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n tips & techniquesSection Editor: Steven F. Harwin, MD

Technique to Prepare the Bed for Autologous Bone Grafting in Nonunion SurgeryTakahiro Niikura, MD, PhD; Masahiko Miwa, MD, PhD; Sang Yang Lee, MD, PhD; Keisuke Oe, MD, PhD; Takashi Iwakura, MD, PhD; Yoshitada Sakai, MD, PhD; Akihiro Koh, MD, PhD; Takaaki Koga, MD; Yoshihiro Dogaki, MD; Etsuko Okumachi, MD; Masahiro Kurosaka, MD, PhD

Nonunions and delayed unions are serious com-

plications in fracture manage-ment and are often challeng-ing to treat. Autologous bone grafting is the gold standard for supplementing bone defects and for enhancing bone healing in nonunions and delayed unions.1 In bone grafting, it is necessary to prepare the bed for grafting; however, detailed techniques for

preparing the bed for grafting have not been described, except for Judet and Patel’s decortica-tion technique.2

Judet and Patel’s2 decortica-tion technique is theoretically a useful technique; however, it is technically difficult to reproduce in the same manner as outlined in the original report. Therefore, the current authors use a tech-nique in which they chip the

cortical bone, providing a bed for autologous bone grafting and enabling them to graft autolo-gous bone into the prepared ap-erture of the chipped bone. The authors hypothesized that chip-ping the bone would produce pathways into the bone marrow, allowing bone marrow cells to be mobilized while simultane-ously inducing osteoinductive factors from the bone matrix and further enhancing bone healing.

Materials and MethodsBetween 2003 and 2010,

forty-five nonunion or delayed union fractures in 45 patients were treated with this tech-nique and followed for at least 6 months postoperatively. Mean follow-up was 21.3 months (range, 6-69 months). Thirty-three patients were followed for at least 1 year. Thirty-three men and 12 women, with an average age of 42.6 years (range, 17-82 years), were included. Five clav-icle, 4 ulna, 2 radius, 17 femur, 15 tibia, and 2 fibula fractures were included. Defects were divided according to Weber’s radiological nonunion classifica-tion3: 6 hypertrophic, 7 atrophic,

22 oligotrophic, and 10 defect types. Autologous bone grafting without exchange or the addition of implants was performed in 7 patients. The remaining patients were treated by appropriate frac-ture fixation, including revision of the implants in combination with autologous bone grafting. Mean duration from trauma to nonunion surgery was 13.9 months (range, 4-76 months). Infection found in 6 patients was eradicated before nonunion sur-gery.

surgical techniqueIntraoperatively, the site of

delayed union or nonunion is

Drs Niikura, Miwa, Lee, Oe, Iwakura, Sakai, Koh, Koga, Dogaki, Oku-machi, and Kurosaka are from the Department of Orthopaedic Surgery, Kobe University Graduate School of Medicine, Chuo-ku, Kobe, Japan.

Drs Niikura, Miwa, Lee, Oe, Iwakura, Sakai, Koh, Koga, Dogaki, Oku-machi, and Kurosaka have no relevant financial relationships to disclose.

Correspondence should be addressed to: Takahiro Niikura, MD, PhD, Department of Orthopaedic Surgery, Kobe University Graduate School of Medicine, 7-5-1 Kusunoki-cho, Chuo-ku, Kobe 650-0017, Japan (tniikura@med.kobe-u.ac.jp).

doi: 10.3928/01477447-20120525-03

Abstract: This article describes a technique for preparing the bed for autologous bone grafting in nonunion surgery. The procedure is divided into 2 steps. First, both ends of the frac-ture fragments are chipped into small pieces using an osteo-tome and hammer without peeling off the periosteum, creat-ing pathways into the bone marrow. Second, cancellous bone harvested from the iliac crest is grafted into the aperture cre-ated by the previous bone chipping treatment. The technique is easy to perform and is a promising approach for enhancing bone healing in nonunion and delayed union.

Figure 1: Exposure of the delayed union or nonunion site. Exposure is done without pealing off the periosteum. The size of incision and extent of surgical exposure is minimized as much as pos-sible to preserve the blood supply.

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exposed without peeling off the periosteum (Figure 1). The size of the incision and the extent of surgical exposure is minimized as much as possible to preserve blood supply to the nonunion or delayed union site. Rarely, a larger exposure is needed if the

previously implanted plates and screws need to be removed.

The procedure is divided into 2 steps (Figure 2). First, both ends of the fracture fragments are chipped into small pieces us-ing an osteotome and a hammer, and pathways into the bone mar-

row are produced. Second, can-cellous bone is harvested from the iliac crest and grafted into the aperture created by the pre-vious bone chipping treatment. For the femur, approximately 2 to 3 cm of both fracture ends are chipped into small pieces (Fig-ure 3). The extent of bone chip-ping is adjusted according to the size of the fractured bone.

