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
persistent nonunion of the clavicle. We describe 3
cases in which a free vascularized corticoperiosteal
flap was harvested from the medial aspect of the femo-
ral condyle and transferred to the fractured clavicle by
use of microvascular anastomoses. Healing was con-
firmed by tomography in all 3 patients. The function of
the upper extremity was remarkably improved at final
follow-up. Vascularized free corticoperiosteal bone
flaps are an option in clavicle fracture treatment. The
technique of periosteal grafting is ideally suited to
chronic nonunions with poor chances of healing on
their own. Rapid subperiosteal new bone and im-
proved local blood flow serve to correct many of those
changes attributed to necrosis of bone. (J Shoulder
Elbow Surg 2005;14:264-268.)
C lavicular fractures associated with radiation ther-
apy are not infrequent events. The chances of healing
under these circumstances are low, and the clinical
outcome therefore is unsatisfactory. Surgical recon-
struction in this anatomic area is challenging because
of the difficulty of obtaining good fixation and be-
cause of the limited soft-tissue mantle over the clavicle,
which does not allow any bulky tissue transfer. In
addition, in patients in whom several attempts at
surgical fixation have failed, potentially complicated
by infection, it can be difficult to achieve final fracture
healing.
We describe the use of a free vascularized corti-
coperiosteal bone graft, harvested from the medial
femoral condyle, for these difficult problems.
From the Department of Orthopedic Surgery, Mayo Clinic.
Reprint requests: Allen T. Bishop, MD, Professor and Chair, Divi-
sion of Hand Surgery, Department of Orthopedic Surgery, Mayo
Clinic, 200 First St SW, Rochester, MN 55905. (E-mail:
bishop.allen@mayo.edu)
Copyright © 2005 by Journal of Shoulder and Elbow Surgery
Board of Trustees.
1058-2746/2005/$30.00
doi:10.1016/j.jse.2004.06.007
264
MATERIALS AND METHODS
Operative cases
Two patients with radiation-induced pathologic clavicle
fractures were treated with free vascularized corticoperios-
teal bone flaps. One patient was a 36-year-old woman who
was treated for dermatofibrosarcoma protuberans overly-
ing the left anterior shoulder and clavicle. The other patient
was a 55-year-old man with a metastatic squamous cell
carcinoma to the left neck. Both were treated by surgical
excision of the tumor and subsequent radiation therapy. The
dose received by the first patient is not known, but the
second patient received 66 Gy to the left neck area. Spon-
taneous pathologic clavicle fractures occurred 30 and 9
months afterward, respectively, and remained ununited for
12 and 9 months, respectively, until the flap procedure was
performed. Preoperatively, both patients complained of
limited and disabling shoulder motion, as well as rest and
activity-related pain. Imaging studies and surgical inspec-
tion both revealed atrophic nonunion and avascular changes
of the clavicle. Both patients had a corticoperiosteal bone
graft. Healing was confirmed by tomography at 5 and 7
months, respectively (Figure 1).
A third patient, a 32-year-old man, had a clavicle frac-
ture malunion fixed with an iliac crest graft and plating. It
became infected, and the plate was removed 4 months
later. Two months after debridement and antibiotic treat-
ment, the clavicle was replated. Five months later, the
nonunion persisted, and the hardware fixation had failed.
A third attempt at fixation of the fracture was attempted 8
months later with the use of a vascularized corticoperiosteal
bone flap. At 3 months postoperatively, the fracture had
healed clinically and radiographically. There were no in-
traoperative or postoperative complications. No donor-site
morbidity in either case other than transient medial knee
pain was seen. The function of the upper extremity was
restored to normal at final follow-up 2 years after the
procedure.
Operative technique
At the recipient site, the clavicle is first reduced and
stabilized with a low contact dynamic compression plate
(LC-DCP) (stainless steel), and the thoracoacromial trunk
arising from the subclavian vessels is identified and dis-
sected. The technique of harvesting the free vascularized
thin corticoperiosteal bone graft from the medial condylar
and supracondylar region has previously been de-
scribed.6,7,12,18,21,22 We use the ipsilateral medial femo-
ral condyle as the preferred donor. A medial incision is
made overlying the distal medial femur along the posterior
border of the vastus medialis. The investing fascia of the
J Shoulder Elbow Surg
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-
orly. The descending genicular vessels are then easily visu-
alized on the floor of the muscle compartment proximally
and on the surface of the medial femoral condyle distally.
