JBJS | Distraction Osteogenesis After Acute Limb-Shortening for Segmental Tibial Defects : Comparison of a Monofocal and a Bifocal Technique in Rabbits*

The Journal of Bone & Joint Surgery, Volume 82, Issue 6

Articles | June 01, 2000

Distraction Osteogenesis After Acute Limb-Shortening for Segmental Tibial Defects : Comparison of a Monofocal and a Bifocal Technique in Rabbits*

Rainer H. Meffert, M.D.†; Nozomu Inoue, M.D., PhD.; John E. Tis, M.D.‡; Erwin Brug, M.D.§; Edmund Y. S. Chao, Ph.D.†

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Investigation performed at the Department of Orthopaedic Surgery, Orthopaedic Biomechanics Laboratory, The Johns Hopkins University, Baltimore, Maryland
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding sources were the Max-Kade Foundation, New York, and Orthofix, Limited, Verona, Italy. The external fixators were provided by Orthofix, Limited, Verona, Italy, and the microplates were provided by Howmedica Leibinger, Pfizer Medical Technology Group, Dallas, Texas.
†Department of Orthopaedic Surgery, Orthopaedic Biomechanics Laboratory, The Johns Hopkins University, Ross Research Building, 720 Rutland Avenue, Room 235, Baltimore, Maryland 21205-2196.
‡Orthopaedic Surgery Service, Walter Reed Army Medical Center, Washington, D.C. 20307.
§Department of Trauma and Hand Surgery, University of Münster, Waldeyerstrasse 1, D-48129 Münster, Germany.

The Journal of Bone & Joint Surgery. 2000; 82:799-799

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Abstract

Background: Segmental bone defects can be treated with immediate limb-shortening followed by monofocal or bifocal distraction osteogenesis. In the present study, the efficacy of monofocal distraction osteogenesis was compared with that of bifocal distraction osteogenesis in a rabbit model.

Methods: Twenty-four skeletally mature New Zealand White rabbits were divided into two equal groups: one group had monofocal distraction osteosynthesis, and the other had bifocal distraction osteosynthesis. In both groups, a one-centimeter-long segment of bone was resected from the midpart of the tibial shaft. In the monofocal reconstruction group, the limb was immediately shortened to close the segmental defect and the defect was allowed to heal for ten days. Lengthening was then begun at this site, with use of a specially designed external fixator, at a rate of 0.5 millimeter per twelve hours. In the bifocal reconstruction group, the segmental defect was closed immediately and the fragments were fixed with microplates. A subperiosteal osteotomy was performed proximal to the tibiofibular junction, and lengthening was performed at the site of the osteotomy. The animals in both groups were killed twenty days after the lengthening was completed. New-bone formation then was evaluated with use of radiographs, densitometry, biomechanical testing, and histological and histomorphometric analysis.

Results: Osseous consolidation occurred in all but one of the animals. Biomechanical testing demonstrated that the tibiae that had been treated with use of the simple monofocal reconstruction technique tended to have greater torsional stiffness (p = 0.14) and strength (p = 0.09). Follow-up radiographs revealed that both groups had a significant decrease in radiolucent area (p < 0.05), which occurred at essentially the same rate after lengthening. No significant differences were found between the groups with respect to new-bone mineral density, new-bone area, or the amount of callus. Thus, after resection of a diaphyseal bone segment comprising 10 percent of the original length of the tibia and acute shortening, limb reconstruction was completed successfully through distraction osteogenesis with use of either a monofocal or a bifocal technique in rabbits.

Conclusions: In the present study, both monofocal and bifocal techniques of shortening and distraction osteogenesis were effective for the reconstruction of segmental bone defects. Under some conditions, the monofocal method may provide a simpler means of treating such defects.

Clinical Relevance: Damage to the soft-tissue envelope as well as venous and lymphatic stasis impose limits on the amount of limb-shortening that can be achieved with use of the monofocal method and also influence the indications for this procedure in the clinical setting.

Figures in this Article

Introduction

Introduction | Materials and Methods | Results | Discussion | References

High-velocity trauma may lead to open fractures with soft-tissue damage and bone loss, particularly in the lower limb. Adequate dè¡²idement of soft tissue and bone, combined with a minimally invasive fixation technique, is the key to improving local perfusion, reducing the rate of infection, and promoting bone-healing after severe trauma^{1,16,33,43,44}. In addition, early local or free tissue transfer to cover bone defects and to enhance local perfusion has been shown to improve the clinical outcome^{6,9,12,23,26,32,45}. Immediate limb-shortening after dè¡²idement, performed to close bone defects and to gain viable soft tissue for bone coverage, may be an alternative in selected situations^4,13,26,31. Distraction osteogenesis can also be employed to restore bone length by segmental bone transport or bifocal shortening and lengthening^{3,5,7,8,10,14,15,17-22,27,36-39,42,45}. In primary limb-shortening procedures, a secondary osteotomy for lengthening is usually performed in the proximal metaphyseal region^8,13. Little is known about the possibility of stretching soft callus from the primary shortening site, which would eliminate the need for additional operations and would reduce tissue devascularization. The main concerns are the unpredictable posttraumatic vascularity of the local tissue, the amount and quality of periosteal callus, and the venous and lymphatic stasis distal to the shortening site. Previous case reports have indicated that monofocal shortening-lengthening procedures are in fact currently being carried out in patients^31,41. In the study by Möllenhoff et al., the mean latency time - that is, the delay before distraction osteogenesis was started - was prolonged in order to improve vascularity and to allow wound consolidation³¹.

