Exostoses and Vascular Complications in the Lower Limbs: Two Case Reports and Review of the Literature Bahaa Nasr, Benedicte Albert, Charles H. David, Pedro Marques da Fonseca, Ali Badra, and Pierre Gouny, Brest, France
Exostosis is a very common bone tumor. Complications occur in 4% of the cases (nerve compression, exostosis degeneration, orthopedic complication); however, vascular complications are rare. This is the report of 2 cases of vascular complications that occurred in 2 patientsdone with a solitary form and the other with hereditary multiple exostoses. A review of the literature found 57 cases of lower limb vascular complication, secondary to an exostosis. The most common vascular complication was the popliteal aneurysm. Femoral exostosis topography was found in 89% of the cases. A triggering trauma was found in 36% of the cases and the most common form was the solitary exostosis (58%). The treatment of these complications is surgical, and it treats the vascular lesion and the bone tumor at the same time. Surgical treatment of exostosis vascular complications is recommended as an urgent procedure to prevent the occurrence of irreversible damages.
Osteogenic exostosis (also known as osteochondroma) is an abnormal proliferation of bone tissue, in which multiple bony spurs or lumps develop on the bones. It is the most common skeletal tumor, and represents 10e15% of bone tumors that appear during the growth period.1 It is characterized by the growth of cartilage-capped benign bone tumors around areas of active bone growth, particularly the metaphysis of the long bones. Complications occur in 4% of the cases; they include bone deformity, fractures, neurological compression, and vascular damage. The most common vascular complications that may develop are formation of a pseudoaneurysm, stenosis, occlusion, and venous thrombosis. Malignant transformation occurs in 1% of patients with solitary osteochondroma and in 8.3% of patients with hereditary
Department of Thoracic and Cardiovascular Surgery, University Hospital of Brest, Brest, France. Correspondence to: Bahaa Nasr, Service de Chirurgie Cardiaque, Thoracique et Vasculaire, CHU Brest - Cavale Blanche, Bd Tanguy Prigent, 29609 Brest Cedex, France; E-mail: [email protected] Ann Vasc Surg 2015; 29: 1315.e7–1315.e14 http://dx.doi.org/10.1016/j.avsg.2015.02.020 Ó 2015 Elsevier Inc. All rights reserved. Manuscript received: August 23, 2014; manuscript accepted: February 19, 2015; published online: May 29, 2015.
multiple exostosis (HME).2 This is the report of 2 cases of vascular complications that occurred in 2 patientsdone with a solitary form and the other with HME.
CASE REPORTS Case 1 A 17-year-old male patient (1 m 67, 70 kg) was admitted for a lower limb ischemia. He had a history of HME with relevant family history. His father and sister had the same disease but they had never presented complications. The patient complained of a right popliteal fossa pain, with no clear cause of a recent trauma. On physical examination, he had a cold, white and painful right foot, with a global hypoesthesia. Right dorsalis pedis and right posterior tibial artery pulses were absent. He also had a pulsatile right popliteal fossa mass (Fig. 1). The clinical examination revealed the presence of bone spurs in the right wrist. Computed tomography angiography (CTA) showed a pseudoaneurysm of 7 cm in diameter at the right femoropopliteal junction, largely thrombosed. It also showed the absence of opacification of the articular segment of the right popliteal artery extending to the tibiofibular trunk (Fig. 2). The right femoral superficial artery was in contact with the bony spur on the anteromedial face of the distal end of the femur (Fig. 3). 1315.e7
1315.e8 Case reports
Annals of Vascular Surgery
Fig. 1. Pulsatile right popliteal fossa mass. Flattening of the pseudoaneurysm with high popliteal approach was made as an urgent procedure on the same day. After checking the superficial femoral artery and the popliteal artery, a 3 7 cm pseudoaneurysm was developed, as well as a perforation of the artery wall localized in front of the femoral exostosis. The exostosis was removed, and histopathology report confirmed the diagnosis of osteochondroma with no malignant transformation. Vascular damage was then repaired, and an end-to-end anastomosis was made with a 7/0 Prolene separated sutures. Absence of distal thrombus was checked using a size 1 Fogarty catheter. The arteriography revealed the presence of very thin arteries, with an arterial spasm. The immediate follow-up was marked by the absence of distal pulses and the patency of anastomosis was confirmed by the postoperative Doppler. A medical treatment with Nimotop 360 mg/day was established for 48 hr to treat the arterial spasm. In the following days, the pain disappeared, and the CTA confirmed the permeability of the anastomosis and the 3 axes of the leg. The patient was discharged after 12 days of hospitalization. He was seen 1 month after the procedure. He did not complain of any functional discomfort, and he presented an unlimited walking perimeter. Case 2 A 17-year-old male patient (1 m 82, 74 kg) was admitted for a pseudoaneurysm of the left superficial femoral artery associated with an exostosis. Medical history revealed the occurrence of swelling next to the left thigh’s posterior medial side, 1 month after a football trauma. CTA showed a thrombosed pseudoaneurysm of the left superficial
Fig. 2. Computed tomography angiography, pseudoaneurysm of the right femoropopliteal junction, embolic occlusion of the articular segment of the right popliteal artery extending to the tibiofibular trunk.
femoral artery (Fig. 4), and a solitary femoral exostosis on the distal end. The operative procedure was realized with a high popliteal approach, consisting of the pseudoaneurysm’s flattening, exostosis excision, and arterial revascularization using a reverse venous bypass (end-to-end anastomosis) because of the great loss of artery. The patient was discharged after 2 days of hospitalization. Postoperative monitoring showed a clean scar, absence of functional discomfort, and resumption of sports activity. Doppler monitoring confirmed the patency of the vein graft. Review of the Literature Between 1965 and 2013, we collected 57 cases (including our 2 cases) of vascular complications secondary to the lower limb osteochondroma (Table I). It affected young people with a mean age of 20 years (9e51 years). The mean age of the HME was 19.3 years, and 20.9 years for the solitary osteochondroma. It seemed there is a large predominance in men; we found 45 male patients (79%) and 12 female patients (21%). The osteochondromas were often asymptomatic and usually discovered incidentally after an X-ray or during
Vol. 29, No. 6, August 2015
Case reports 1315.e9
Fig. 4. Thrombosed pseudoaneurysm of the left superficial femoral artery. flattening or artery ligature, combined with revascularization by a direct repair of the artery wall (19, 33%); interposing a venous graft (22, 39%); and prosthetic bypass (2, 4%) or direct end-to-end anastomosis of the artery (9, 16%).