Intraoperative photographs show a tibial nonunion (Figure 4). In this patient, the removal of previously implanted plates was necessary; therefore, a large sur-gical exposure was created. The implanted plate was removed,

and the medial side of the non-union site, which would be covered by a revised plate, was chipped into small pieces (Fig-ure 4A). Cancellous bone graft-ing to this site was performed, followed by revision plate fixa-tion. The remainder of the non-union site was then chipped into small pieces (Figure 4B), and cancellous bone grafting was performed (Figure 4C). Chip-ping of the nonunion site and cancellous bone grafting were also performed on the posterior side of the plate (Figure 4D).

To obtain optimal results using this technique, the osteo-

Figure 3: For the femur, approximately 2 to 3 cm of both fracture ends are chipped into small pieces.

Figure 4: Intraoperative photographs of a case of tibial nonunion. The yel-low arrow indicates the nonunion site. Previously implanted plates and screws were removed. The medial side of the nonunion site was chipped into small pieces before the revision plate fixation (A). After revision plate fixation, the remaining nonunion site was chipped into small pieces (B). Cancellous bone grafting was performed (C). Cancellous bone grafting was also performed on the posterior side of the plate and under the plate (D).

4B4A

4D4C

Figure 5: A case of nonunion without implantation of an intramedullary nail. The whole bone area, including the opposite side, can be chipped via a small skin incision (A). A case of nonunion implanted with an intramedullary nail is shown. Sufficient access to the nonunion site is available, including the anterior, lateral, and posterior sides, despite the obstruction by the intramedullary nail (B).

5B5A

Figure 2: Diagram showing 2 steps of the procedure. Step 1: Bone chipping. Both ends of the fracture fragments are chipped into small pieces and pathways into the bone marrow are produced using an osteotome and hammer without peeling off the periosteum. Step 2: Autologous bone grafting. Cancellous bone harvested from the iliac crest is grafted into the aperture created by the bone chipping.

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Table

Patient Data

moPatient No./Sex/Age, y

Fracture Site

Weber’s Classification

Initial Treatment Nonunion Surgerya

Time from Trauma to Nonunion

Surgery

Time from Nonunion Surgery

to Bony Uniona Follow-up1/F/56 Femur Atrophic Nail Exchange nailing 7 10 692/M/21 Femur Oligotrophic Nail Exchange nailing 16 10 523/M/67 Clavicle Atrophic Conservative Plate 12 13 524/F/53 Femur Defect Plate Ilizarov 22 7 405/M/28 Ulna Hypertrophic Conservative Plate 4 5 496/M/32 Femur Hypertrophic Nail Exchange nailing 13.5 3 207/M/23 Tibia Atrophic Nail (1) Plate (2) plate 9 19 (8.5) 658/M/57 Tibia Defect External fixator Nail 10 5.5 159/M/17 Clavicle Hypertrophic Conservative Plate 8 3 1210/M/25 Tibia Oligotrophic Nail Exchange nailing 7 3 1311/M/36 Femur Oligotrophic Nail Exchange nailing 18 4 3112/M/22 Tibia Defect Nail Bone graft only 8 4 1413/M/31 Ulna Hypertrophic Conservative Plate 7 4.5 2214/F/64 Tibia Oligotrophic External fixator Plate 5 5 3615/M/39 Femur Oligotrophic Nail Without removing nail,