The key terms used in the present article are defined as follows. A monofocal procedure involves osteogenesis at one level, and a bifocal procedure involves osteogenesis at two levels. The speed of a step or process is characterized as either acute or gradual, and the timing is characterized as either simultaneous or sequential. The procedures and processes include distraction, compression, translation, rotation, and angulation. Lastly, the objectives of treatment include osteosynthesis, lengthening, and correction.

The purpose of this study was to evaluate and compare the outcome of monofocal sequential acute compression shortening gradual distraction osteosynthesis with that of bifocal sequential acute compression shortening gradual distraction osteosynthesis in an animal model.

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TABLE I: Densitometric Measurements After Monofocal and Bifocal Limb Reconsruction

*The terms proximal and distal refer to the proximal and distal portions of the regenerated bone area adjacent to the cortex.†The values are expressed as the ratio of the bone-mineral content of the proximal cortical fragment to that of the distal cortical fragment.‡P = 0.86 compared with the distal region after monofocal reconstruction, and p = 0.77 compared with the proximal region after bifocal reconstruction.§P = 0.15 compared with bifocal reconstruction.#P = 0.67 compared with the distal region after bifocal reconstruction.

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Bone-Mineral Content in New-Bone Area (g/cm²)		Bone-Mineral Content in Diaphyseal Cortex†	Specimen	Bone-Mineral Content in New-Bone Area (g/cm²)		Bone-Mineral Content in Diaphyseal Cortex†
Proximal*	Distal*	Proximal*	Distal*
1	0.44	0.56	1.05	1	0.55	0.45	1.19
2	0.67	0.64	0.99	2	0.59	0.58	0.90
3	0.60	0.66	0.97	3	0.92	0.89	1.00
4	0.35	0.33	1.15	4	0.43	0.47	0.96
5	0.62	0.51	1.14	5	0.56	0.44	1.13
6	0.47	0.45	0.98	6	0.54	0.48	1.07
7	0.60	0.65	0.98	7	0.39	0.45	0.97
8	0.58	0.53	0.96	8	0.25	0.31	0.89
9	0.60	0.66	0.99	9	0.67	0.71	0.91
10	0.44	0.41	1.29	10	0.69	0.67	0.96
11	0.43	0.40	1.06	11	0.33	0.35	0.80
12	0.32	0.36	1.13	12	0.42	0.45	1.11
Mean and standard deviation	0.51 ± 0.11‡	0.51 ± 0.12	1.06 ± 0.10§	Mean and standard deviation	0.53 ± 0.18#	0.52 ± 0.16	0.99 ± 0.11

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TABLE I: Densitometric Measurements After Monofocal and Bifocal Limb Reconsruction

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Bone-Mineral Content in New-Bone Area (g/cm²)		Bone-Mineral Content in Diaphyseal Cortex†	Specimen	Bone-Mineral Content in New-Bone Area (g/cm²)		Bone-Mineral Content in Diaphyseal Cortex†
Proximal*	Distal*	Proximal*	Distal*
1	0.44	0.56	1.05	1	0.55	0.45	1.19
2	0.67	0.64	0.99	2	0.59	0.58	0.90
3	0.60	0.66	0.97	3	0.92	0.89	1.00
4	0.35	0.33	1.15	4	0.43	0.47	0.96
5	0.62	0.51	1.14	5	0.56	0.44	1.13
6	0.47	0.45	0.98	6	0.54	0.48	1.07
7	0.60	0.65	0.98	7	0.39	0.45	0.97
8	0.58	0.53	0.96	8	0.25	0.31	0.89
9	0.60	0.66	0.99	9	0.67	0.71	0.91
10	0.44	0.41	1.29	10	0.69	0.67	0.96
11	0.43	0.40	1.06	11	0.33	0.35	0.80
12	0.32	0.36	1.13	12	0.42	0.45	1.11
Mean and standard deviation	0.51 ± 0.11‡	0.51 ± 0.12	1.06 ± 0.10§	Mean and standard deviation	0.53 ± 0.18#	0.52 ± 0.16	0.99 ± 0.11

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TABLE II: Torsional Stiffness After Monofocal and Bifocal Limb Reconstruction

*P < 0.01 compared with the contralateral side, and p = 0.14 compared with bifocal reconstruction.P = 0.32 compared with bifocal reconstruction.P < 0.001 compared with the contralateral side.

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Stiffness on Experimental Side (Nmm/degree)	Stiffness on Contralateral Side (Nmm/degree)	Stiffness on Experimental Side/ Stiffness on Contralateral Side (percent)	Specimen	Stiffness on Experimental Side (Nmm/degree)	Stiffness on Contralateral Side (Nmm/degree)	Stiffness on Experimental Side/ Stiffness on Contralateral Side (percent)
1	187	259	72	1	196	250	78
2	250	310	81	2	231	268	86
3	340	420	81	3	206	375	55
4	151	272	56	4	230	307	75
5	209	283	74	5	180	308	58
6	183	305	60	6	271	324	84
7	302	435	69	7	154	353	44
8	281	379	74	8	130	394	33
9	242	441	55	9	241	470	51
10	223	267	84	10	172	233	74
Mean and standard deviation	237 ± 59*	337 ± 74	71 ± 10	Mean and standard deviation	201 ± 35	328 ± 56	64 ± 16

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TABLE II: Torsional Stiffness After Monofocal and Bifocal Limb Reconstruction

*P < 0.01 compared with the contralateral side, and p = 0.14 compared with bifocal reconstruction.P = 0.32 compared with bifocal reconstruction.P < 0.001 compared with the contralateral side.

