fill the bone cavity defect. For type III metastasis, a side plate with interlocking screws was used to stabilize the metastatic fracture.
The following were evaluated retrospectively: surgical technique, perioperative blood loss, operation time, postoperative pain relief, functional recovery, local and systemic complications, local recurrence, treatment of primary cancer, and postoperative survival time.
According to the evaluation of Dijkstra et al,3 an objective pain scale was classified as none (no pain, 0 points), mild (no pain with analgesics, 1 point), moderate (controllable pain with analgesics, 2 points), and severe (no relief of pain even with analgesics, 3 points). The function of the upper limb was classified as normal (essentially normal function, 0 points), slight (slight impairment of function with normal activities of daily living, 1 point), limited (limited use, 2 points), and inability (inability to use the upper extremity, 3 points).
Results are summarized in Table 2.
Four patients had cancer metastasis to the scapula. In each of these, pain and functional impairment were not severe. The 2 earliest patients underwent tumor resection and cementing due to uncontrollable tumor size (Figure 3). Even with preoperative embolization, perioperative blood loss was approximately 1000 mL. Tumor size was controlled postoperatively with an effective response to chemotherapy. The 2 most recent patients underwent selective arterial embolization by a radiologist, and their tumor masses almost disappeared with chemotherapy.
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|Figure 3: Patient 2 with an uncontrollable tumor of liver cancer. Skin necrosis caused by a rapidly expanding tumor (A). Coronal T2-weighted MRI showing a huge mass extending to the scapula and skin (B). |
Three of 12 patients with type I metastasis underwent wide resection and reconstruction with endoprosthesis (Figure 4). Blood loss was 500 to 1000 mL. Postoperative pain relief was good (1-3 points), but functional recovery remained fair due to the limited range of motion. One patient had axillary nerve palsy, and 1 died unexpectedly 3 months postoperatively.
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|Figure 4: Patient 6 with humerus type I metastasis (head) of liver cancer. Plain radiograph showing pathological fracture and tumor expanding to the humerus head (A). Endoprosthetic reconstruction was performed with successful pain relief (B). |
Five patients with type II metastasis underwent curettage and stabilization with an intramedullary rod (Figure 5). One patient had massive bleeding (5500 mL) during curettage because of the lack of embolization and because a tourniquet was unavailable. Pain relief and functional recovery up to final follow-up were good, even with some local recurrence. Stabilization of the humerus was maintained by the intramedullary nail.
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|Figure 5: Patient 9 with humerus type II metastasis (diaphysis) of kidney cancer. Selective arterial embolization of the metastatic lesion was performed one day preoperatively to decrease intraoperative blood loss (A). After curettage of the tumor and cryosurgery, an antegrade intramedullary nail with locking screw was used for reconstruction. Polymethylmethacrylate containing doxorubicin was applied to fill the bone cavity defect (B). |
Two of 4 patients with type III metastasis underwent curettage, plate fixation, and cementing. Blood loss was controlled by use of a tourniquet. However, the pathological fracture could not be stabilized due to early local recurrence of the cancer. The humeral condyle almost disappeared following recurrence. Pain relief and functional recovery were poor, but reoperation was not performed due to the poor condition of the patients. Two patients with slight impairment of activities of daily living were treated effectively with a splint, and good results were also obtained with chemotherapy.
One patient underwent embolization alone, and the tumor mass diminished during 2 years of follow-up. In a lymphoma case, the fracture was stabilized with a locking plate and bony union was obtained with excellent pain relief. A case with uncontrollable liver cancer to the distal radius successfully underwent nonvascularized fibula graft to stabilize the wrist. A patient with lung cancer metastasis was treated first with a splint but then underwent forearm amputation due to uncontrollable tumor mass. One patient with kidney cancer metastasis to the olecranon underwent resection and reconstruction with endoprosthesis. Pain relief was successful postoperatively.
Metastasis to the Scapula
Metastatic lesions of the scapula are generally treated nonsurgically with immobilization, radiation, chemotherapy, or medical management. In the series of Thai et al,16 only 3 of 96 patients with metastasis of the upper extremity underwent resection. In our series, scapula metastasis showed less pain and less functional impairment compared to humeral metastasis. Two patients underwent resection because of rapid tumor growth and skin necrosis. These conditions, together with destructive lesions of the articular portion of the glenoid, may be the only surgical indications for scapula metastasis (Figure 1).2
Metastasis to the Humerus
Twenty percent of bone metastases occur in the upper limb, with approximately half of these occurring in the humerus.2 To date, many surgical procedures have been described to treat pathologic fractures of the humerus depending on their location.9 Bickels et al8 divided the humerus into 3 regions, and this was slightly modified in the current study. Our strategy for type I metastasis was to perform intra-articular resection of the tumor and endoprosthetic reconstruction (Figure 2). As reported by Thai et al16 and Camnasio et al,14 satisfactory pain relief was achieved but some functional restriction remained.