The superomedial genicular vessels also contribute to the
condylar blood supply and are identified at the metaphy-
seal level. The latter vessels are ligated if the descending
genicular vessels are large enough to be used for microa-
nastomosis. A large and easily visible network of anasto-
motic vessels derived from the genicular blood supply cov-
ers the medial surface of the distal femoral metaphysis.
Once this distribution of genicular vessels is fully exposed,
the graft is outlined on the supracondylar periosteum to
include the blood supply. It extends approximately 8 cm in
length from the metaphyseal-diaphyseal junction proximally
to the medial collateral ligament origin distally. Its width
(typically measuring 6 cm) is limited by the posterior border
of the femur and medial patellar facet anteriorly. Flap
elevation is, in fact, performed without violating the joint
capsule, as follows. With the graft margins identified, the
periosteum is progressively elevated with a curved os-
teotome. Elevation of the graft proceeds from the margins
toward the center, by gentle advancement of the osteotome
a few millimeters at a time and then prying of the graft from
underlying cancellous bone. Dissection in this fashion pre-
serves the cambium layer and results in a thin flap that
includes the periosteum and connected fragments of cortical
bone. Next, the vascular pedicle of the graft is dissected
proximally to its origin from the superficial femoral vessels
in Hunter’s canal and divided (Figure 2). Because the
harvested graft is thin and pliable, it can be wrapped
around the clavicle and secured with heavy nonabsorbable
suture. Microvascular anastomoses are performed to the
thoracoacromial trunk vessels. Vessel patency and a bleed-
ing flap surface confirm a successful transfer (Figure 3). The
flap circulation may be continuously monitored postopera-
tively with an implanted Cook-Swartz probe (Cook Vascu-
lar, Leechburg, PA). A bone scan performed in the first week
after surgery confirms graft viability. Postoperatively, a
shoulder immobilizer is used for 6 to 8 weeks. Passive
Fuchs, Steinmann, and Bishop 265
range of motion is then initiated. Immediate full weight-
bearing is allowed on the donor leg as tolerated. Use of a
cane in the opposite hand until donor site pain subsides is
helpful, generally for 2 to 3 weeks. For this reason, the
ipsilateral leg is chosen as the donor site.
DISCUSSION
Functional compromise, including avascular necro-
sis to the clavicle, can result from radiation treatment
of tumors of the shoulder girdle.4,15,30 Radiation-
induced necrosis of the clavicle has a particularly
unfavorable prognosis.19,24,29 Partial excision of the
clavicle, often advocated in this situation, may result
in persisting pain, weakness, sensation of instability,
and brachial plexopathy.1-3,13,17,25,31,33 Because of
the thin soft-tissue envelope covering the clavicle,
bulky bone and/or soft-tissue reconstruction is prefer-
entially avoided. Several methods of surgical recon-
struction have been described. Although Dacron
(Deknatel, Falls River, MA) graft reconstruction has
been described, it has been associated with compli-
cations such as stress fracture9 or erosion of the first
rib.20 A Marlex (C.R. Bard Inc., Billerica, MA) mesh–
enveloped composite graft consisting of a hydroxyap-
atite prosthesis and autogenous bone has been pro-
posed, although secure fixation of this construct
remains a challenge.23 In cases involving failed prior
plating or infection, conventional nonvascularized il-
iac tricortical bone graft may not be used successfully,
especially if a significant defect remains in the clavi-
cle. Microvascular fibular transfer combined with au-
tografting has been reported as an appropriate treat-
ment option for difficult nonunions associated with
previously irradiated long bones8; however, a high
failure rate for the clavicular site has been
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-
ing the serratus anterior and/or latissimus dorsi.5,10
Because of its osteogenic capability, vascularized
