Free vascularized corticoperiosteal bone graft for the

treatment of persistent nonunion of the clavicle

Bruno Fuchs, MD, Scott P. Steinmann, MD, and Allen T. Bishop, MD, Rochester, MN

Radiation-induced necrosis or infection can result in a MATERIALS AND METHODS

persistent nonunion of the clavicle. We describe 3 Operative cases
cases in which a free vascularized corticoperiosteal
Two patients with radiation-induced pathologic clavicle
flap was harvested from the medial aspect of the femo- fractures were treated with free vascularized corticoperios-
ral condyle and transferred to the fractured clavicle by teal bone flaps. One patient was a 36-year-old woman who
use of microvascular anastomoses. Healing was con- was treated for dermatofibrosarcoma protuberans overly-
ing the left anterior shoulder and clavicle. The other patient
firmed by tomography in all 3 patients. The function of
was a 55-year-old man with a metastatic squamous cell
the upper extremity was remarkably improved at final carcinoma to the left neck. Both were treated by surgical
follow-up. Vascularized free corticoperiosteal bone excision of the tumor and subsequent radiation therapy. The
flaps are an option in clavicle fracture treatment. The dose received by the first patient is not known, but the
second patient received 66 Gy to the left neck area. Spon-
technique of periosteal grafting is ideally suited to
taneous pathologic clavicle fractures occurred 30 and 9
chronic nonunions with poor chances of healing on months afterward, respectively, and remained ununited for
their own. Rapid subperiosteal new bone and im- 12 and 9 months, respectively, until the flap procedure was
proved local blood flow serve to correct many of those performed. Preoperatively, both patients complained of
limited and disabling shoulder motion, as well as rest and
changes attributed to necrosis of bone. (J Shoulder
activity-related pain. Imaging studies and surgical inspec-
Elbow Surg 2005;14:264-268.) tion both revealed atrophic nonunion and avascular changes
of the clavicle. Both patients had a corticoperiosteal bone
C lavicular fractures associated with radiation ther- graft. Healing was confirmed by tomography at 5 and 7
months, respectively (Figure 1).
apy are not infrequent events. The chances of healing
A third patient, a 32-year-old man, had a clavicle frac-
under these circumstances are low, and the clinical
ture malunion fixed with an iliac crest graft and plating. It
outcome therefore is unsatisfactory. Surgical recon- became infected, and the plate was removed 4 months
struction in this anatomic area is challenging because later. Two months after debridement and antibiotic treat-
of the difficulty of obtaining good fixation and be- ment, the clavicle was replated. Five months later, the
cause of the limited soft-tissue mantle over the clavicle, nonunion persisted, and the hardware fixation had failed.
which does not allow any bulky tissue transfer. In A third attempt at fixation of the fracture was attempted 8
addition, in patients in whom several attempts at months later with the use of a vascularized corticoperiosteal
bone flap. At 3 months postoperatively, the fracture had
surgical fixation have failed, potentially complicated healed clinically and radiographically. There were no in-
by infection, it can be difficult to achieve final fracture traoperative or postoperative complications. No donor-site
healing. morbidity in either case other than transient medial knee
We describe the use of a free vascularized corti- pain was seen. The function of the upper extremity was
coperiosteal bone graft, harvested from the medial restored to normal at final follow-up 2 years after the
femoral condyle, for these difficult problems. procedure.

Operative technique
At the recipient site, the clavicle is first reduced and
stabilized with a low contact dynamic compression plate
From the Department of Orthopedic Surgery, Mayo Clinic. (LC-DCP) (stainless steel), and the thoracoacromial trunk
Reprint requests: Allen T. Bishop, MD, Professor and Chair, Divi- arising from the subclavian vessels is identified and dis-
sion of Hand Surgery, Department of Orthopedic Surgery, Mayo sected. The technique of harvesting the free vascularized
Clinic, 200 First St SW, Rochester, MN 55905. (E-mail: thin corticoperiosteal bone graft from the medial condylar
[email protected]) and supracondylar region has previously been de-
Copyright © 2005 by Journal of Shoulder and Elbow Surgery scribed.6,7,12,18,21,22 We use the ipsilateral medial femo-
Board of Trustees. ral condyle as the preferred donor. A medial incision is
1058-2746/2005/$30.00 made overlying the distal medial femur along the posterior
doi:10.1016/j.jse.2004.06.007 border of the vastus medialis. The investing fascia of the