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Stiffness on Experimental Side (Nmm/degree)	Stiffness on Contralateral Side (Nmm/degree)	Stiffness on Experimental Side/ Stiffness on Contralateral Side (percent)	Specimen	Stiffness on Experimental Side (Nmm/degree)	Stiffness on Contralateral Side (Nmm/degree)	Stiffness on Experimental Side/ Stiffness on Contralateral Side (percent)
1	187	259	72	1	196	250	78
2	250	310	81	2	231	268	86
3	340	420	81	3	206	375	55
4	151	272	56	4	230	307	75
5	209	283	74	5	180	308	58
6	183	305	60	6	271	324	84
7	302	435	69	7	154	353	44
8	281	379	74	8	130	394	33
9	242	441	55	9	241	470	51
10	223	267	84	10	172	233	74
Mean and standard deviation	237 ± 59*	337 ± 74	71 ± 10	Mean and standard deviation	201 ± 35	328 ± 56	64 ± 16

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TABLE III: Torsional Strength After Monofocal and Bifocal Limb Reconstruction

*P < 0.0001 compared with the contralateral side, and p = 0.09 compared with the experimental side after bifocal reconstruction.†P = 0.09 compared with bifocal reconstruction.‡P < 0.0001 compared with the contralateral side.

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Strength on Experimental Side (Nmm/degree)	Strength on Contralateral Side (Nmm/degree)	Strength on Experimental Side/Strength on Contralateral Side (percent)	Specimen	Strength on Experimental Side (Nmm/degree)	Strength on Contralateral Side (Nmm/degree)	Strength on Experimental Side/Strength on Contralateral Side (percent)
1	1155	2845	41	1	1314	2922	45
2	1874	3111	60	2	1775	3025	59
3	2760	2708	102	3	1048	3056	34
4	1385	2519	55	4	1872	3086	61
5	1771	2802	63	5	1806	2512	72
6	1410	2674	53	6	2216	3108	71
7	2267	3601	63	7	1386	2850	47
8	1893	3383	56	8	849	3431	25
9	1847	2574	72	9	1183	3052	39
10	2202	2860	77	10	1565	2636	59
Mean and standard deviation	1856 ± 475*	2908 ± 353	64 ± 71†	Mean and standard deviation	1501 ± 345‡	2968 ± 190	51 ± 13

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TABLE III: Torsional Strength After Monofocal and Bifocal Limb Reconstruction

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Strength on Experimental Side (Nmm/degree)	Strength on Contralateral Side (Nmm/degree)	Strength on Experimental Side/Strength on Contralateral Side (percent)	Specimen	Strength on Experimental Side (Nmm/degree)	Strength on Contralateral Side (Nmm/degree)	Strength on Experimental Side/Strength on Contralateral Side (percent)
1	1155	2845	41	1	1314	2922	45
2	1874	3111	60	2	1775	3025	59
3	2760	2708	102	3	1048	3056	34
4	1385	2519	55	4	1872	3086	61
5	1771	2802	63	5	1806	2512	72
6	1410	2674	53	6	2216	3108	71
7	2267	3601	63	7	1386	2850	47
8	1893	3383	56	8	849	3431	25
9	1847	2574	72	9	1183	3052	39
10	2202	2860	77	10	1565	2636	59
Mean and standard deviation	1856 ± 475*	2908 ± 353	64 ± 71†	Mean and standard deviation	1501 ± 345‡	2968 ± 190	51 ± 13

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TABLE IV: New-Bone Area After Monofocal and Bifocal Limb Reconsruction*

*The values are given as the percentage of new bone in regenerated tissue, as measured on histological analysis of decalcified specimens.†The values are given as the new-bone area in the regions adjacent to the cortex.‡The values are given as the mean new-bone area in the neocortex.§P = 0.91 compared with the distal region after monofocal reconstruction.#P = 0.41 compared with bifocal reconstruction.**P = 0.97 compared with the distal region after bifocal reconstruction.

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Proximal†	Distal†	Mean†	Specimen	Proximal†	Distal†	Mean†
1	48	52	53	1	49	63	52
2	71	67	61	2	58	47	50
3	56	36	43	3	33	25	39
4	54	59	54	4	46	46	46
5	71	55	66	5	52	56	58
6	48	49	52	6	49	48	50
7	60	65	59	7	72	70	70
8	52	69	59	8	58	56	58
9	69	70	67	9	60	53	51
10	48	47	57	10	48	62	55
11	45	56	51	11	-	-	-
12	48	41	47	12	-	-	-
Mean and standard deviation	56 ± 10§	55 ± 10	56 ± 7#	Mean and standard deviation	53 ± 10**	53 ± 12	54 ± 8

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TABLE IV: New-Bone Area After Monofocal and Bifocal Limb Reconsruction*