For type II metastasis, selection of the appropriate surgical procedure is controversial. Surgical treatment options for humeral metastasis include intramedullary nails, plates, and prosthetic replacement. Schürmann et al17 introduced a new iso-elastic diaphyseal prosthesis for humeral shaft reconstruction and obtained clinically successful results. Generally, intramedullary fixation18-21 and internal plate fixation3,9 are the most common techniques used for stabilization of these fractures. Dijkstra et al3 reported both plate fixation and intramedullary nailing with interlocking screw for the surgical treatment of pathologic humeral fracture in 38 patients. They observed no difference in terms of pain relief, function, and complications between the 2 techniques and advocated the use of either procedure for diaphyseal metastatic fracture. On the other hand, Harrington et al22 suggested that plate fixation should generally be avoided for diaphyseal lesions when the screws are placed into structurally inadequate bone. Thai et al16 reported on 51 patients with metastatic bone lesion of the humerus and recommended the use of rigid intramedullary fixation alone.
Intramedullary nails provide effective resistance against angulation, torque, and distraction force. The major advantage of intramedullary nailing compared to plate fixation is the ability to achieve stabilization of the whole bone. A major pitfall of the antegrade interlocking nail is impingement of the acromion during shoulder abduction. This can be prevented by protruding the nail tip deep into the humeral cortical head. However, leaving the tumor mass in situ is a clear disadvantage because it prevents sufficient local tumor control. The tumor could be spread iatrogenically into the distal portion of the marrow cavity by the nail. The rate of local progression using the closed procedure is therefore higher than with open curettage and cement. For good local tumor control, intramedullary fixation should be followed by irradiation.21
As advocated by some authors,16,20 our strategy for type II metastasis was to use tumor curettage, cryosurgery, intramedullary fixation with locking screw, and cement containing doxorubicin. This approach can lead to adequate tumor control and stability of the long bones. However, it involves extensive procedures that are associated with risks of nerve injury, bleeding, infection, delayed wound healing, and local recurrence. To be less invasive, we used the safer approach of deltopectolaris for proximal metastasis and anterolateral for the middle shaft, resulting in no nerve injuries. To prevent massive bleeding, effective preoperative embolization is an essential procedure. Cryosurgery using liquid nitrogen is an effective tool for decreasing the rate of local recurrence. Polymethylmethacrylate containing doxorubicin is also a helpful tool for preventing local recurrence, as well as acting as a filling material for bone defects and thus providing better internal stability (Figure 2).
Some reports have addressed whether surgical intervention influences postoperative survival. Dijkstra et al3 reported no mortality was associated with the surgical procedure of osteosynthesis using plating and intramedullary rods. Hoare23 showed that tumor cells could be detected in blood at the time of intramedullary nailing of pathological fractures. This raises the issue of possible systemic dissemination of tumor cells during the operation, although it did not appear to influence disease outcome.
For type III metastasis, we attempted to stabilize the pathological fracture in 2 patients by using an interlocking plate. However, this failed due to unexpectedly rapid local recurrence. Some patients can be treated conservatively, but endoprosthesis should be the first choice for reconstruction if tumor resection is necessary (Figure 2).13-15
Metastasis to the Forearm
Few reports describe the resection of metastasis in the forearm bones, particularly for large series of patients.11,22 Some authors have recommended the use of a flexible rod or plate.2 In our series, 2 patients underwent surgery due to uncontrollable tumor size. However, the majority of metastatic bone lesions can be treated effectively by nonsurgical procedures such as embolization, radiotherapy, or chemotherapy. An operative indication is less frequent than for the humerus because the forearm has 2 bones: the radius and ulna (Figure 1). If metastatic tumor invaded into the elbow joint, tumor resection and endoprosthesis reconstruction should be considered.
- Aboulafia AJ, Levine AM, Schmidt D, Aboulafia D. Surgical therapy of bone metastases. Semin Oncol. 2007; 34(3):206-214.
- Weber KL, Lewis VO, Randall RL, Lee AK, Springfield D. An approach to the management of the patient with metastatic bone disease. Instr Course Lect. 2004; (53):663-676.
- Dijkstra S, Stapert J, Boxma H, Wiggers T. Treatment of pathological fractures of the humeral shaft due to bone metastases: a comparison of intramedullary locking nail and plate osteosynthesis with adjunctive bone cement. Eur J Surg Oncol. 1996; 22(6):621-626.
- Katzer A, Meenen NM, Grabbe F, Rueger JM. Surgery of skeletal metastases [published online ahead of print December 4, 2001]. Arch Orthop Trauma Surg. 2002; 122(5):251-258.
