The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 91, Issue 7

Scientific Articles | July 01, 2009

The Effect of Distraction-Resisting Forces on the Tibia During Distraction Osteogenesis

Ashok K. Shyam, MS¹; Hae-Ryong Song, MD, PhD¹; Hyonggin An, PhD²; Dileep Isaac, MS¹; Gautam M. Shetty, MS³; Seok Hyun Lee, MD, PhD⁴

¹ Rare Disease Institute, Department of Orthopedic Surgery, Korea University, Guro Hospital, #80, Guro-Dong, Guro-Gu, Seoul, 152-703 South Korea. E-mail address for H.-R. Song: songhae@korea.ac.kr
² Department of Biostatistics, College of Medicine, Korea University, Anam-dong Seongbuk-Gu, Seoul, 136-701, South Korea
³ Department of Orthopaedic Surgery, B.Y.L. Nair Hospital, T.N. Medical College, Mumbai University, Dr A.L. Nair Road, Mumbai Central, Mumbai-400008, India
⁴ Department of Orthopedic Surgery, Dongguk University International Hospital, Ilsan, South Korea

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Disclosure: The authors did not receive any outside funding or grants in support of their research for or preparation of this work. Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, division, center, clinical practice, or other charitable or nonprofit organization with which the authors, or a member of their immediate families, are affiliated or associated.

Investigation performed at Rare Disease Institute, Department of Orthopedic Surgery, Korea University, Guro Hospital, Guro-gu, Seoul, South Korea

The Journal of Bone and Joint Surgery, Inc.

J Bone Joint Surg Am, 2009 Jul 01;91(7):1671-1682. doi: 10.2106/JBJS.G.01238

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Abstract

Background: Distraction-resisting forces that are generated during distraction osteogenesis can be responsible for complications, including a lag effect on fibular distraction leading to a tibiofibular distraction difference, tibial axial deviation, and distraction at the proximal and distal tibiofibular joints. We investigated the nature of distraction-resisting forces by studying their correlation with these parameters.

Methods: One hundred and eleven tibial lengthening procedures in sixty-three patients were chosen. Seventy-six segments underwent lengthening with an Ilizarov ring fixator, and thirty-five segments had lengthening over an intramedullary nail. Serial radiographs were evaluated with regard to the amounts of tibiofibular distraction difference, proximal tibiofibular joint distraction, distal tibiofibular joint distraction, tibial axial deviation, and heel malalignment. Clinically, laxity at the knee was evaluated and fibular head instability was assessed. Variations in all of these parameters were evaluated with respect to tibiofibular joint fixation, etiology, skeletal maturity, lengthening over an intramedullary nail, and amount of lengthening.

Results: The mean tibiofibular distraction difference was 19.1 ± 10.6 mm (range, 2 to 51 mm), the mean proximal tibiofibular joint distraction was 10.1 ± 6.8 mm (range, 0 to 33 mm), and the mean tibial valgus angulation was 8.7° ± 4.4°. At the time of the latest follow-up, twenty-eight segments (25%) had lateral knee joint laxity at 30° of knee flexion and eight segments (7%) had fibular head subluxation at 90° of knee flexion. Twenty-four (86%) of the twenty-eight cases of knee laxity were observed in skeletally immature patients. The tibiofibular distraction difference, proximal tibiofibular joint distraction, and tibial valgus angulation were significantly greater in the group without fixation of the proximal tibiofibular joint. A significant decrease in the tibial valgus angulation and knee laxity was found in patients with lengthening over an intramedullary nail. In the intramedullary nail group, after fixation of the proximal tibiofibular joint, the tibiofibular distraction difference and the proximal tibiofibular joint distraction decreased; however, the proportion of cases with clinically important tibial valgus angulation (>10°) increased significantly.

Conclusions: Fixing both tibiofibular joints with a single Ilizarov wire decreases proximal tibiofibular joint distraction; however, more secure fixation would help to decrease the prevalence of delayed knee laxity. When tibial lengthening is performed over an intramedullary nail, avoiding proximal tibiofibular joint fixation will limit tibial valgus angulation. Limiting lengthening to <25% will decrease the proportion of cases with knee laxity, and limiting lengthening to <50% will significantly limit tibial valgus angulation.

Level of Evidence: Therapeutic Level III. See Instructions to Authors for a complete description of levels of evidence.

Figures in this Article

Introduction

Distraction osteogenesis is a complex procedure. A clear understanding of the process will help to prevent avoidable complications and to deal with unforeseen ones. The difference in the adaptability of the newly formed bone and established soft tissues during distraction osteogenesis generates resistive tension, termed distraction-resisting forces¹. Codivilla, in 1904, stated that the major limiting factor for bone distraction is the resistance offered by the soft tissues². Abbot, in 1939, tried to solve this problem of soft-tissue resistance by excessive dissection of the muscles and fasciae³. In 1956, Ilizarov developed the biological principles of distraction osteogenesis with use of a modular ring fixator and modified his apparatus according to the differences in muscular resistance and balance at various limb segment levels⁴. Currently, soft tissues are considered to be the single most limiting factor in distraction osteogenesis, causing complications such as muscle contractures, joint stiffness, joint subluxations, and axial deviations⁵.

To address the distraction-resisting forces, modifications and innovations have been made in distraction osteogenesis techniques^6-8. For example, fixation of the distal tibiofibular joint is done to prevent heel valgus deformity that results from proximal migration of the lateral malleolus during tibial lengthening⁹. Ilizarov proposed slanting the proximal wires and rings 10° medially to prevent tibial valgus angulation⁴, and Catagni recommended orienting the proximal ring block in 5° to 7° of valgus and procurvatum to prevent tibial valgus and procurvatum deformities¹⁰.