DISCUSSION
Fig. 3. Erosion of the right superficial femoral artery by a bony spur on the anteromedial face of the distal end of the femur. a follow-up of the HME form. The most common symptoms were swelling associated with pain in the lower third of the thigh (27, 47%), acute ischemia with cold and pale lower limb (8, 14%), isolated knee pain (9, 16%), isolated thigh swelling (11, 20%), one case of intermittent claudication, and a case of thigh pulsatile mass. In the literature, complications have been described in both forms of the disease. Thirty-five patients (61%) presented a solitary form, 21 patients a multiple exostosis (37%), and it was not informed in one case. The primary location of the osteochondromas was the lower limb. Exostosis topography was found at the femur in 90% of the cases, at the tibia in 9% of the cases (5 patients), and at the fibula in 1 case. Vascular complications concerned most frequently the popliteal artery at the femoropopliteal junction, because of the exostosis placement at the distal end of the femur. Vascular complications were not essentially triggered by an initial trauma. Chronic disease progression was described in 35 (61%) cases, while trigger trauma was found only in 22 (39%) cases. A prevalence of solitary form (13, 65%) was observed in cases of vascular complications with a triggering trauma. The treatment of these vascular complications was surgical and it treated the vascular lesions and the bone tumor at the same operative time. Several surgical techniques have been described: pseudoaneurysm
Osteogenic exostosis is the most common bone tumor. It represents 10e15% of all bone tumors. It occurs mainly during adolescence. It has been described as a solitary form in 1e2% of the population, or it has been included in multiple hereditary osteochondroma pathologic condition. Stocks and Barrington described the HME in 1925. It is a rare genetic autosomal dominant condition with a prevalence of 1 in 50,000.49 This condition has been linked with mutations in 3 different genes. Most of the affected families presented a mutation in the gene EXT1 that maps to chromosome 8q24, and the gene EXT2 that maps to 11p11ep12, while the mutation in the gene EXT3 was probably less common. Paul50 has described pseudoaneurysms secondary to exostosis for the first time in 1953. In this literature review, there are 57 cases; however only Ennker et al.,15 Smits and Moll,26 Vasseur and Fabre,29 and Chaouch et al.45 have described more than one case. The exostosis is made of hyperplasic bone arising from subperiostal displacement of adjacent epiphyseal plane cartilage. These lesions have a protective cartilaginous cap, which ossifies at the end of the growth period with epiphyseal closure. The resorption of this cartilaginous cap might happen in young adults, leaving sharp bone which can be a source of repetitive microtraumatism of the adjacent artery wall during movement (knee flexion extension), leading to a pseudoaneurysm or vessel thrombosis.
Symptoms
Topography
Surgical techniques
Masson and Pullan3
Swelling + pain
Femur
Kover et al.4
Swelling + pain
Femur
Manner and Makinen5 Solhaugh and Olerud6 Shah7
Swelling + pain Swelling + pain Acute ischemia
Femur Femur Femur
Kieffer et al.8 Leve and Kalideen9 Greenway et al.10
Acute ischemia Swelling + pain Pain
Tibia Femur Femur
Israels and Downs11
Swelling + pain
Femur
Metras et al.12
Acute ischemia
Femur
Ferriter et al.13 Zini and Negri14
Swelling + pain Swelling
Tibia Femur
Ennker et al.15
Swelling Swelling + pain
Femur Femur
Lizama et al.16 Marcove et al.17 Woolson et al.18 Harrington et al.19 Asselineau et al.20 Lieberman et al.21 Scott et al.22 Hasselgren et al.23 Kalinga et al.24 Ballaro et al.25 Smits and Moll26
Swelling + pain Pain Swelling + ischemia Pain Swelling + pain Pulsatile mass Swelling + pain Swelling + pain Swelling + pain Swelling + pain Calf swelling Acute ischemia Acute ischemia Pain Pain Swelling
Femur Femur Femur Femur Femur Femur Femur Femur Femur Fibula Tibia Femur Femur Femur Femur Femur
Popliteal artery ligature + venous bypass Pseudoaneurysm resection + venous bypass NI Direct repair Pseudoaneurysm resection + direct repair Flattening + venous bypass Direct repair Pseudoaneurysm resection + end-to-end anastomosis Pseudoaneurysm resection + end-to-end anastomosis Pseudoaneurysm resection + venous bypass Flattening + venous bypass Pseudoaneurysm resection + end-to-end anastomosis Direct repair Pseudoaneurysm resection + end-to-end anastomosis Ligature + direct repair Direct repair Flattening + venous bypass Direct repair Flattening + venous bypass Vein patch Ligature + venous bypass Ligature + prosthetic bypass Ligature + venous bypass Vein patch NI NI NI Venous bypass Vein patch Ligature + venous bypass
Wiater and Farley27 Matsushita et al.28 Vasseur and Fabre29
Age (years)
Exostosis
Artery
Trauma
9
Multiple
High popliteal
No
15
Solitary
High popliteal
Yes
13 17 16
Solitary Multiple Solitary
High popliteal High popliteal High popliteal
No No No
NI 17 16
Solitary Multiple Multiple
Lower popliteal High popliteal High popliteal
No No No
51
Solitary
High popliteal
No
48
Solitary
High popliteal
No
23 32
Solitary Solitary
Lower popliteal High popliteal
No No
20 22
Multiple NI
High popliteal High popliteal
Yes Yes
16 30 13 22 16 19 37 45 16 33 28 39 14 17 13 14
Solitary Multiple Solitary Solitary Solitary Solitary Solitary Multiple Solitary Solitary Solitary Solitary Solitary Multiple Solitary Solitary
High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal Lower popliteal Lower popliteal High popliteal High popliteal High popliteal High popliteal High popliteal
No No No Yes Yes Yes No No No Yes No No Yes Yes Yes Yes
Annals of Vascular Surgery
References
1315.e10 Case reports
Table I. Cases of vascular complications secondary to femoral, tibial, and fibular exostosis reported in the literature
Femur Femur Femur Femur
Cardon et al.30
Pain
Femur
Klebuc et al.31 Otsuka et al.32
Pain Swelling + pain
Femur Femur
T oth et al.33 Perez-Burkhardt and Gomez Castilla34 Taneda et al.35
Swelling + pain Swelling + pain
Femur Femur
Swelling + pain
Femur
Bursztyn et al.36 Antonio et al.37 Orawczyk et al.38 Al-Hadidy et al.39 Argin et al.40 Davies et al.41 Petratos et al.42 Oxenius et al.43 Thevenin et al.44 Chaouch et al.45
Swelling + pain Pain Pain Swelling + pain Swelling Swelling Swelling + pain Swelling + pain Swelling + pain Right swelling Left claudication Swelling + pain Swelling + pain Swelling Swelling + pain
Femur Femur Tibia Femur Femur Femur Femur Femur Femur Femur Femur Tibia Femur Femur Femur
Belmir et al.46 Sadeghi-Azandaryani et al.47 Pavic et al.48 Vanhegan et al.49
Direct repair Direct repair Ligature + venous bypass Pseudoaneurysm resection + end-to-end anastomosis Resection + end-to-end anastomosis Direct repair Pseudoaneurysm resection + end-to-end anastomosis Flattening + prosthetic bypass Direct repair
24 15 22 14
Multiple Multiple Solitary Solitary
High High High High
popliteal popliteal popliteal popliteal
No No No No
12
Solitary
High popliteal
Yes
15 21
Multiple Multiple
High popliteal High popliteal
No Yes
17 14
Multiple Solitary
High popliteal High popliteal
No Yes
Pseudoaneurysm resection + end-to-end anastomosis Flattening + venous bypass Direct repair Direct repair Flattening + venous bypass Flattening + venous bypass Vein patch Vein patch Pericardial patch Flattening + venous bypass Flattening + venous bypass Flattening + venous bypass Flattening + venous bypass NI Flattening + venous bypass Flattening + venous bypass
49
Solitary
High popliteal
No
12 9 14 16 14 18 11 13 21 20
Multiple Solitary Solitary Multiple Solitary Solitary Solitary Solitary Multiple Multiple
20 22 14 21
Solitary Solitary Multiple Multiple
High popliteal High popliteal Lower popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal Lower popliteal High popliteal High popliteal High popliteal
Yes No No No No Yes No Yes Yes No No Yes No No Yes
Vol. 29, No. 6, August 2015
Swelling Swelling Acute ischemia Swelling
NI, not informed.