- Devitt BM, Shelly MJ, Timlin M, OByrne J. Prophylactic stabilization of proximal femoral metastatic bone disease: reconstruction intramedullary nail fracture. Orthopedics. 2008; 31(4):404.
- Manoso MW, Frassica DA, Lietman ES, Frassica FJ. Proximal femoral replacement for metastatic bone disease. Orthopedics. 2007; 30(5):384-388.
- Yazawa Y, Frassica FJ, Chao EY, Pritchard DJ, Sim FH, Shives TC. Metastatic bone disease. A study of the surgical treatment of 166 pathologic humeral and femoral fractures. Clin Orthop Relat Res. 1990; (251):213-219.
- Bickels J, Kollender Y, Wittig JC, Meller I, Malawer MM. Function after resection of humeral metastases: analysis of 59 consecutive patients. Clin Orthop Relat Res. 2005; (437):201-208.
- Frassica FJ, Frassica DA. Metastatic bone disease of the humerus. J Am Acad Orthop Surg. 2003; 11(4):282-288.
- Potter BK, Adams SC, Pitcher JD Jr, Malinin TI, Temple HT. Proximal humerus reconstructions for tumors (published online ahead of print September 27, 2008]. Clin Orthop Relat Res. 2009; 467(4):1035-1041.
- Sarahrudi K, Wolf H, Funovics P, Pajenda G, Hausmann JT, Vécsei V. Surgical treatment of pathological fractures of the shaft of the humerus. J Trauma. 2009; 66(3):789-794.
- Flemming JE, Beals RK. Pathologic fracture of the humerus. Clin Orthop Relat Res. 1986; (203):258-260.
- Weber KL, Lin PP, Yasko AW. Complex segmental elbow reconstruction after tumor resection. Clin Orthop Relat Res. 2003; (415):31-44.
- Camnasio F, Scotti C, Peretti GM, Fontana F, Fraschini G. Prosthetic joint replacement for long bone metastases: analysis of 154 cases [published online ahead of print October 9. 2007]. Arch Orthop Trauma Surg. 2008; 128(8):787-793.
- Manabe J, Kawaguchi N, Matsumoto S, Tanizawa T. Surgical treatment of bone metastasis: indications and outcomes. Int J Clin Oncol. 2005; 10(2):103-111.
- Thai DM, Kitagawa Y, Choong PF. Outcome of surgical management of bony metastases to the humerus and shoulder girdle: a retrospective analysis of 93 patients. Int Semin Surg Oncol. 2006; (3):5-13.
- Schürmann M, Gradl G, Andress HJ, Kauschke T, Hertlein H, Lob G. Metastatic lesions of the humerus treated with the isoelastic diaphysis prosthesis. Clin Orthop Relat Res. 2000; (380):204-214.
- Atesok K, Liebergall M, Sucher E, Temper M, Mosheiff R, Peyser A. Treatment of pathological humeral shaft fractures with unreamed humeral nail [published online ahead of print January 9, 2007]. Ann Surg Oncol. 2007; 14(4):1493-1498.
- Bauze AJ, Clayer MT. Treatment of pathological fractures of the humerus with a locked intramedullary nail. J Orthop Surg (Hong Kong). 2003; 11(1):34-37.
- Chrobok A, Spindel J, Miszczyk L, et al. The surgical management of metastases to humerus-clinical evaluation. Orthop Traumatol Rehabil. 2003; 5(3):348-352.
- Ofluoglu O, Erol B, Ozgen Z, Yildiz M. Minimally invasive treatment of pathological fractures of the humeral shaft [published online ahead of print April 3, 2008]. Int Orthop. 2009; 33(3):707-712.
- Harrington KD, Sim FH, Enis JE, Johnston JO, Diok HM, Gristina AG. Methylmethacrylate as an adjunct in internal fixation of pathological fractures. Experience with three hundred and seventy-five cases. J Bone Joint Surg Am. 1976; 58(8):1047-1055.
- Hoare JR. Pathological fractures. Proceedings of Northwest Metropolitan Orthopaedic Club. J Bone Joint Surg Br. 1968; (50):232.
Drs Muramatsu, Iwanagaa, and Taguchi are from the Department of Orthopedic Surgery, Yamaguchi University School of Medicine, and Dr Ihara is from the Department of Orthopedic Surgery, Kanmon Medical Center, Yamaguchi, Japan.
Drs Muramatsu, Ihara, Iwanagaa, and Taguchi have no relevant financial relationships to disclose.
Correspondence should be addressed to: Keiichi Muramatsu, MD, PhD, Department of Orthopedic Surgery, Yamaguchi University School of Medicine, 1-1-1 Minami-Kogushi, Ube, Yamaguchi 755-8505, Japan (muramatu@ yamaguchi-u.ac.jp).