264
J Shoulder Elbow Surg Fuchs, Steinmann, and Bishop 265
Volume 14, Number 3

Figure 1 Preoperative and postoperative radiographs. A, A 36-year-old woman in whom an atrophic painful
nonunion of the left clavicle developed with compromised soft-tissue quality subsequent to surgical excision and
radiation treatment of a dermatofibrosarcoma protuberans overlying the clavicle. B, Two years postoperatively, the
radiograph confirms healing of the bone.

vastus medialis is incised and the muscle retracted anteri- range of motion is then initiated. Immediate full weight-
orly. The descending genicular vessels are then easily visu- bearing is allowed on the donor leg as tolerated. Use of a
alized on the floor of the muscle compartment proximally cane in the opposite hand until donor site pain subsides is
and on the surface of the medial femoral condyle distally. helpful, generally for 2 to 3 weeks. For this reason, the
The superomedial genicular vessels also contribute to the ipsilateral leg is chosen as the donor site.
condylar blood supply and are identified at the metaphy-
seal level. The latter vessels are ligated if the descending DISCUSSION
genicular vessels are large enough to be used for microa-
nastomosis. A large and easily visible network of anasto- Functional compromise, including avascular necro-
motic vessels derived from the genicular blood supply cov- sis to the clavicle, can result from radiation treatment
ers the medial surface of the distal femoral metaphysis. of tumors of the shoulder girdle.4,15,30 Radiation-
Once this distribution of genicular vessels is fully exposed, induced necrosis of the clavicle has a particularly
the graft is outlined on the supracondylar periosteum to
include the blood supply. It extends approximately 8 cm in
unfavorable prognosis.19,24,29 Partial excision of the
length from the metaphyseal-diaphyseal junction proximally clavicle, often advocated in this situation, may result
to the medial collateral ligament origin distally. Its width in persisting pain, weakness, sensation of instability,
(typically measuring 6 cm) is limited by the posterior border and brachial plexopathy.1-3,13,17,25,31,33 Because of
of the femur and medial patellar facet anteriorly. Flap the thin soft-tissue envelope covering the clavicle,
elevation is, in fact, performed without violating the joint bulky bone and/or soft-tissue reconstruction is prefer-
capsule, as follows. With the graft margins identified, the entially avoided. Several methods of surgical recon-
periosteum is progressively elevated with a curved os- struction have been described. Although Dacron
teotome. Elevation of the graft proceeds from the margins (Deknatel, Falls River, MA) graft reconstruction has
toward the center, by gentle advancement of the osteotome
been described, it has been associated with compli-
a few millimeters at a time and then prying of the graft from
underlying cancellous bone. Dissection in this fashion pre- cations such as stress fracture9 or erosion of the first
serves the cambium layer and results in a thin flap that rib.20 A Marlex (C.R. Bard Inc., Billerica, MA) mesh–
includes the periosteum and connected fragments of cortical enveloped composite graft consisting of a hydroxyap-
bone. Next, the vascular pedicle of the graft is dissected atite prosthesis and autogenous bone has been pro-
proximally to its origin from the superficial femoral vessels posed, although secure fixation of this construct
in Hunter’s canal and divided (Figure 2). Because the remains a challenge.23 In cases involving failed prior
harvested graft is thin and pliable, it can be wrapped plating or infection, conventional nonvascularized il-
around the clavicle and secured with heavy nonabsorbable iac tricortical bone graft may not be used successfully,
suture. Microvascular anastomoses are performed to the especially if a significant defect remains in the clavi-
thoracoacromial trunk vessels. Vessel patency and a bleed-
cle. Microvascular fibular transfer combined with au-
ing flap surface confirm a successful transfer (Figure 3). The
flap circulation may be continuously monitored postopera- tografting has been reported as an appropriate treat-
tively with an implanted Cook-Swartz probe (Cook Vascu- ment option for difficult nonunions associated with
lar, Leechburg, PA). A bone scan performed in the first week previously irradiated long bones8; however, a high
after surgery confirms graft viability. Postoperatively, a failure rate for the clavicular site has been
shoulder immobilizer is used for 6 to 8 weeks. Passive shown.11,32 Other biologic options include the vas-
266 Fuchs, Steinmann, and Bishop J Shoulder Elbow Surg
May/June 2005

Figure 2 Harvesting of periosteal graft at donor site. A, A medially based incision posterior to the vastus medialis
muscle is made. B, Schematic overview of anatomic structures at the medial distal femur with outlining of the graft.
C, Intraoperative exposure of the medial distal femur showing descending genicular artery, adductor magnus
tendon, superior genicular artery, and medial collateral ligament. D, The superomedial genicular artery is ligated
and the graft prepared for harvesting. E, The corticoperiosteal graft is elevated carefully with a curved osteotome.
F, After the corticoperiosteal graft is elevated, the vessels are ligated before its transfer.
J Shoulder Elbow Surg Fuchs, Steinmann, and Bishop 267
Volume 14, Number 3