(1) Plate (2) plate10.5 20 (13) 43

16/M/40 Tibia Oligotrophic Nail (1) Exchange nailing, (2) plate

6 12 (5) 42

17/M/37 Ulna Oligotrophic Plate Plate revision 8 4.5 818/M/61 Tibia Defect Plate Bone graft only 9 3.5 1219/F/73 Femur Oligotrophic Nail Exchange nailing 36 9 2020/F/37 Tibia Oligotrophic Nail Bone graft only 8 8 2121/F/34 Femur Oligotrophic Nail Exchange nailing 8.5 10 2422/M/27 Femur Oligotrophic Nail Exchange nailing 5 5.5 1523/M/32 Femur Oligotrophic Nail Exchange nailing 27 8.5 2224/F/28 Femur Oligotrophic Nail Exchange nailing 6.5 3.5 2125/M/24 Radius Hypertrophic Plate Plate revision 8 2 826/M/24 Ulna Oligotrophic Plate Bone graft only 8 6 827/M/30 Femur Hypertrophic Nail Locking screw exchange 40.5 4 1428/M/58 Tibia Oligotrophic Nail Plate 30.5 4 2029/M/58 Femur Oligotrophic Nail Plate 32 10 1830/M/30 Fibula Defect Conservative Plate 76 3 1831/M/57 Tibia Defect Nail Exchange nailing 13 5 1632/M/37 Femur Defect Nail Bone graft only 6 8 1133/M/35 Femur Defect Nail Bone graft only 25 4 734/F/76 Tibia Atrophic Plate Ilizarov 7 10 1635/M/19 Clavicle Oligotrophic K-wire Plate 8 3.5 1236/F/41 Clavicle Oligotrophic Plate Plate revision 4 9 1337/M/32 Fibula Oligotrophic Conservative Plate 5 5 1238/F/82 Tibia Atrophic Ilizarov Plate 5.5 4 1239/M/60 Femur Defect Nail Exchange nailing 13 9 1040/F/76 Radius Atrophic Conservative Plate 5 6 941/M/34 Tibia Defect Plate Plate revision 19 4 842/F/62 Clavicle Oligotrophic Plate Plate revision 12 3 643/M/30 Femur Oligotrophic Nail Plate 15 4 844/M/45 Tibia Oligotrophic Plate Bone graft only 6 3 745/M/65 Tibia Atrophic Nail Plate 14 4 7aTime from nonunion surgery to bony union: When a second number appears in parenthesis, it refers to the time from second nonunion surgery to bony union, in the 3 patients requiring revision surgeries. Patients 7, 14, 24, 28, 43, and 45 experienced infection.

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tome should be inserted into the bone parallel to the bone axis but not parallel to the fracture line. Bleeding from the bone marrow should be identified, and care should be taken not to let the small bone fragments complete-ly detach. The existing fibrous

tissue in the fracture gap should not be curetted but should be chipped.

In addition, a nonunion can be implanted with an intramed-ullary nail. The whole bone area, including the opposite side, can be chipped via a small

skin incision (Figure 5A). In contrast, accessing the opposite side of the surgical exposure from the same incision is dif-ficult due to obstruction of the intramedullary nail. However, sufficient access is available to the nonunion site, including the

anterior, lateral, and posterior sides, despite the obstruction by the intramedullary nail (Figure 5B).

resultsPatient details are summa-

rized in the Table. Bony union was successfully obtained in all patients. Of the 45 patients with nonunion or delayed union, 42 obtained bony union unevent-fully in single operations and the remaining 3 required sec-ond operations. The reasons for second operations included: bi-ologically impaired bone activ-ity due to a previous infection in patient 7 (atrophic nonunion of the tibia), insufficient fixa-tion in patient 15 (oligotrophic nonunion of the femur), and insufficient fixation, diabetes mellitus, and a heavy smoking habit in patient 16 (oligotrophic nonunion of the tibia). Mean duration from surgery to bony union was 5.7 months (range, 2-13 months) in the 42 patients undergoing single operations. Complications, such as infec-tion and major donor site mor-bidity, were not detected in any patient.

The authors used this tech-nique mainly to treat cases of femoral and tibial nonunion. Five cases are presented.

case reports Patient 23

Exchange nailing and au-tologous bone grafting was per-formed for femoral nonunion, and bony union was achieved (Figure 6).

Patient 24In a femoral nonunion, infec-

tion was eradicated by removal

Figure 9: Anteroposterior radiographs of patient 16 showing tibial nonunion in which previous exchange nailing was unsuccessful (A), conversion to a locking plate and autologous bone grafting using the current technique (B), and bony union (C).

9B9A 9C

Figure 6: Anteroposterior radiographs of patient 23 showing femoral nonunion (A), exchange nailing and au-tologous bone grafting using the current technique (B), and bony union (C).

6B6A 6CFigure 7: Anteroposterior radiographs of patient 24 showing femoral nonunion with infection (A), revision of intramed-ullary nail, and autologous bone grafting using the current technique (B), and bony union (C).

7B7A 7C

Figure 8: Anteroposterior radiographs of patient 27 showing femoral nonunion (A), revision of distal locking screws and autologous bone grafting using the current technique (B), and bony union (C).

8B8A 8C

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of the intramedullary nail, anti-biotic-loaded cement implanta-tion, and external fixation. Revi-sion of the intramedullary nail and autologous bone grafting was performed, and bony union was achieved (Figure 7).

Patient 27 Revision of distal locking

screws and autologous bone grafting was performed for fem-oral nonunion, and bony union was achieved (Figure 8).

Patient 16Previous exchange nailing

was unsuccessful. Conversion to a locking plate and autologous bone grafting was performed for tibial nonunion, and bony union was achieved (Figure 9).