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Proximal†	Distal†	Mean†	Specimen	Proximal†	Distal†	Mean†
1	48	52	53	1	49	63	52
2	71	67	61	2	58	47	50
3	56	36	43	3	33	25	39
4	54	59	54	4	46	46	46
5	71	55	66	5	52	56	58
6	48	49	52	6	49	48	50
7	60	65	59	7	72	70	70
8	52	69	59	8	58	56	58
9	69	70	67	9	60	53	51
10	48	47	57	10	48	62	55
11	45	56	51	11	-	-	-
12	48	41	47	12	-	-	-
Mean and standard deviation	56 ± 10§	55 ± 10	56 ± 7#	Mean and standard deviation	53 ± 10**	53 ± 12	54 ± 8

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Fig. 1-A:: Schematic drawing of the monofocal resection and lengthening model. During a single operation, an external fixator was applied, a diaphyseal bone segment was resected, and the limb was immediately shortened. After a latency period of ten days, distraction osteogenesis was begun.

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Fig. 1-B:: Schematic drawing of the bifocal resection and lengthening model. After resection and shortening, the fragments were united by internal fixation with use of two titanium microplates and a proximal osteotomy was carried out. Distraction osteogenesis was begun at the proximal osteotomy site after a ten-day latency period.

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Fig. 2-A:: High-resolution radiographs, made forty days postoperatively in the anteroposterior plane, showing the involved tibia and the contralateral, untreated tibia from animals treated with monofocal reconstruction (Fig. 2-A) and bifocal reconstruction (Fig. 2-B). Full length, anatomical alignment and complete osseous bridging were achieved after both procedures.

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Fig. 2-B::

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Fig. 3:: Schematic drawing of tibiae treated with monofocal (left) and bifocal (right) limb reconstruction, illustrating the embedding technique in which thirty-two millimeters of reconstructed tibia is exposed between squares of Wood's metal for torsion-testing. In the bifocal reconstruction group, the microplates remained attached to the shortening site.

Materials and Methods

Introduction | Materials and Methods | Results | Discussion | References

Twenty-four skeletally mature New Zealand White rabbits (Covance Research, Denver, Pennsylvania) that weighed between 3.5 and 4.0 kilograms were randomly separated into two groups of twelve animals each in order to compare two different operative techniques of limb reconstruction after acute shortening. In both groups, a one-centimeter-long segment of bone (approximately 10 percent of the total length of the tibia), including the periosteum, was excised from the tibial diaphysis. The periosteum of the tibia in the osteotomy zone was preserved. In the monofocal reconstruction group (treated with monofocal sequential acute compression after shortening followed by gradual distraction osteosynthesis), the limb was shortened until there was contact between the proximal and the distal fragment. Lengthening at this site was begun ten days later (Fig. 1-A). In the bifocal reconstruction group (treated with bifocal sequential acute compression after shortening followed by gradual distraction osteosynthesis), the segment of bone was resected, the limb was shortened, and the fragments were fixed with use of unicortical screws and microplates. A subperiosteal proximal osteotomy was performed simultaneously. Lengthening at this site was begun ten days later (Fig. 1-B). In both groups, full load-bearing and unrestricted motion were allowed immediately after the operation. After the ten-day latency period, a gradual distraction of 0.5 millimeter per twelve hours was performed with use of an external fixation device until full limb length was achieved. All animals were killed with an overdose of ketamine and inhalation of carbon dioxide twenty days after the lengthening was completed. The protocol was approved by the institutional animal-care committee.

Operative Procedure

With use of general anesthesia and under sterile conditions, the skin was incised longitudinally over the medial aspect of the tibial diaphysis. A unilateral external fixator-distractor (M-103; Orthofix, Verona, Italy) was applied to the anteromedial aspect of one tibia. The side of the procedure (left or right) was alternated in consecutive animals. A one-centimeter segment of bone was removed from the midpart of the tibial shaft with use of a reciprocating saw under irrigation with saline solution. Primary limb-shortening and approximation of the bone fragments closed the bone gap. Soft-tissue interposition between the fragments was avoided. In the bifocal reconstruction group, compression osteosynthesis was achieved with use of two titanium three-hole microplates and one-by-four-millimeter unicortical titanium screws (Howmedica Leibinger, Pfizer Medical Technology Group, Dallas, Texas). For lengthening, a subperiosteal osteotomy was carried out proximal to the tibiofibular junction. In both groups, the bone was completely covered by a tension-free adaptation of local muscle and fascia, which were shifted onto the medial surface of the tibia in order to maximize contact between bone and soft tissue in the resection area. The detached periosteum of the tibia was not readapted or repaired on either side of the osteotomy site. A tension-free skin closure was then performed.

Measurement of Compartment Pressure

In both groups, the intramuscular pressure in the anterior tibial compartment was measured on the involved side and on the contralateral (control) side before and after limb-shortening. The purpose of such measurements was to ensure normal muscle perfusion after acute limb-shortening. Follow-up measurements were made, with the rabbits under general anesthesia, at eight and twenty-four hours after the operation. A piezoelectric transducer (KODIAG; Braun-Dexon GmbH, Spangenberg, Germany) on a 1.4-millimeter-diameter test tube was placed directly into the anterior tibial compartment. In contrast to other techniques, no fluid injection into the muscle compartment was required. The catheter tube was placed into the proximal third of the anterior tibial compartment through a skin incision made two centimeters distal to the muscle origin. The insertion depth ranged from 1.5 to 2.0 millimeters.