Case reports 1315.e11
1315.e12 Case reports
In our review, trauma was found in 39% of cases, which confirms the hypothesis of repetitive microtraumatism responsible for chronic disease progression leading to the adjacent artery wall perforation, and the incidence of a pseudoaneurysm. In case of direct trauma, the osteochondroma had perforated the surrounding vessel and had produced an adventitial defect followed by a false aneurysm. These pseudoaneurysms, which evolve into thrombosis, were responsible for the other vascular complications with the occurrence of lower limb ischemia because of the distal arterial embolism, arterial compression, or venous compression and popliteal venous thrombosis. Direct artery compression reduced the artery size leading to a decreased distally arterial flow. This condition was clinically interpreted as a chronic artery disease in young patients, often without cardiovascular risk factors.29 These patients kept a member protective flexion attitude. Exostosis diagnosis is based on patients’ clinical examination. Bone X-ray is systematically performed; it is beneficial when the exostosis is localized at regions inaccessible to clinical examination. Arteriography, long considered the examination of choice, is now being substituted by noninvasive tests, to demonstrate the presence of vascular complications.26,29,31 Furthermore, angiography may fail to see the pseudoaneurysm or underestimate its size because of the presence of the thrombus. The use of computed tomography and magnetic resonance imaging for diagnosis is restricted to exceptional spinal localization. They are interesting for the preoperative check-up, the staging of multiple heredity exostosis, and in case of symptomatic exostosis. They present images that precisely define soft tissues, vascular structures, and bone structures.31 A genetic test is theoretically possible in family members at risk, including the patients’ children. However, this test is not useful because there are currently no preventive measures to avoid the occurrence of exostosis in patients who carry the genetic mutation. The most dreadful exostosis complication is the progression toward the incidence of a sarcoma, mainly chondrosarcoma, and rarely osteosarcoma.1 This complication is suspected when expansion of the exostosis volume is noticed. In this case, an annual clinical and radiological monitoring is recommended. The risk of malignant transformation is about 1%.1 This risk is higher in the case of HME (8.3%).2 In most cases, they are low-grade chondrosarcoma with a risk of local recurrence of 16% and 17.5% at 5 and 10 years, respectively.1 The mortality rate is 1.6% at 5 years.51
Annals of Vascular Surgery
The surgical management is the gold standard. It allows the treatment of exostosis and of the complication in the same operation. The management of vascular complications with endovascular treatment remains limited, especially in the popliteal location. The treatment may consist of either pseudoaneurysm embolization or setting a covered stent. The difficulty in endovascular treatment is also related to the need of excision of the responsible bone tumor in the same operative time. Ayerza et al.52 have described an arthroscopic resection of the exostosis located in the femur lower end, but not for those located on the posterior side because the neurovascular risk is significant. Only one case of embolization of the superficial femoral artery aneurysm was reported by Wong et al.53 Prophylactic resection of the other osteochondromas in patients with HME is not systematically indicated. From our point of view, we think that exostosis excision can be suggested only when artery compression by the exostosis, at the femoropopliteal junction, is highlighted by dynamic shots of a Doppler ultrasound. The annual monitoring should be a dynamic Doppler (flexion/extension of the knee), which could be the indication of exostosis excision.
CONCLUSION Surgical treatment of osteochondroma’s vascular complications is recommended as an urgent procedure, to prevent the occurrence of irreversible damages such as distal vessel occlusion by an embolism or phlebitis with the risk of pulmonary embolism. The excision of the exostosis responsible for the vascular damage seems obvious. REFERENCES 1. Lee KC, Davies AM, Cassar-Pullicino VN. Imaging the complications of osteochondromas. Clin Radiol 2002;57:18e28. 2. Kivioja A, Ervasti H, Kinnunen J, et al. Chondrosarcoma in a family with multiple hereditary exostoses. J Bone Joint Surg Br 2000;82:261e6. 3. Masson AF, Pullan JM. Aneurysm complicating exostosis. Br J Surg 1966;53:929e32. 4. Kover JH, Schwalbe N, Levowitz BS. Popliteal aneurysm due to osteochondroma in athletic injury. N Y State J Med 1970;70:3001e3. 5. Manner R, Makinen E. Angiographic findings in a false popliteal aneurysm due to osteochondroma of the femur. Pediatr Radiol 1975;3:244e6. 6. Solhaugh JH, Olerud SE. Pseudoaneurysm of the femoral artery caused by osteochondroma of the femur. A case report. J Bone Joint Surg Am 1975;57:867e8. 7. Shah PJ. Aneurysm of the popliteal artery secondary to trauma from an osteochondroma of the femur: a case
Vol. 29, No. 6, August 2015
8.
9. 10.
11.
12.