Figure 3 Periosteal graft and recipient site. A, The size of the graft is tailored according to the clavicular defect.
The nutrient vessels measure 7 cm. B, The clavicle is anatomically reduced and fixed with a plate. The bracket
shows the defect. C, Schematic overview of how the graft is wrapped around the clavicle. D, Intraoperative view
shows the microvascular anastomoses between the periosteal graft and the thoracoacromial trunk.

cularized transfer of a rib as a composite flap includ- possibility of including not only bone but skin and mus-
ing the serratus anterior and/or latissimus dorsi.5,10 cle, depending on the reconstructive need.18
Because of its osteogenic capability, vascularized The transfer of free vascularized corticoperiosteal
periosteal grafts have considerable potential for the bone flaps seems to be ideally suited for post-radia-
reconstruction of bone defects.14,27,28 Several sites of tion–induced fractures or chronic nonunions of the
periosteal elevation have been described, including clavicle without substantial bone loss but with poor
the fibula, radius, scapula, iliac crest, and medial chances of healing on their own. The flap is thin and
supracondylar region.16,18,26,34 The use of perios- can be shaped according to the reconstructive re-
teum from the medial supracondylar region of the quirements without compromising its blood supply. It
femur was extensively analyzed by Masquelet and can be wrapped around the clavicle without visible
coworkers12,18,21 and then popularized by Doi et bulk, thereby avoiding further stress on the previously
al.6,7 It was shown experimentally that the associa- irradiated overlying skin. It enables clavicular healing
tion of a vascularized periosteal flap and cancellous at one bone contact site, avoiding the difficulties of
bone is a better means by which to produce compact interposing, fixing, and healing a bridging vascular-
bone than either a vascularized periosteal flap alone ized structural graft. Rapid subperiosteal new bone
or an isolated cancellous bone graft.12,18,21 In an ani- and improved local blood flow both serve to correct
mal model, a vascularized periosteal flap wrapped many of those changes attributed to radiation necro-
around a cancellous bone graft resulted in new cortical sis of bone. Although microvascular expertise is nec-
bone formation with little resorption of the initial cancel- essary, flap exposure and elevation are straightfor-
lous graft.21 Among the advantages of this graft is the ward. The thoracoacromial trunk artery and vein as
268 Fuchs, Steinmann, and Bishop J Shoulder Elbow Surg
May/June 2005