Radiographic Analysis

Radiographs (Kodak Diagnostic Films Min-R M, MRM-I; Eastman Kodak, Rochester, New York) were made in two planes before and after the operation, after the latency and lengthening periods, and at weekly intervals thereafter. Immediately after the lengthening was completed and at one and two weeks thereafter, the central (unmineralized) callus area was measured directly on radiographs with use of an image-analyzer software package (Bioquant System IV; R and M Biometrics, Nashville, Tennessee). The results were then expressed as the percentage of the total callus area. The maximum diameter of the callus was measured on the high-resolution radiographs with use of digital calipers, and the values from the two planes were averaged and normalized to the shaft diameter.

Densitometry

A radiograph of each tibia was made, in the anteroposterior plane, with use of a high-resolution film (Konica Powermatic Premium RAP-4; Walker Supply, Rockville, Maryland) that was exposed at seventy kilovolts and three milliamperes for thirty seconds in a self-contained x-ray cabinet (Faxitron x-Ray, Buffalo Grove, Illinois) (Fig. 2-A and Fig. 2-B). The images on the film were captured and digitized with a high-resolution charge-coupled device (CCD) camera (DXC-151; Sony, Tokyo, Japan). Digitized data from the images were transferred to a workstation (Iris Indigo Elan; Silicon Graphics, Mountain View, California) and were measured in fifteen defined anatomical areas with use of a custom software program. The gray level of each pixel was corrected with use of a correction equation calculated from a nonlinear gray level-aluminum step relationship²⁸. High-resolution radiographs showing different concentrations of hydroxyapatite were used to construct a linear standard curve depicting the relationship between radiographic density and hydroxyapatite concentration. Bone-mineral density was calculated with use of the density of hydroxyapatite as a reference. The bone-mineral density was measured in the cortical and endosteal regions close to the osteotomy line as well as in the distal, middle, and proximal parts of the distracted new-bone area. The densities measured in the medial and lateral regions were averaged.

Biomechanical Testing

The distal and proximal aspects of the tibia were embedded into a metal alloy (Wood's Metal; Cerrometal Products, Bellefonte, Pennsylvania) in order to expose exactly thirty-two millimeters of the diaphysis, including the area of new-bone formation, for mechanical torsion-testing. In the bifocal reconstruction group, the shortening site with the attached microplates was included in the exposed area as well. This procedure reproduced not only the mechanical stability of the lengthened bone but also that of the reconstructed portion of the limb (Fig. 3). Specimens were deep-frozen at -18 degrees Celsius once before testing²⁵. Torsion tests were performed with use of a servohydraulic universal testing machine (Bionix 858; MTS Systems, Eden Prairie, Minnesota) by applying a nonphysiological slow load in external rotation at 10 degrees per minute until failure²⁹. The slope of the initial linear portion of the curve was measured as an index of torsional stiffness. Ultimate strength was defined as the maximum torque applied during testing.

Histological and Histomorphometric Analysis

After mechanical testing was performed, a three-centimeter-long specimen from each tibia, containing the new bone and the shortening site, was cut longitudinally in the sagittal plane with a diamond saw (Buehler Isomed, Lake Bluff, Illinois). One side was decalcified for histological and histomorphometric analysis, and the other side was embedded in methylmethacrylate (Technovit 9100; Heraeus Kulzer GmbH, Wehrheim, Germany) without decalcification for undecalcified histological analysis. Specimens for decalcification were fixed in 10 percent formalin and decalcified completely with formic acid and sodium citrate. After the decalcified specimens had been embedded in paraffin and stained with hematoxylin and eosin, five-micrometer sections were cut for histological and histomorphometric analysis. One randomly selected specimen from each group was not used for mechanical testing and was fixed in formalin without freezing for histological analysis. Bone area was measured on hematoxylin and eosin-stained slides of decalcified specimens, at 100 times magnification, with use of an image-analyzer software package (Bioquant System IV; R and M Biometrics) in five defined anatomical areas.

Statistical Analysis

All values were expressed as the mean and the standard deviation. An unpaired t test was used for comparisons between the two groups. A paired t test was used to compare the proximal and distal regions with regard to bone density and bone area as well as to compare the experimental and contralateral sides with regard to torsional strength and stiffness. Analysis of variance with the Tukey post hoc t test was used to evaluate time-sequential changes in muscle compartment pressure and radiographic parameters.

Results

Introduction | Materials and Methods | Results | Discussion | References

One animal in each group was replaced because of a fracture through a fixator pin-hole during the postoperative period. In the bifocal reconstruction group, one animal with unstable fixation at the shortening site was excluded because a nonunion had developed at the lengthening site. In the twenty-three animals that had stable fixation, osseous union with straight alignment was attained. In the monofocal reconstruction group, one specimen fractured due to a technical error before mechanical testing was completed. No animal had pin-loosening, infection, or soft-tissue-related problems.

Muscle Compartment Pressure

The pressure in the anterior tibial compartment was evaluated for all twelve animals in each group before, immediately after, and at eight and twenty-four hours after the limb-shortening. No significant difference between the groups was found at any time point. In addition, no significant difference was detected between the involved side and the contralateral side in either group.