13. 14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
report and review of the literature. Br J Surg 1978;65: 786e8. Kieffer E, Maraval M, Tricot JF, et al. Aneurysm due to an exostosis of the upper end of the tibia. Rev Chir Orthop Reparatrice Appar Mot 1978;64:155e62. Leve L, Kalideen JM. Popliteal false aneurysm complicating osteochondroma. S Afr Med J 1979;1087e8. Greenway G, Resnick D, Bookstein JJ. Popliteal pseudoaneurysm as a complication of an adjacent osteochondroma: angiographic diagnosis. AJR Am J Roentgenol 1979;132: 294e6. Israels SJ, Downs AR. Traumatic aneurysm of the popliteal artery due to an osteochondroma of the femur. Can J Surg 1980;23:270e2. Metras D, Coulibaly AO, Calvy H, et al. Arterial thrombosis of the femoro-popliteal axis: an exceptional case of vascular complication by exostosis. J Mal Vasc 1981;6:289e91. Ferriter P, Hirschy J, Kesseler H, et al. Popliteal pseudoaneurysm. J Bone Joint Surg Am 1983;65:695e7. Zini F, Negri V. A case of popliteal pseudoaneurysm caused by femoral exostoses. Acta Biomed Ateneo Parmense 1984;55:43e7. Ennker J, Freyschmidt J, Reilmann H, et al. False aneurysm of the femoral artery due to an osteochondroma. Arch Orthop Trauma Surg 1984;102:206e9. Lizama VA, Zerbini MA, Gagliardi RA, et al. Popliteal vein thrombosis and popliteal artery pseudoaneurysm complicating osteochondroma of the femur. AJR Am J Roentgenol 1987;148:783e4. Marcove RC, Lindeque BG, Silane MF. Pseudoaneurysm of the popliteal artery with an unusual arteriographic presentation. A case report. Clin Orthop 1988;234:142e4. Woolson ST, Maloney WJ, James DR. Superficial femoral pseudoaneurysm and arterial thromboembolism caused by an osteochondroma. J Pediatr Orthop 1989;9:335e7. Harrington I, Campbell V, Valazques R, et al. Pseudoaneurysm of the popliteal artery as a complication of an osteochondroma. A review of the literature and a case report. Clin Orthop 1991;270:283e7. Asselineau A, Coubret P, Lahoud JC. False aneurysm of the femoral artery complicating exostosis. Rev Chir Orthop Reparatrice Appar Mot 1993;79:411e4. Lieberman J, Mazzucco J, Kwasnik E, et al. Popliteal pseudoaneurysm as a complication of an adjacent osteochondroma. Ann Vasc Surg 1994;8:198e203. Scott EM, White FJ, Jennings PE. Popliteal vein thrombosis associated with femoral osteochondroma and popliteal artery pseudoaneurysm. Postgrad Med J 1995;71:441e2. Hasselgren PO, Eriksson B, Lukes P, et al. False popliteal aneurysm caused by exostosis of the femur. J Cardiovasc Surg 1983;24:540e2. Kalinga MJ, Lo NN, Tan SK. Popliteal artery pseudoaneurysm caused by an osteochondromada traditional medicine massage sequelae. Singapore Med J 1996;37:443e5. Ballaro A, Fox AD, Collin J. Rupture of a popliteal artery pseudoaneurysm secondary to a fibular osteochondroma. Eur J Vasc Endovasc Surg 1997;14:151e2. Smits AB, Moll FL. Unusual arterial complications caused by an osteochondroma of the femur or tibia in young patients. Ann Vasc Surg 1998;12:370e2. Wiater JM, Farley FA. Popliteal pseudoaneurysm caused by an adjacent osteochondroma: a case report and review of the literature. Am J Orthop 1999;28:412e6. Matsushita M, Nishikimi N, Sakurai T, et al. Pseudoaneurysm of the popliteal artery caused by exostosis of the femur:
Case reports 1315.e13
29. 30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
case report and review of the literature. J Vasc Surg 2000;32: 201e4. Vasseur MA, Fabre O. Vascular complications of osteochondromas. Ann Vasc Surg 2000;31:532e8. Cardon A, Aillet S, Ledu J, et al. Pseudo-aneurysm of the popliteal artery by femoral exostosis in a young child. J Cardiovasc Surg (Torino) 2001;42:241e4. Klebuc M, Burrow S, Organek A, et al. Osteochondroma as a causal agent in popliteal artery pseudoaneurysms: case report and literature review. J Reconstr Microsurg 2001;17:475e9. Otsuka T, Yonezawa M, Kamiyama F, et al. Popliteal pseudoaneurysm simulating soft tissue sarcoma: complication of osteochondroma resection. Int J Clin Oncol 2001;6: 105e8. T oth C, Olvaszt o S, Dinya T. Rare case of popliteal artery injury caused by distal femoral exostosis. Case report. Magy Seb 2001;54:115e7. Perez-Burkhardt JL, Gomez Castilla JC. Postraumatic popliteal pseudoaneurysm from femoral osteochondroma: case report and review of the literature. J Vasc Surg 2003;37: 669e71. Taneda Y, Nakamura K, Yano M, et al. Popliteal artery pseudoaneurysm caused by an osteochondroma. Ann Vasc Surg 2004;18:121e3. Bursztyn M, Strcher M, Sanchez JI, et al. Pseudoaneurysm associated with multiple osteochondromatosis. J Pediatr Surg 2005;40:1201e3. Antonio ZP, Alejandro RM, Luis MR, et al. Femur osteochondroma and secondary pseudoaneurysm of the popliteal artery. Arch Orthop Trauma Surg 2006;126:127e30. Orawczyk T, Kuczmik W, Kazibudzki M, et al. Popliteal pseudoaneurysm as a rare complication of a solitary tibial osteochondroma. EJVES Extra 2006;12:21e3. Al-Hadidy AM, Al-Smady MM, Haroun AA, et al. Hereditary multiple exostoses with pseudoaneurysm. Cardiovasc Intervent Radiol 2007;30:537e40. Argin M, Biceroglu S, Arkun R, et al. Solitary osteochondroma causing popliteal pseudoaneurysm that presented as a mass lesion. Diagn Interv Radiol 2007;13:190e2. Davies R, Satti U, Duffield R. Popliteal artery pseudoaneurysm secondary to femoral osteochondroma: a case report and literature review. Ann R Coll Surg Engl 2007;89:8e11. Petratos DV, Bakogiannis KS, Anastasopoulos JN, et al. Popliteal artery pseudoaneurysm secondary to a osteochondroma in children and adolescents: a case report and literature review. J Surg Orthop Adv 2009;18:205e10. Oxenius A, Knirsch W, Kretschmar O, et al. Unclear swelling of the popliteal fossa due to a giant pseudoaneurysm associated with osteochondroma. J Pediatr 2009;154: 147. Thevenin F, Dumaine V, Feydy A, et al. False aneurysm of the femoral artery in multiple exostosis syndrome. J Radiol 2009;90:612e4. Chaouch N, Alimi F, Kortas C, et al. Bilateral popliteal artery complications of multiple hereditary exostosis. Ann Cardiol Angeiol 2011;60:109e12. Belmir H, Azghari A, Mechchat A, et al. Rupture of a popliteal artery pseudo-aneurysm revealing a tibial osteochondroma: case report and review of the literature. J Mal Vasc 2011;36:50e5. Sadeghi-Azandaryani M, Mendl N, Rademacher A, et al. Pseudoaneurysm of the popliteal artery due to osteochondroma of the distal femur. Vasa 2010;39:274e7.
1315.e14 Case reports
48. Pavic P, Vergles D, Sarlija M, et al. Pseudoaneurysm of the popliteal artery in a patient with multiple hereditary exostoses. Ann Vasc Surg 2011;25:268.e1e2. 49. Vanhegan IS, Shehzad KN, Bhatti TS, et al. Acute popliteal pseudoaneurysm rupture secondary to distal femoral osteochondroma in a patient with hereditary multiple exostoses. Ann R Coll Surg Engl 2012;94:134e6. 50. Paul M. Aneurysm of the popliteal artery from perforation by a cancellous exostosis of the femur. J Bone Joint Surg Br 1953;35:270e1.
Annals of Vascular Surgery
51. Ahmed AR, Tan TS, Unni KK, et al. Secondary chondrosarcoma in osteochondroma: report of 107 patients. Clin Orthop Relat Res 2003;411:193e206. 52. Ayerza MA, Abalo E, Aponte-Tinao L, et al. Endoscopic resection of symptomatic osteochondroma of the distal femur. Clin Orthop Relat Res 2007;459: 150e3. 53. Wong KT, Chu WC, Griffith JF, et al. Pseudoaneurysm complicating osteochondromas: symptom relief with embolization. Clin Orthop 2002;404:339e42.