Patient 44 Plate fixation was not re-

vised. Autologous bone graft-ing was performed for tibial nonunion, and bony union was achieved (Figure 10).

discussionAlthough

new technolo-gy to enhance bone healing has been ap-plied to some cases of non-union, such as osteogenic p r o t e i n - 1 , which is also known as bone morphogenet-ic protein-7,4,5 a u t o l o g o u s bone grafting is still a use-ful and fre-quently used tool.6-8 The

best results may be achieved by adding autologous bone grafting because it is osteogenic, osteo-inductive, and osteoconductive.1

Matsushita and Watanabe9 used a similar technique they called a chipping and length-ening technique for treating delayed unions and nonunions with shortening or bone loss in combination with a lengthening technique using external fixators in the absence of autologous bone grafting. The current tech-nique is different in that the au-thors not only chip the bone, but also add autologous bone graft-ing to further enhance the bone healing capacity. In addition, the current technique was used in patients originally treated with various intramedullary nails, plates, and external fixators.

The current technique dif-fers from Judet and Patel’s2 de-cortication technique because decortication only chips off the surface of the bone whereas the current technique chips the

entire area of bone. Bone heal-ing capacity is inherent in this technique because stem or pro-genitor cells with osteogenic ca-pacity will be introduced from the bone marrow, and osteo-inductive factors such as bone morphogenic proteins will be introduced from the bone ma-trix into the fracture site. Bone morphogenic proteins exist in the extracellular matrix of the bone and bind to the collagen network,10 and they are expect-ed to be released from the extra-cellular matrix and participate in the healing process as a result of chipping the cortical bone.

Moreover, in the current technique the authors did not curette fibrous tissue at the frac-ture gap due to results from their previous research revealing that human nonunion tissue contains osteogenic or chondrogenic pro-genitor cells.11 In these patients, the reservation of intercalary fibrous tissue is helpful in re-ducing the amount of harvested bone to graft.

The best indication for using this technique lies in the suc-cessful treatment of nonunion patients, especially those with oligotrophic and atrophic non-union, which are considered bi-ologically less active. From the authors’ clinical experience, the strengths of this technique are the good nonunion healing rate and the absence of complica-tions. The limitation of the study is the lack of a control group with which to compare results.

This technique provides a simple method for preparing the bed for autologous bone grafting and is a promising approach for enhancing bone healing in non-union and delayed union.

references 1. Sen MK, Miclau T. Autologous

iliac crest bone graft: should it still be the gold standard for treat-ing nonunions? Injury. 2007; 38(suppl 1):S75-S80.

2. Judet PR, Patel A. Muscle pedicle bone grafting of long bones by osteoperiosteal decortication. Clin Orthop Relat Res. 1972; 87:74-80.

3. Frölke JP, Patka P. Definition and classification of fracture non-unions. Injury. 2007; 38(suppl 2):S19-S22.

4. Friedlaender GE, Perry CR, Cole JD, et al. Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial non-unions. J Bone Joint Surg Am. 2001; 83(suppl 1):S151-S158.

5. Dohin B, Dahan-Oliel N, Fassier F, Hamdy R. Enhancement of dif-ficult nonunion in children with osteogenic protein-1 (OP-1): ear-ly experience. Clin Orthop Relat Res. 2009; 467:3230-3238.

6. Lin CL, Fang CK, Chiu FY, Chen CM, Chen TH. Revision with dynamic compression plate and cancellous bone graft for aseptic nonunion after surgical treatment of humeral shaft fracture. J Trau-ma. 2009; 67:1393-1396.

7. Chen CM, Su YP, Hung SH, Lin CL, Chiu FY. Dynamic compres-sion plate and cancellous bone graft for aseptic nonunion after intramedullary nailing of femo-ral fracture. Orthopedics. 2010; 33:393.

8. Sun SG, Zhang Y, Zheng LH, Li J, Fan DG, Ma BA. Applica-tion of locking plate in long-bone atrophic nonunion following external fixation. Orthopedics. 2011; 34:358.

9. Matsushita T, Watanabe Y. Chip-ping and lengthening technique for delayed unions and nonunions with shortening or bone loss. J Orthop Trauma. 2007; 21:404-406.

10. Reddi AH. Morphogenetic mes-sages are in the extracellular ma-trix: biotechnology from bench to bedside. Biochem Soc Trans. 2000; 28:345-349.

11. Iwakura T, Miwa M, Sakai Y, et al. Human hypertrophic non-union tissue contains mesenchy-mal progenitor cells with mul-tilineage capacity in vitro. J Orthop Res. 2009; 27:208-215.

Figure 10: Anteroposterior radiographs of patient 44 showing tibial nonunion (A), autologous bone grafting using the current technique without plate revision (B), and bony union (C).

10B10A 10C