Radiographic Analysis

New callus eventually filled the lengthening site in all of the animals. Follow-up radiographs revealed a significant reduction in the radiolucent area in both groups immediately after lengthening and after one and two weeks of callus maturation (p < 0.05). The percentage of uncalcified callus in the monofocal reconstruction group was not significantly different from that in the bifocal reconstruction group after lengthening (39.3 ± 11.5 compared with 40.4 ± 15.8; p = 0.31), at one week (8.9 ± 4.6 compared with 10.3 ± 7.7; p = 0.39), or at two weeks (0.7 ± 1.3 compared with 0.8 ± 2.6; p = 0.86).

The mean maximum diameter of the callus was the same in both groups (11.6 ± 1.8 millimeters in the monofocal reconstruction group and 11.6 ± 1.5 millimeters in the bifocal reconstruction group; p = 0.91). Normalized callus diameter to the shaft diameter, however, revealed a significantly larger value after monofocal reconstruction than after bifocal reconstruction (1.6 ± 0.16 compared with 1.3 ± 0.15; p = 0.0003).

Densitometry (Table I)

No significant differences between proximal and distal callus density were found within or between the groups. In the bifocal reconstruction group, cortical bone density in the isolated fragment tended to be higher than that in the proximal fragment, but the differences were not found to be significant (p = 0.15).

Biomechanical Testing (Tables II and III)

Torsional stiffness and maximum torsional strength were somewhat greater after monofocal reconstruction than after bifocal reconstruction, but these differences were not found to be significant (p = 0.14 and p = 0.09, respectively). In both groups, stiffness and strength were significantly lower on the experimental side than on the contralateral side (p < 0.01 and p < 0.0001, respectively, for the monofocal reconstruction group, and p < 0.001 and p < 0.0001, respectively, for the bifocal reconstruction group).

Histological and Histomorphometric Analysis (Table IV)

All of the specimens were evaluated histologically, and twenty-two of twenty-three specimens were evaluated histomorphometrically. Cancellous bone without cartilage or fibrous tissue formed in the lengthening site after both types of reconstruction. The greatest amounts of new-bone formation were found between the proximal and distal cortical fragments in association with the formation of new cortices. New bone constituted a mean of 56 percent of the neocortex area in the monofocal reconstruction group and a mean of 54 percent in the bifocal reconstruction group (p = 0.41).

Discussion

Introduction | Materials and Methods | Results | Discussion | References

The osteoinductive microenvironment for the generation of new bone with use of the Ilizarov technique depends on the availability and activation of bone progenitor cells, the local vascularity, and the mechanical environment^11,20. Mesenchymal progenitor cells derived from bone marrow, periosteum, and connective tissue of muscle are capable of differentiating into bone³⁵. Therefore, a viable and well perfused soft-tissue envelope in the area of distraction osteogenesis is important for the creation of sufficient amounts of new bone. The success or failure of monofocal distraction osteogenesis in a clinical setting therefore is directly related to the characteristics and quality of this soft-tissue envelope.

The value of the periosteum in distraction osteogenesis has been demonstrated in studies of immature rabbits²⁴. In skeletally mature rabbits, the periosteum is a thin membrane that cannot be stripped from the bone surface and readily reapproximated, as is the case in growing animals. This is an important consideration in the construction of trauma models involving segmental bone resection. Therefore, mature animals were chosen for this model. As a result, it was possible to create an environment in which sufficient amounts of new bone were generated by means of distraction with use of both the monofocal and the bifocal technique.

Both the rate and the timing of distraction have been shown to affect callus formation in experimental studies involving rabbits^46,48. A distraction rate of between 0.35 and 0.70 millimeter per twelve hours, applied after a latency period of seven to ten days and following a careful subperiosteal osteotomy, has been shown to generate adequate callus^46,48. Since all of the tibiae in the present study were subjected to increased trauma rather than a simple osteotomy for limb-lengthening, a long latency period was used to allow vascularization. Clinical experience has also supported the need for a prolonged latency period³¹.

A recent study involving a muscle-trauma model in rabbits demonstrated that, when the total tibial length was shortened by 10 percent, elevated compartment pressure decreased and bone and soft-tissue perfusion improved substantially³⁰. These findings support the concept of immediate posttraumatic shortening within certain limits³¹. Venous and lymphatic stasis and vascular kinking leading to secondary swelling after limb-shortening are concerns that clearly impose limits on such a technique. Experimentally, these abnormalities were demonstrated after shortening of 25 and 50 percent of the total tibial length³⁰.

A previous study of bifocal limb reconstruction in rabbits, performed to simulate bone transport, revealed substantially greater bone formation at the proximal end of the lengthening area than at the distal end⁴⁷. The authors of that study suggested that this finding might have been due to avascular necrosis of the bone segment located between the compression site and the distraction site. In the present study, neither necrosis of the isolated bone segment located between the shortening site and the lengthening site nor decreased new-bone formation in the distal aspect of the lengthening site was observed following the use of the bifocal technique. Since the experimental conditions in the two studies were very similar, this finding may have resulted from better bone perfusion associated with the bifocal shortening reconstruction than that associated with segmental bone transport. The proximal osteotomy in the bifocal reconstruction group was performed simultaneously with the resection and shortening in order to compare the results of the two reconstruction procedures after equal durations of treatment. This method, as well as the two-step procedure, has been established clinically¹⁴. Since a prolonged latency period prior to lengthening allows revascularization^46,48, the current model may simulate both techniques. This conclusion is supported by our findings of equal bone-mineral content and equal distribution of new-bone formation proximally and distally.