Exostosis is a very common bone tumor. Complications occur in 4% of the cases (nerve compression, exostosis degeneration, orthopedic complication); however, vascular complications are rare. This is the report of 2 cases of vascular complications that occurred in 2 patientsdone with a solitary form and the other with hereditary multiple exostoses. A review of the literature found 57 cases of lower limb vascular complication, secondary to an exostosis. The most common vascular complication was the popliteal aneurysm. Femoral exostosis topography was found in 89% of the cases. A triggering trauma was found in 36% of the cases and the most common form was the solitary exostosis (58%). The treatment of these complications is surgical, and it treats the vascular lesion and the bone tumor at the same time. Surgical treatment of exostosis vascular complications is recommended as an urgent procedure to prevent the occurrence of irreversible damages.
Osteogenic exostosis (also known as osteochondroma) is an abnormal proliferation of bone tissue, in which multiple bony spurs or lumps develop on the bones. It is the most common skeletal tumor, and represents 10e15% of bone tumors that appear during the growth period.1 It is characterized by the growth of cartilage-capped benign bone tumors around areas of active bone growth, particularly the metaphysis of the long bones. Complications occur in 4% of the cases; they include bone deformity, fractures, neurological compression, and vascular damage. The most common vascular complications that may develop are formation of a pseudoaneurysm, stenosis, occlusion, and venous thrombosis. Malignant transformation occurs in 1% of patients with solitary osteochondroma and in 8.3% of patients with hereditary
Department of Thoracic and Cardiovascular Surgery, University Hospital of Brest, Brest, France. Correspondence to: Bahaa Nasr, Service de Chirurgie Cardiaque, Thoracique et Vasculaire, CHU Brest - Cavale Blanche, Bd Tanguy Prigent, 29609 Brest Cedex, France; E-mail: [email protected] Ann Vasc Surg 2015; 29: 1315.e7–1315.e14 http://dx.doi.org/10.1016/j.avsg.2015.02.020 Ó 2015 Elsevier Inc. All rights reserved. Manuscript received: August 23, 2014; manuscript accepted: February 19, 2015; published online: May 29, 2015.
multiple exostosis (HME).2 This is the report of 2 cases of vascular complications that occurred in 2 patientsdone with a solitary form and the other with HME.
CASE REPORTS Case 1 A 17-year-old male patient (1 m 67, 70 kg) was admitted for a lower limb ischemia. He had a history of HME with relevant family history. His father and sister had the same disease but they had never presented complications. The patient complained of a right popliteal fossa pain, with no clear cause of a recent trauma. On physical examination, he had a cold, white and painful right foot, with a global hypoesthesia. Right dorsalis pedis and right posterior tibial artery pulses were absent. He also had a pulsatile right popliteal fossa mass (Fig. 1). The clinical examination revealed the presence of bone spurs in the right wrist. Computed tomography angiography (CTA) showed a pseudoaneurysm of 7 cm in diameter at the right femoropopliteal junction, largely thrombosed. It also showed the absence of opacification of the articular segment of the right popliteal artery extending to the tibiofibular trunk (Fig. 2). The right femoral superficial artery was in contact with the bony spur on the anteromedial face of the distal end of the femur (Fig. 3). 1315.e7
1315.e8 Case reports
Annals of Vascular Surgery
Fig. 1. Pulsatile right popliteal fossa mass. Flattening of the pseudoaneurysm with high popliteal approach was made as an urgent procedure on the same day. After checking the superficial femoral artery and the popliteal artery, a 3 7 cm pseudoaneurysm was developed, as well as a perforation of the artery wall localized in front of the femoral exostosis. The exostosis was removed, and histopathology report confirmed the diagnosis of osteochondroma with no malignant transformation. Vascular damage was then repaired, and an end-to-end anastomosis was made with a 7/0 Prolene separated sutures. Absence of distal thrombus was checked using a size 1 Fogarty catheter. The arteriography revealed the presence of very thin arteries, with an arterial spasm. The immediate follow-up was marked by the absence of distal pulses and the patency of anastomosis was confirmed by the postoperative Doppler. A medical treatment with Nimotop 360 mg/day was established for 48 hr to treat the arterial spasm. In the following days, the pain disappeared, and the CTA confirmed the permeability of the anastomosis and the 3 axes of the leg. The patient was discharged after 12 days of hospitalization. He was seen 1 month after the procedure. He did not complain of any functional discomfort, and he presented an unlimited walking perimeter. Case 2 A 17-year-old male patient (1 m 82, 74 kg) was admitted for a pseudoaneurysm of the left superficial femoral artery associated with an exostosis. Medical history revealed the occurrence of swelling next to the left thigh’s posterior medial side, 1 month after a football trauma. CTA showed a thrombosed pseudoaneurysm of the left superficial
Fig. 2. Computed tomography angiography, pseudoaneurysm of the right femoropopliteal junction, embolic occlusion of the articular segment of the right popliteal artery extending to the tibiofibular trunk.
femoral artery (Fig. 4), and a solitary femoral exostosis on the distal end. The operative procedure was realized with a high popliteal approach, consisting of the pseudoaneurysm’s flattening, exostosis excision, and arterial revascularization using a reverse venous bypass (end-to-end anastomosis) because of the great loss of artery. The patient was discharged after 2 days of hospitalization. Postoperative monitoring showed a clean scar, absence of functional discomfort, and resumption of sports activity. Doppler monitoring confirmed the patency of the vein graft. Review of the Literature Between 1965 and 2013, we collected 57 cases (including our 2 cases) of vascular complications secondary to the lower limb osteochondroma (Table I). It affected young people with a mean age of 20 years (9e51 years). The mean age of the HME was 19.3 years, and 20.9 years for the solitary osteochondroma. It seemed there is a large predominance in men; we found 45 male patients (79%) and 12 female patients (21%). The osteochondromas were often asymptomatic and usually discovered incidentally after an X-ray or during
Vol. 29, No. 6, August 2015
Case reports 1315.e9
Fig. 4. Thrombosed pseudoaneurysm of the left superficial femoral artery. flattening or artery ligature, combined with revascularization by a direct repair of the artery wall (19, 33%); interposing a venous graft (22, 39%); and prosthetic bypass (2, 4%) or direct end-to-end anastomosis of the artery (9, 16%).