periosteal grafts have considerable potential for the
reconstruction of bone defects.14,27,28 Several sites of
periosteal elevation have been described, including
the fibula, radius, scapula, iliac crest, and medial
supracondylar region.16,18,26,34 The use of perios-
teum from the medial supracondylar region of the
femur was extensively analyzed by Masquelet and
coworkers12,18,21 and then popularized by Doi et
al.6,7 It was shown experimentally that the associa-
tion of a vascularized periosteal flap and cancellous
bone is a better means by which to produce compact
bone than either a vascularized periosteal flap alone
or an isolated cancellous bone graft.12,18,21 In an ani-
mal model, a vascularized periosteal flap wrapped
around a cancellous bone graft resulted in new cortical
bone formation with little resorption of the initial cancel-
lous graft.21 Among the advantages of this graft is the
possibility of including not only bone but skin and mus-
cle, depending on the reconstructive need.18
The transfer of free vascularized corticoperiosteal
bone flaps seems to be ideally suited for post-radia-
tion–induced fractures or chronic nonunions of the
clavicle without substantial bone loss but with poor
chances of healing on their own. The flap is thin and
can be shaped according to the reconstructive re-
quirements without compromising its blood supply. It
can be wrapped around the clavicle without visible
bulk, thereby avoiding further stress on the previously
irradiated overlying skin. It enables clavicular healing
at one bone contact site, avoiding the difficulties of
interposing, fixing, and healing a bridging vascular-
ized structural graft. Rapid subperiosteal new bone
and improved local blood flow both serve to correct
many of those changes attributed to radiation necro-
sis of bone. Although microvascular expertise is nec-
essary, flap exposure and elevation are straightfor-
ward. The thoracoacromial trunk artery and vein as
268 Fuchs, Steinmann, and Bishop
well as the descending genicular vessels are con-
stantly present and are of sufficient size for reliable
microsurgical anastomoses. No long-term morbidity
was encountered at the donor site in any of our
patients.
REFERENCES
1. Adolfsson L, Lysholm J, Nettelblad H. Adverse effects of extensive
clavicular resections and a suggested method of reconstruction.
J Shoulder Elbow Surg 1999;8:361-4.
2. Boyer MI, Axelrod TS. Atrophic nonunion of the clavicle: treat-
ment by compression plate, lag-screw fixation and bone graft.
J Bone Joint Surg Br 1997;79:301-3.
3. Craig E. Fractures of the clavicle. In: Rockwood JA Jr, Matsen FA
III. The shoulder. Philadelphia: Saunders; 1990. p. 367-412.
4. Damron TA, Sim FH, Shives TC, et al. Intercalary spacers in the
treatment of segmentally destructive diaphyseal humeral lesions in
disseminated malignancies. Clin Orthop 1996;324:233-43.
5. Devaraj VS, Kay SP, Batchelor AG. Vascularised reconstruction of
the clavicle. Br J Plast Surg 1990;43:625-7.
6. Doi K, Oda T, Soo-Heong T, Nanda V. Free vascularized bone
graft for nonunion of the scaphoid. J Hand Surg [Am] 2000;25:
507-19.
7. Doi K, Sakai K. Vascularized periosteal bone graft from the
supracondylar region of the femur. Microsurgery 1994;15: 305-
15.
8. Duffy GP, Wood MB, Rock MG, Sim FH. Vascularized free
fibular transfer combined with autografting for the management of
fracture nonunions associated with radiation therapy. J Bone Joint
Surg Am 2000;82:544-54.
9. Dust WN, Lenczner EM. Stress fracture of the clavicle leading to
nonunion secondary to coracoclavicular reconstruction with Da-
cron. Am J Sports Med 1989;17:128-9.
10. Guelinckx PJ, Sinsel NK. The “Eve” procedure: the transfer of
vascularized seventh rib, fascia, cartilage, and serratus muscle to
reconstruct difficult defects. Plast Reconstr Surg 1996; 97:527-
35.
11. Han CS, Wood MB, Bishop AT, Cooney WP III. Vascularized
bone transfer. J Bone Joint Surg Am 1992;74:1441-9.
12. Hertel R, Masquelet AC. The reverse flow medial knee osteope-
riosteal flap for skeletal reconstruction of the leg. Description and
anatomical basis. Surg Radiol Anat 1989;11:257-62.