Because of the technical limitations associated with use of a unilateral frame on the proximal metaphysis of a rabbit tibia, we performed an osteotomy that left a relatively short segment of bone between the compression and distraction sites in the bifocal reconstruction group. A true metaphyseal osteotomy with consecutive distraction osteogenesis and a larger bone segment, as is preferred in clinical use, might have led to a better mechanical outcome and a more advanced stage of remodeling in the bifocal reconstruction group^2,13,34,40. Nonetheless, the results of the present study demonstrate the efficacy of both techniques for regeneration of a segmental bone defect through shortening and distraction osteogenesis.

Note: We thank E. McCarthy, M.D., Department of Pathology, The Johns Hopkins University, for processing the decalcified specimens.

References

Introduction | Materials and Methods | Results | Discussion | References

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TABLE I: Densitometric Measurements After Monofocal and Bifocal Limb Reconsruction

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Bone-Mineral Content in New-Bone Area (g/cm²)		Bone-Mineral Content in Diaphyseal Cortex†	Specimen	Bone-Mineral Content in New-Bone Area (g/cm²)		Bone-Mineral Content in Diaphyseal Cortex†
Proximal*	Distal*	Proximal*	Distal*
1	0.44	0.56	1.05	1	0.55	0.45	1.19
2	0.67	0.64	0.99	2	0.59	0.58	0.90
3	0.60	0.66	0.97	3	0.92	0.89	1.00
4	0.35	0.33	1.15	4	0.43	0.47	0.96
5	0.62	0.51	1.14	5	0.56	0.44	1.13
6	0.47	0.45	0.98	6	0.54	0.48	1.07
7	0.60	0.65	0.98	7	0.39	0.45	0.97
8	0.58	0.53	0.96	8	0.25	0.31	0.89
9	0.60	0.66	0.99	9	0.67	0.71	0.91
10	0.44	0.41	1.29	10	0.69	0.67	0.96
11	0.43	0.40	1.06	11	0.33	0.35	0.80
12	0.32	0.36	1.13	12	0.42	0.45	1.11
Mean and standard deviation	0.51 ± 0.11‡	0.51 ± 0.12	1.06 ± 0.10§	Mean and standard deviation	0.53 ± 0.18#	0.52 ± 0.16	0.99 ± 0.11

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TABLE I: Densitometric Measurements After Monofocal and Bifocal Limb Reconsruction

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Bone-Mineral Content in New-Bone Area (g/cm²)		Bone-Mineral Content in Diaphyseal Cortex†	Specimen	Bone-Mineral Content in New-Bone Area (g/cm²)		Bone-Mineral Content in Diaphyseal Cortex†
Proximal*	Distal*	Proximal*	Distal*
1	0.44	0.56	1.05	1	0.55	0.45	1.19
2	0.67	0.64	0.99	2	0.59	0.58	0.90
3	0.60	0.66	0.97	3	0.92	0.89	1.00
4	0.35	0.33	1.15	4	0.43	0.47	0.96
5	0.62	0.51	1.14	5	0.56	0.44	1.13
6	0.47	0.45	0.98	6	0.54	0.48	1.07
7	0.60	0.65	0.98	7	0.39	0.45	0.97
8	0.58	0.53	0.96	8	0.25	0.31	0.89
9	0.60	0.66	0.99	9	0.67	0.71	0.91
10	0.44	0.41	1.29	10	0.69	0.67	0.96
11	0.43	0.40	1.06	11	0.33	0.35	0.80
12	0.32	0.36	1.13	12	0.42	0.45	1.11
Mean and standard deviation	0.51 ± 0.11‡	0.51 ± 0.12	1.06 ± 0.10§	Mean and standard deviation	0.53 ± 0.18#	0.52 ± 0.16	0.99 ± 0.11

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TABLE II: Torsional Stiffness After Monofocal and Bifocal Limb Reconstruction

*P < 0.01 compared with the contralateral side, and p = 0.14 compared with bifocal reconstruction.P = 0.32 compared with bifocal reconstruction.P < 0.001 compared with the contralateral side.

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Stiffness on Experimental Side (Nmm/degree)	Stiffness on Contralateral Side (Nmm/degree)	Stiffness on Experimental Side/ Stiffness on Contralateral Side (percent)	Specimen	Stiffness on Experimental Side (Nmm/degree)	Stiffness on Contralateral Side (Nmm/degree)	Stiffness on Experimental Side/ Stiffness on Contralateral Side (percent)
1	187	259	72	1	196	250	78
2	250	310	81	2	231	268	86
3	340	420	81	3	206	375	55
4	151	272	56	4	230	307	75
5	209	283	74	5	180	308	58
6	183	305	60	6	271	324	84
7	302	435	69	7	154	353	44
8	281	379	74	8	130	394	33
9	242	441	55	9	241	470	51
10	223	267	84	10	172	233	74
Mean and standard deviation	237 ± 59*	337 ± 74	71 ± 10	Mean and standard deviation	201 ± 35	328 ± 56	64 ± 16

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TABLE II: Torsional Stiffness After Monofocal and Bifocal Limb Reconstruction

*P < 0.01 compared with the contralateral side, and p = 0.14 compared with bifocal reconstruction.P = 0.32 compared with bifocal reconstruction.P < 0.001 compared with the contralateral side.