DISCUSSION
Fig. 3. Erosion of the right superficial femoral artery by a bony spur on the anteromedial face of the distal end of the femur. a follow-up of the HME form. The most common symptoms were swelling associated with pain in the lower third of the thigh (27, 47%), acute ischemia with cold and pale lower limb (8, 14%), isolated knee pain (9, 16%), isolated thigh swelling (11, 20%), one case of intermittent claudication, and a case of thigh pulsatile mass. In the literature, complications have been described in both forms of the disease. Thirty-five patients (61%) presented a solitary form, 21 patients a multiple exostosis (37%), and it was not informed in one case. The primary location of the osteochondromas was the lower limb. Exostosis topography was found at the femur in 90% of the cases, at the tibia in 9% of the cases (5 patients), and at the fibula in 1 case. Vascular complications concerned most frequently the popliteal artery at the femoropopliteal junction, because of the exostosis placement at the distal end of the femur. Vascular complications were not essentially triggered by an initial trauma. Chronic disease progression was described in 35 (61%) cases, while trigger trauma was found only in 22 (39%) cases. A prevalence of solitary form (13, 65%) was observed in cases of vascular complications with a triggering trauma. The treatment of these vascular complications was surgical and it treated the vascular lesions and the bone tumor at the same operative time. Several surgical techniques have been described: pseudoaneurysm
Osteogenic exostosis is the most common bone tumor. It represents 10e15% of all bone tumors. It occurs mainly during adolescence. It has been described as a solitary form in 1e2% of the population, or it has been included in multiple hereditary osteochondroma pathologic condition. Stocks and Barrington described the HME in 1925. It is a rare genetic autosomal dominant condition with a prevalence of 1 in 50,000.49 This condition has been linked with mutations in 3 different genes. Most of the affected families presented a mutation in the gene EXT1 that maps to chromosome 8q24, and the gene EXT2 that maps to 11p11ep12, while the mutation in the gene EXT3 was probably less common. Paul50 has described pseudoaneurysms secondary to exostosis for the first time in 1953. In this literature review, there are 57 cases; however only Ennker et al.,15 Smits and Moll,26 Vasseur and Fabre,29 and Chaouch et al.45 have described more than one case. The exostosis is made of hyperplasic bone arising from subperiostal displacement of adjacent epiphyseal plane cartilage. These lesions have a protective cartilaginous cap, which ossifies at the end of the growth period with epiphyseal closure. The resorption of this cartilaginous cap might happen in young adults, leaving sharp bone which can be a source of repetitive microtraumatism of the adjacent artery wall during movement (knee flexion extension), leading to a pseudoaneurysm or vessel thrombosis.
Symptoms
Topography
Surgical techniques
Masson and Pullan3
Swelling + pain
Femur
Kover et al.4
Swelling + pain
Femur
Manner and Makinen5 Solhaugh and Olerud6 Shah7
Swelling + pain Swelling + pain Acute ischemia
Femur Femur Femur
Kieffer et al.8 Leve and Kalideen9 Greenway et al.10
Acute ischemia Swelling + pain Pain
Tibia Femur Femur
Israels and Downs11
Swelling + pain
Femur
Metras et al.12
Acute ischemia
Femur
Ferriter et al.13 Zini and Negri14
Swelling + pain Swelling
Tibia Femur
Ennker et al.15
Swelling Swelling + pain
Femur Femur
Lizama et al.16 Marcove et al.17 Woolson et al.18 Harrington et al.19 Asselineau et al.20 Lieberman et al.21 Scott et al.22 Hasselgren et al.23 Kalinga et al.24 Ballaro et al.25 Smits and Moll26
Swelling + pain Pain Swelling + ischemia Pain Swelling + pain Pulsatile mass Swelling + pain Swelling + pain Swelling + pain Swelling + pain Calf swelling Acute ischemia Acute ischemia Pain Pain Swelling
Femur Femur Femur Femur Femur Femur Femur Femur Femur Fibula Tibia Femur Femur Femur Femur Femur
Popliteal artery ligature + venous bypass Pseudoaneurysm resection + venous bypass NI Direct repair Pseudoaneurysm resection + direct repair Flattening + venous bypass Direct repair Pseudoaneurysm resection + end-to-end anastomosis Pseudoaneurysm resection + end-to-end anastomosis Pseudoaneurysm resection + venous bypass Flattening + venous bypass Pseudoaneurysm resection + end-to-end anastomosis Direct repair Pseudoaneurysm resection + end-to-end anastomosis Ligature + direct repair Direct repair Flattening + venous bypass Direct repair Flattening + venous bypass Vein patch Ligature + venous bypass Ligature + prosthetic bypass Ligature + venous bypass Vein patch NI NI NI Venous bypass Vein patch Ligature + venous bypass
Wiater and Farley27 Matsushita et al.28 Vasseur and Fabre29
Age (years)
Exostosis
Artery
Trauma
9
Multiple
High popliteal
No
15
Solitary
High popliteal
Yes
13 17 16
Solitary Multiple Solitary
High popliteal High popliteal High popliteal
No No No
NI 17 16
Solitary Multiple Multiple
Lower popliteal High popliteal High popliteal
No No No
51
Solitary
High popliteal
No
48
Solitary
High popliteal
No
23 32
Solitary Solitary
Lower popliteal High popliteal
No No
20 22
Multiple NI
High popliteal High popliteal
Yes Yes
16 30 13 22 16 19 37 45 16 33 28 39 14 17 13 14
Solitary Multiple Solitary Solitary Solitary Solitary Solitary Multiple Solitary Solitary Solitary Solitary Solitary Multiple Solitary Solitary
High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal Lower popliteal Lower popliteal High popliteal High popliteal High popliteal High popliteal High popliteal
No No No Yes Yes Yes No No No Yes No No Yes Yes Yes Yes
Annals of Vascular Surgery
References
1315.e10 Case reports
Table I. Cases of vascular complications secondary to femoral, tibial, and fibular exostosis reported in the literature
Femur Femur Femur Femur
Cardon et al.30
Pain
Femur
Klebuc et al.31 Otsuka et al.32
Pain Swelling + pain
Femur Femur
T oth et al.33 Perez-Burkhardt and Gomez Castilla34 Taneda et al.35
Swelling + pain Swelling + pain
Femur Femur
Swelling + pain
Femur
Bursztyn et al.36 Antonio et al.37 Orawczyk et al.38 Al-Hadidy et al.39 Argin et al.40 Davies et al.41 Petratos et al.42 Oxenius et al.43 Thevenin et al.44 Chaouch et al.45
Swelling + pain Pain Pain Swelling + pain Swelling Swelling Swelling + pain Swelling + pain Swelling + pain Right swelling Left claudication Swelling + pain Swelling + pain Swelling Swelling + pain
Femur Femur Tibia Femur Femur Femur Femur Femur Femur Femur Femur Tibia Femur Femur Femur
Belmir et al.46 Sadeghi-Azandaryani et al.47 Pavic et al.48 Vanhegan et al.49
Direct repair Direct repair Ligature + venous bypass Pseudoaneurysm resection + end-to-end anastomosis Resection + end-to-end anastomosis Direct repair Pseudoaneurysm resection + end-to-end anastomosis Flattening + prosthetic bypass Direct repair
24 15 22 14
Multiple Multiple Solitary Solitary
High High High High
popliteal popliteal popliteal popliteal
No No No No
12
Solitary
High popliteal
Yes
15 21
Multiple Multiple
High popliteal High popliteal
No Yes
17 14
Multiple Solitary
High popliteal High popliteal
No Yes
Pseudoaneurysm resection + end-to-end anastomosis Flattening + venous bypass Direct repair Direct repair Flattening + venous bypass Flattening + venous bypass Vein patch Vein patch Pericardial patch Flattening + venous bypass Flattening + venous bypass Flattening + venous bypass Flattening + venous bypass NI Flattening + venous bypass Flattening + venous bypass
49
Solitary
High popliteal
No
12 9 14 16 14 18 11 13 21 20
Multiple Solitary Solitary Multiple Solitary Solitary Solitary Solitary Multiple Multiple
20 22 14 21
Solitary Solitary Multiple Multiple
High popliteal High popliteal Lower popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal High popliteal Lower popliteal High popliteal High popliteal High popliteal
Yes No No No No Yes No Yes Yes No No Yes No No Yes
Vol. 29, No. 6, August 2015
Swelling Swelling Acute ischemia Swelling
NI, not informed.