well as the descending genicular vessels are con- 16. Milanov NO, Trofimov EI, Umerenkov AG. Treatment of long
stantly present and are of sufficient size for reliable tubular bone pseudoarthrosis with revascularized cortical layer of
radius. [in Russian]. Vestn Ross Akad Med Nauk 1997;9:38-42.
microsurgical anastomoses. No long-term morbidity 17. Neer C. Nonunion of the clavicle. JAMA 1960;172:1006-11.
was encountered at the donor site in any of our 18. Penteado CV, Masquelet AC, Romana MC, Chevrel JP. Perios-
patients. teal flaps: anatomical bases of sites of elevation. Surg Radiol
Anat 1990;12:3-7.
REFERENCES 19. Pillon P, Troussier B, Martin A, et al. Osteoradionecrosis of the
clavicle after treatment of cancer of the upper respiratory and
1. Adolfsson L, Lysholm J, Nettelblad H. Adverse effects of extensive digestive tract. [in French]. Rev Rhum Mal Osteoartic 1990; 57:
clavicular resections and a suggested method of reconstruction. 341-5.
J Shoulder Elbow Surg 1999;8:361-4. 20. Reilly P, Bruguera JA, Copeland SA. Erosion and nonunion of the
2. Boyer MI, Axelrod TS. Atrophic nonunion of the clavicle: treat- first rib after sternoclavicular reconstruction with Dacron. J Shoul-
ment by compression plate, lag-screw fixation and bone graft. der Elbow Surg 1999;8:76-8.
J Bone Joint Surg Br 1997;79:301-3. 21. Romana MC, Masquelet AC. Vascularized periosteum associ-
3. Craig E. Fractures of the clavicle. In: Rockwood JA Jr, Matsen FA ated with cancellous bone graft: an experimental study. Plast
III. The shoulder. Philadelphia: Saunders; 1990. p. 367-412. Reconstr Surg 1990;85:587-92.
4. Damron TA, Sim FH, Shives TC, et al. Intercalary spacers in the 22. Sakai K, Doi K, Kawai S. Free vascularized thin corticoperiosteal
treatment of segmentally destructive diaphyseal humeral lesions in graft. Plast Reconstr Surg 1991;87:290-8.
disseminated malignancies. Clin Orthop 1996;324:233-43. 23. Shinjo K. Reconstruction of a segmental clavicular defect with a
5. Devaraj VS, Kay SP, Batchelor AG. Vascularised reconstruction of Marlex mesh-enveloped composite graft consisting of a hydroxy-
the clavicle. Br J Plast Surg 1990;43:625-7. apatite prosthesis and autogenous bone: a case report. Jpn J Clin
6. Doi K, Oda T, Soo-Heong T, Nanda V. Free vascularized bone Oncol 1992;22:221-4.
graft for nonunion of the scaphoid. J Hand Surg [Am] 2000;25: 24. Skinner WL, Buzdar AU, Libshitz HI. Massive osteolysis of the
507-19. right clavicle developing after radiation therapy. JAMA 1988;
7. Doi K, Sakai K. Vascularized periosteal bone graft from the 260:375-6.
supracondylar region of the femur. Microsurgery 1994;15: 305- 25. Spar I. Total claviculectomy for pathological fractures. Clin Or-
15. thop 1977;129:236-7.
8. Duffy GP, Wood MB, Rock MG, Sim FH. Vascularized free 26. Stock W, Hierner R, Dielert E, et al. The iliac crest region: donor
fibular transfer combined with autografting for the management of site for vascularized bone periosteal and soft tissue flaps. Ann
fracture nonunions associated with radiation therapy. J Bone Joint Plast Surg 1991;26:105-9.
Surg Am 2000;82:544-54. 27. Stock W, Hierner R, Wolf K. Vascularized periosteal transplant.
9. Dust WN, Lenczner EM. Stress fracture of the clavicle leading to A review of a new therapeutic possibility. [in German]. Handchir
nonunion secondary to coracoclavicular reconstruction with Da- Mikrochir Plast Chir 1991;23:149-56
cron. Am J Sports Med 1989;17:128-9. 28. Takato T, Harii K, Nakatsuka T, Ueda K, Ootake T. Vascularized
10. Guelinckx PJ, Sinsel NK. The “Eve” procedure: the transfer of periosteal grafts: an experimental study using two different forms
vascularized seventh rib, fascia, cartilage, and serratus muscle to of tibial periosteum in rabbits. Plast Reconstr Surg 1986; 78:489-
reconstruct difficult defects. Plast Reconstr Surg 1996; 97:527- 97.
35. 29. Wang EH, Sekyi-Otu A, O’Sullivan B, Bell RS. Management of
11. Han CS, Wood MB, Bishop AT, Cooney WP III. Vascularized long-term postirradiation periclavicular complications. J Surg On-
bone transfer. J Bone Joint Surg Am 1992;74:1441-9. col 1992;51:259-65.
12. Hertel R, Masquelet AC. The reverse flow medial knee osteope- 30. Widmann RF, Pelker RR, Friedlaender GE, Panjabi MM, Peschel
riosteal flap for skeletal reconstruction of the leg. Description and RE. Effects of prefracture irradiation on the biomechanical param-
anatomical basis. Surg Radiol Anat 1989;11:257-62. eters of fracture healing. J Orthop Res 1993;11:422-8.
13. Jupiter JB, Leffert RD. Non-union of the clavicle. Associated com- 31. Wilkins RM, Johnston RM. Ununited fractures of the clavicle.
plications and surgical management. J Bone Joint Surg Am 1987; J Bone Joint Surg Am 1983;65:773-8.
69:753-60. 32. Wood MB. Upper extremity reconstruction by vascularized bone
14. King KF. Periosteal pedicle grafting in dogs. J Bone Joint Surg Br transfers: results and complications. J Hand Surg [Am] 1987;
1976;58:117-21. 12:422-7.
15. Markbreiter LA, Pelker RR, Friedlaender GE, Peschel R, Panjabi 33. Wood VE. The results of total claviculectomy. Clin Orthop 1986;
MM. The effect of radiation on the fracture repair process. A 207:186-90.
biomechanical evaluation of a closed fracture in a rat model. 34. Yajima H, Tamai S, Ono H, Kizaki K. Vascularized bone grafts
J Orthop Res 1989;7:178-83. to the upper extremities. Plast Reconstr Surg 1998;101:727-37.