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Stiffness on Experimental Side (Nmm/degree)	Stiffness on Contralateral Side (Nmm/degree)	Stiffness on Experimental Side/ Stiffness on Contralateral Side (percent)	Specimen	Stiffness on Experimental Side (Nmm/degree)	Stiffness on Contralateral Side (Nmm/degree)	Stiffness on Experimental Side/ Stiffness on Contralateral Side (percent)
1	187	259	72	1	196	250	78
2	250	310	81	2	231	268	86
3	340	420	81	3	206	375	55
4	151	272	56	4	230	307	75
5	209	283	74	5	180	308	58
6	183	305	60	6	271	324	84
7	302	435	69	7	154	353	44
8	281	379	74	8	130	394	33
9	242	441	55	9	241	470	51
10	223	267	84	10	172	233	74
Mean and standard deviation	237 ± 59*	337 ± 74	71 ± 10	Mean and standard deviation	201 ± 35	328 ± 56	64 ± 16

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TABLE III: Torsional Strength After Monofocal and Bifocal Limb Reconstruction

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Strength on Experimental Side (Nmm/degree)	Strength on Contralateral Side (Nmm/degree)	Strength on Experimental Side/Strength on Contralateral Side (percent)	Specimen	Strength on Experimental Side (Nmm/degree)	Strength on Contralateral Side (Nmm/degree)	Strength on Experimental Side/Strength on Contralateral Side (percent)
1	1155	2845	41	1	1314	2922	45
2	1874	3111	60	2	1775	3025	59
3	2760	2708	102	3	1048	3056	34
4	1385	2519	55	4	1872	3086	61
5	1771	2802	63	5	1806	2512	72
6	1410	2674	53	6	2216	3108	71
7	2267	3601	63	7	1386	2850	47
8	1893	3383	56	8	849	3431	25
9	1847	2574	72	9	1183	3052	39
10	2202	2860	77	10	1565	2636	59
Mean and standard deviation	1856 ± 475*	2908 ± 353	64 ± 71†	Mean and standard deviation	1501 ± 345‡	2968 ± 190	51 ± 13

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TABLE III: Torsional Strength After Monofocal and Bifocal Limb Reconstruction

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Strength on Experimental Side (Nmm/degree)	Strength on Contralateral Side (Nmm/degree)	Strength on Experimental Side/Strength on Contralateral Side (percent)	Specimen	Strength on Experimental Side (Nmm/degree)	Strength on Contralateral Side (Nmm/degree)	Strength on Experimental Side/Strength on Contralateral Side (percent)
1	1155	2845	41	1	1314	2922	45
2	1874	3111	60	2	1775	3025	59
3	2760	2708	102	3	1048	3056	34
4	1385	2519	55	4	1872	3086	61
5	1771	2802	63	5	1806	2512	72
6	1410	2674	53	6	2216	3108	71
7	2267	3601	63	7	1386	2850	47
8	1893	3383	56	8	849	3431	25
9	1847	2574	72	9	1183	3052	39
10	2202	2860	77	10	1565	2636	59
Mean and standard deviation	1856 ± 475*	2908 ± 353	64 ± 71†	Mean and standard deviation	1501 ± 345‡	2968 ± 190	51 ± 13

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TABLE IV: New-Bone Area After Monofocal and Bifocal Limb Reconsruction*

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Proximal†	Distal†	Mean†	Specimen	Proximal†	Distal†	Mean†
1	48	52	53	1	49	63	52
2	71	67	61	2	58	47	50
3	56	36	43	3	33	25	39
4	54	59	54	4	46	46	46
5	71	55	66	5	52	56	58
6	48	49	52	6	49	48	50
7	60	65	59	7	72	70	70
8	52	69	59	8	58	56	58
9	69	70	67	9	60	53	51
10	48	47	57	10	48	62	55
11	45	56	51	11	-	-	-
12	48	41	47	12	-	-	-
Mean and standard deviation	56 ± 10§	55 ± 10	56 ± 7#	Mean and standard deviation	53 ± 10**	53 ± 12	54 ± 8

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TABLE IV: New-Bone Area After Monofocal and Bifocal Limb Reconsruction*

Monofocal Reconstruction				Bifocal Reconstruction
Specimen	Proximal†	Distal†	Mean†	Specimen	Proximal†	Distal†	Mean†
1	48	52	53	1	49	63	52
2	71	67	61	2	58	47	50
3	56	36	43	3	33	25	39
4	54	59	54	4	46	46	46
5	71	55	66	5	52	56	58
6	48	49	52	6	49	48	50
7	60	65	59	7	72	70	70
8	52	69	59	8	58	56	58
9	69	70	67	9	60	53	51
10	48	47	57	10	48	62	55
11	45	56	51	11	-	-	-
12	48	41	47	12	-	-	-
Mean and standard deviation	56 ± 10§	55 ± 10	56 ± 7#	Mean and standard deviation	53 ± 10**	53 ± 12	54 ± 8