Case reports 1315.e11
1315.e12 Case reports
In our review, trauma was found in 39% of cases, which confirms the hypothesis of repetitive microtraumatism responsible for chronic disease progression leading to the adjacent artery wall perforation, and the incidence of a pseudoaneurysm. In case of direct trauma, the osteochondroma had perforated the surrounding vessel and had produced an adventitial defect followed by a false aneurysm. These pseudoaneurysms, which evolve into thrombosis, were responsible for the other vascular complications with the occurrence of lower limb ischemia because of the distal arterial embolism, arterial compression, or venous compression and popliteal venous thrombosis. Direct artery compression reduced the artery size leading to a decreased distally arterial flow. This condition was clinically interpreted as a chronic artery disease in young patients, often without cardiovascular risk factors.29 These patients kept a member protective flexion attitude. Exostosis diagnosis is based on patients’ clinical examination. Bone X-ray is systematically performed; it is beneficial when the exostosis is localized at regions inaccessible to clinical examination. Arteriography, long considered the examination of choice, is now being substituted by noninvasive tests, to demonstrate the presence of vascular complications.26,29,31 Furthermore, angiography may fail to see the pseudoaneurysm or underestimate its size because of the presence of the thrombus. The use of computed tomography and magnetic resonance imaging for diagnosis is restricted to exceptional spinal localization. They are interesting for the preoperative check-up, the staging of multiple heredity exostosis, and in case of symptomatic exostosis. They present images that precisely define soft tissues, vascular structures, and bone structures.31 A genetic test is theoretically possible in family members at risk, including the patients’ children. However, this test is not useful because there are currently no preventive measures to avoid the occurrence of exostosis in patients who carry the genetic mutation. The most dreadful exostosis complication is the progression toward the incidence of a sarcoma, mainly chondrosarcoma, and rarely osteosarcoma.1 This complication is suspected when expansion of the exostosis volume is noticed. In this case, an annual clinical and radiological monitoring is recommended. The risk of malignant transformation is about 1%.1 This risk is higher in the case of HME (8.3%).2 In most cases, they are low-grade chondrosarcoma with a risk of local recurrence of 16% and 17.5% at 5 and 10 years, respectively.1 The mortality rate is 1.6% at 5 years.51
Annals of Vascular Surgery
The surgical management is the gold standard. It allows the treatment of exostosis and of the complication in the same operation. The management of vascular complications with endovascular treatment remains limited, especially in the popliteal location. The treatment may consist of either pseudoaneurysm embolization or setting a covered stent. The difficulty in endovascular treatment is also related to the need of excision of the responsible bone tumor in the same operative time. Ayerza et al.52 have described an arthroscopic resection of the exostosis located in the femur lower end, but not for those located on the posterior side because the neurovascular risk is significant. Only one case of embolization of the superficial femoral artery aneurysm was reported by Wong et al.53 Prophylactic resection of the other osteochondromas in patients with HME is not systematically indicated. From our point of view, we think that exostosis excision can be suggested only when artery compression by the exostosis, at the femoropopliteal junction, is highlighted by dynamic shots of a Doppler ultrasound. The annual monitoring should be a dynamic Doppler (flexion/extension of the knee), which could be the indication of exostosis excision.
CONCLUSION Surgical treatment of osteochondroma’s vascular complications is recommended as an urgent procedure, to prevent the occurrence of irreversible damages such as distal vessel occlusion by an embolism or phlebitis with the risk of pulmonary embolism. The excision of the exostosis responsible for the vascular damage seems obvious. REFERENCES 1. Lee KC, Davies AM, Cassar-Pullicino VN. Imaging the complications of osteochondromas. Clin Radiol 2002;57:18e28. 2. Kivioja A, Ervasti H, Kinnunen J, et al. Chondrosarcoma in a family with multiple hereditary exostoses. J Bone Joint Surg Br 2000;82:261e6. 3. Masson AF, Pullan JM. Aneurysm complicating exostosis. Br J Surg 1966;53:929e32. 4. Kover JH, Schwalbe N, Levowitz BS. Popliteal aneurysm due to osteochondroma in athletic injury. N Y State J Med 1970;70:3001e3. 5. Manner R, Makinen E. Angiographic findings in a false popliteal aneurysm due to osteochondroma of the femur. Pediatr Radiol 1975;3:244e6. 6. Solhaugh JH, Olerud SE. Pseudoaneurysm of the femoral artery caused by osteochondroma of the femur. A case report. J Bone Joint Surg Am 1975;57:867e8. 7. Shah PJ. Aneurysm of the popliteal artery secondary to trauma from an osteochondroma of the femur: a case
Vol. 29, No. 6, August 2015
8.
9. 10.
11.
12.