13. Jupiter JB, Leffert RD. Non-union of the clavicle. Associated com-
plications and surgical management. J Bone Joint Surg Am 1987;
69:753-60.
14. King KF. Periosteal pedicle grafting in dogs. J Bone Joint Surg Br
1976;58:117-21.
15. Markbreiter LA, Pelker RR, Friedlaender GE, Peschel R, Panjabi
MM. The effect of radiation on the fracture repair process. A
biomechanical evaluation of a closed fracture in a rat model.
J Orthop Res 1989;7:178-83.
J Shoulder Elbow Surg
May/June 2005
16. Milanov NO, Trofimov EI, Umerenkov AG. Treatment of long
tubular bone pseudoarthrosis with revascularized cortical layer of
radius. [in Russian]. Vestn Ross Akad Med Nauk 1997;9:38-42.
17. Neer C. Nonunion of the clavicle. JAMA 1960;172:1006-11.
18. Penteado CV, Masquelet AC, Romana MC, Chevrel JP. Perios-
teal flaps: anatomical bases of sites of elevation. Surg Radiol
Anat 1990;12:3-7.
19. Pillon P, Troussier B, Martin A, et al. Osteoradionecrosis of the
clavicle after treatment of cancer of the upper respiratory and
digestive tract. [in French]. Rev Rhum Mal Osteoartic 1990; 57:
341-5.
20. Reilly P, Bruguera JA, Copeland SA. Erosion and nonunion of the
first rib after sternoclavicular reconstruction with Dacron. J Shoul-
der Elbow Surg 1999;8:76-8.
21. Romana MC, Masquelet AC. Vascularized periosteum associ-
ated with cancellous bone graft: an experimental study. Plast
Reconstr Surg 1990;85:587-92.
22. Sakai K, Doi K, Kawai S. Free vascularized thin corticoperiosteal
graft. Plast Reconstr Surg 1991;87:290-8.
23. Shinjo K. Reconstruction of a segmental clavicular defect with a
Marlex mesh-enveloped composite graft consisting of a hydroxy-
apatite prosthesis and autogenous bone: a case report. Jpn J Clin
Oncol 1992;22:221-4.
24. Skinner WL, Buzdar AU, Libshitz HI. Massive osteolysis of the
right clavicle developing after radiation therapy. JAMA 1988;
260:375-6.
25. Spar I. Total claviculectomy for pathological fractures. Clin Or-
thop 1977;129:236-7.
26. Stock W, Hierner R, Dielert E, et al. The iliac crest region: donor
site for vascularized bone periosteal and soft tissue flaps. Ann
Plast Surg 1991;26:105-9.
27. Stock W, Hierner R, Wolf K. Vascularized periosteal transplant.
A review of a new therapeutic possibility. [in German]. Handchir
Mikrochir Plast Chir 1991;23:149-56
28. Takato T, Harii K, Nakatsuka T, Ueda K, Ootake T. Vascularized
periosteal grafts: an experimental study using two different forms
of tibial periosteum in rabbits. Plast Reconstr Surg 1986; 78:489-
97.
29. Wang EH, Sekyi-Otu A, O’Sullivan B, Bell RS. Management of
long-term postirradiation periclavicular complications. J Surg On-
col 1992;51:259-65.
30. Widmann RF, Pelker RR, Friedlaender GE, Panjabi MM, Peschel
RE. Effects of prefracture irradiation on the biomechanical param-
eters of fracture healing. J Orthop Res 1993;11:422-8.
31. Wilkins RM, Johnston RM. Ununited fractures of the clavicle.
J Bone Joint Surg Am 1983;65:773-8.
32. Wood MB. Upper extremity reconstruction by vascularized bone
transfers: results and complications. J Hand Surg [Am] 1987;
12:422-7.
33. Wood VE. The results of total claviculectomy. Clin Orthop 1986;
207:186-90.
34. Yajima H, Tamai S, Ono H, Kizaki K. Vascularized bone grafts
to the upper extremities. Plast Reconstr Surg 1998;101:727-37.