13. 14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
report and review of the literature. Br J Surg 1978;65: 786e8. Kieffer E, Maraval M, Tricot JF, et al. Aneurysm due to an exostosis of the upper end of the tibia. Rev Chir Orthop Reparatrice Appar Mot 1978;64:155e62. Leve L, Kalideen JM. Popliteal false aneurysm complicating osteochondroma. S Afr Med J 1979;1087e8. Greenway G, Resnick D, Bookstein JJ. Popliteal pseudoaneurysm as a complication of an adjacent osteochondroma: angiographic diagnosis. AJR Am J Roentgenol 1979;132: 294e6. Israels SJ, Downs AR. Traumatic aneurysm of the popliteal artery due to an osteochondroma of the femur. Can J Surg 1980;23:270e2. Metras D, Coulibaly AO, Calvy H, et al. Arterial thrombosis of the femoro-popliteal axis: an exceptional case of vascular complication by exostosis. J Mal Vasc 1981;6:289e91. Ferriter P, Hirschy J, Kesseler H, et al. Popliteal pseudoaneurysm. J Bone Joint Surg Am 1983;65:695e7. Zini F, Negri V. A case of popliteal pseudoaneurysm caused by femoral exostoses. Acta Biomed Ateneo Parmense 1984;55:43e7. Ennker J, Freyschmidt J, Reilmann H, et al. False aneurysm of the femoral artery due to an osteochondroma. Arch Orthop Trauma Surg 1984;102:206e9. Lizama VA, Zerbini MA, Gagliardi RA, et al. Popliteal vein thrombosis and popliteal artery pseudoaneurysm complicating osteochondroma of the femur. AJR Am J Roentgenol 1987;148:783e4. Marcove RC, Lindeque BG, Silane MF. Pseudoaneurysm of the popliteal artery with an unusual arteriographic presentation. A case report. Clin Orthop 1988;234:142e4. Woolson ST, Maloney WJ, James DR. Superficial femoral pseudoaneurysm and arterial thromboembolism caused by an osteochondroma. J Pediatr Orthop 1989;9:335e7. Harrington I, Campbell V, Valazques R, et al. Pseudoaneurysm of the popliteal artery as a complication of an osteochondroma. A review of the literature and a case report. Clin Orthop 1991;270:283e7. Asselineau A, Coubret P, Lahoud JC. False aneurysm of the femoral artery complicating exostosis. Rev Chir Orthop Reparatrice Appar Mot 1993;79:411e4. Lieberman J, Mazzucco J, Kwasnik E, et al. Popliteal pseudoaneurysm as a complication of an adjacent osteochondroma. Ann Vasc Surg 1994;8:198e203. Scott EM, White FJ, Jennings PE. Popliteal vein thrombosis associated with femoral osteochondroma and popliteal artery pseudoaneurysm. Postgrad Med J 1995;71:441e2. Hasselgren PO, Eriksson B, Lukes P, et al. False popliteal aneurysm caused by exostosis of the femur. J Cardiovasc Surg 1983;24:540e2. Kalinga MJ, Lo NN, Tan SK. Popliteal artery pseudoaneurysm caused by an osteochondromada traditional medicine massage sequelae. Singapore Med J 1996;37:443e5. Ballaro A, Fox AD, Collin J. Rupture of a popliteal artery pseudoaneurysm secondary to a fibular osteochondroma. Eur J Vasc Endovasc Surg 1997;14:151e2. Smits AB, Moll FL. Unusual arterial complications caused by an osteochondroma of the femur or tibia in young patients. Ann Vasc Surg 1998;12:370e2. Wiater JM, Farley FA. Popliteal pseudoaneurysm caused by an adjacent osteochondroma: a case report and review of the literature. Am J Orthop 1999;28:412e6. Matsushita M, Nishikimi N, Sakurai T, et al. Pseudoaneurysm of the popliteal artery caused by exostosis of the femur:
Case reports 1315.e13
29. 30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
case report and review of the literature. J Vasc Surg 2000;32: 201e4. Vasseur MA, Fabre O. Vascular complications of osteochondromas. Ann Vasc Surg 2000;31:532e8. Cardon A, Aillet S, Ledu J, et al. Pseudo-aneurysm of the popliteal artery by femoral exostosis in a young child. J Cardiovasc Surg (Torino) 2001;42:241e4. Klebuc M, Burrow S, Organek A, et al. Osteochondroma as a causal agent in popliteal artery pseudoaneurysms: case report and literature review. J Reconstr Microsurg 2001;17:475e9. Otsuka T, Yonezawa M, Kamiyama F, et al. Popliteal pseudoaneurysm simulating soft tissue sarcoma: complication of osteochondroma resection. Int J Clin Oncol 2001;6: 105e8. T oth C, Olvaszt o S, Dinya T. Rare case of popliteal artery injury caused by distal femoral exostosis. Case report. Magy Seb 2001;54:115e7. Perez-Burkhardt JL, Gomez Castilla JC. Postraumatic popliteal pseudoaneurysm from femoral osteochondroma: case report and review of the literature. J Vasc Surg 2003;37: 669e71. Taneda Y, Nakamura K, Yano M, et al. Popliteal artery pseudoaneurysm caused by an osteochondroma. Ann Vasc Surg 2004;18:121e3. Bursztyn M, Strcher M, Sanchez JI, et al. Pseudoaneurysm associated with multiple osteochondromatosis. J Pediatr Surg 2005;40:1201e3. Antonio ZP, Alejandro RM, Luis MR, et al. Femur osteochondroma and secondary pseudoaneurysm of the popliteal artery. Arch Orthop Trauma Surg 2006;126:127e30. Orawczyk T, Kuczmik W, Kazibudzki M, et al. Popliteal pseudoaneurysm as a rare complication of a solitary tibial osteochondroma. EJVES Extra 2006;12:21e3. Al-Hadidy AM, Al-Smady MM, Haroun AA, et al. Hereditary multiple exostoses with pseudoaneurysm. Cardiovasc Intervent Radiol 2007;30:537e40. Argin M, Biceroglu S, Arkun R, et al. Solitary osteochondroma causing popliteal pseudoaneurysm that presented as a mass lesion. Diagn Interv Radiol 2007;13:190e2. Davies R, Satti U, Duffield R. Popliteal artery pseudoaneurysm secondary to femoral osteochondroma: a case report and literature review. Ann R Coll Surg Engl 2007;89:8e11. Petratos DV, Bakogiannis KS, Anastasopoulos JN, et al. Popliteal artery pseudoaneurysm secondary to a osteochondroma in children and adolescents: a case report and literature review. J Surg Orthop Adv 2009;18:205e10. Oxenius A, Knirsch W, Kretschmar O, et al. Unclear swelling of the popliteal fossa due to a giant pseudoaneurysm associated with osteochondroma. J Pediatr 2009;154: 147. Thevenin F, Dumaine V, Feydy A, et al. False aneurysm of the femoral artery in multiple exostosis syndrome. J Radiol 2009;90:612e4. Chaouch N, Alimi F, Kortas C, et al. Bilateral popliteal artery complications of multiple hereditary exostosis. Ann Cardiol Angeiol 2011;60:109e12. Belmir H, Azghari A, Mechchat A, et al. Rupture of a popliteal artery pseudo-aneurysm revealing a tibial osteochondroma: case report and review of the literature. J Mal Vasc 2011;36:50e5. Sadeghi-Azandaryani M, Mendl N, Rademacher A, et al. Pseudoaneurysm of the popliteal artery due to osteochondroma of the distal femur. Vasa 2010;39:274e7.
1315.e14 Case reports
48. Pavic P, Vergles D, Sarlija M, et al. Pseudoaneurysm of the popliteal artery in a patient with multiple hereditary exostoses. Ann Vasc Surg 2011;25:268.e1e2. 49. Vanhegan IS, Shehzad KN, Bhatti TS, et al. Acute popliteal pseudoaneurysm rupture secondary to distal femoral osteochondroma in a patient with hereditary multiple exostoses. Ann R Coll Surg Engl 2012;94:134e6. 50. Paul M. Aneurysm of the popliteal artery from perforation by a cancellous exostosis of the femur. J Bone Joint Surg Br 1953;35:270e1.
Annals of Vascular Surgery
51. Ahmed AR, Tan TS, Unni KK, et al. Secondary chondrosarcoma in osteochondroma: report of 107 patients. Clin Orthop Relat Res 2003;411:193e206. 52. Ayerza MA, Abalo E, Aponte-Tinao L, et al. Endoscopic resection of symptomatic osteochondroma of the distal femur. Clin Orthop Relat Res 2007;459: 150e3. 53. Wong KT, Chu WC, Griffith JF, et al. Pseudoaneurysm complicating osteochondromas: symptom relief with embolization. Clin Orthop 2002;404:339e42.