The role of distraction-resisting forces in the restriction of knee and ankle range of motion and in axial deviation of the tibia is well established⁵, and it is thought to be due to the tension generated in the major muscle groups. Distraction at the proximal and distal tibiofibular joints has been noted by many researchers^11-13 and is correlated with distraction-resisting forces generated by the anterolateral soft tissues of the calf.

The study of distraction-resisting forces has been restricted mostly to animal models^1,6,7. The few published human studies have involved tension gauges applied to the frame^14,15. Hatzokos et al., in a study of fibular migration during tibial distraction osteogenesis with use of a monolateral external fixator, observed that fibular distraction appeared to progress slower than the tibial distraction and that the magnitude of fibular lengthening was less than the tibial lengthening¹³. They attributed this difference to counter-tension exerted by the soft tissues. This tibiofibular distraction difference can be seen to be an indirect effect of the distraction-resisting forces generated in the soft tissues and can be taken as a surrogate measure for the distraction-resisting forces. Finally, the role of distraction-resisting forces in the restriction of knee and ankle range of motion and in axial deviation of the tibia is well established⁵.

We performed a comprehensive radiographic analysis to quantify the nature of distraction-resisting forces by using the tibiofibular distraction difference as a surrogate measure. Clinically, laxity of the knee joint and fibular head subluxation associated with radiographic changes were analyzed in order to improve our understanding of this process.

Materials and Methods

We retrospectively evaluated 183 cases of tibial lengthening that were performed at our institute from 2000 to 2005. Sixty-three of the 183 cases were selected; we excluded (1) patients who had been managed with simultaneous performance of deformity correction and lengthening, (2) patients who had been managed with axial correction procedures during lengthening, (3) patients who had generalized ligamentous laxity such as associated with pseudoachondroplasia and Down syndrome¹⁶, and (4) patients who had been managed with bifocal tibial or proximal fibular osteotomies or lengthening of another segment in the same limb.

In this group of sixty-three patients, a total of 111 tibial segments that were lengthened with distraction osteogenesis were selected. Forty-nine patients had bilateral lengthening, and fourteen had unilateral lengthening. One limb of a patient who had bilateral lengthening was excluded from the study because a bifocal osteotomy for deformity correction was performed in that limb. The study group included thirty-four male patients and twenty-nine female patients with a mean age of 16.2 years (range, six to forty-six years) at the time of surgery. Various etiologies were recorded; the subgroup "Others" included vitamin D-resistant rickets (eight cases), hypothyroidism (four), and metaphyseal chondrodysplasia (four) (Table I).

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TABLE I Comparison According to Etiology

Etiology	No. of Segments	Percent Tibial Lengthening*	Tibiofibular Distraction Difference†(mm)	Proximal Tibiofibular Joint Distraction†(mm)	Tibial Valgus Angulation†(deg)	Knee Laxity (no. of segments)	Fibular Head Subluxation (no. of segments)
Achondroplasia	31	54.7%	22.1 ± 8.9	9.2 ± 5.4	11.8 ± 7.6	16	5
Hypochondroplasia	12	39.9%	31.8 ± 13.5	15.8 ± 8.4	7.8 ± 5.1	6	1
Spondyloepiphyseal dysplasia	10	24.4%	14.0 ± 10.1	7.4 ± 6.1	11.3 ± 4.4	0	0
Idiopathic short stature	28	22.4%	16.8 ± 7.9	9.2 ± 5.4	8.3 ± 3.9	2	2
Limb-length discrepancy	14	15.4%	13.4 ± 7.3	8.1 ± 4.9	8.5 ± 4.3	0	0
Others	16	31.1%	17.8 ± 11.4	11.2 ± 7.1	6.7 ± 4.5	4	0
P value			<0.01‡	0.11‡	0.11‡	<0.001§	0.34§

The values are given as the mean.The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

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TABLE I Comparison According to Etiology

Etiology	No. of Segments	Percent Tibial Lengthening*	Tibiofibular Distraction Difference†(mm)	Proximal Tibiofibular Joint Distraction†(mm)	Tibial Valgus Angulation†(deg)	Knee Laxity (no. of segments)	Fibular Head Subluxation (no. of segments)
Achondroplasia	31	54.7%	22.1 ± 8.9	9.2 ± 5.4	11.8 ± 7.6	16	5
Hypochondroplasia	12	39.9%	31.8 ± 13.5	15.8 ± 8.4	7.8 ± 5.1	6	1
Spondyloepiphyseal dysplasia	10	24.4%	14.0 ± 10.1	7.4 ± 6.1	11.3 ± 4.4	0	0
Idiopathic short stature	28	22.4%	16.8 ± 7.9	9.2 ± 5.4	8.3 ± 3.9	2	2
Limb-length discrepancy	14	15.4%	13.4 ± 7.3	8.1 ± 4.9	8.5 ± 4.3	0	0
Others	16	31.1%	17.8 ± 11.4	11.2 ± 7.1	6.7 ± 4.5	4	0
P value			<0.01‡	0.11‡	0.11‡	<0.001§	0.34§

The values are given as the mean.The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

Operative and Postoperative Protocol

Seventy-six segments were lengthened with use of an Ilizarov apparatus alone, and thirty-five segments were lengthened over an intramedullary nail with use of the Ilizarov rings. A single-level transverse osteotomy was performed at the junction of the middle and distal thirds of the fibula. The proximal tibiofibular joint was fixed with use of a single 1.8-mm Ilizarov wire, except in the cases of nine patients with achondroplasia in whom the fibula was high-riding and the proximal tibiofibular joint was not fixed (as recommended by Catagni¹⁰) so that it could be pulled down during distraction in order to obtain a normal tibiofibular relationship. Distraction of 0.25 mm four times daily was begun approximately seven days after the operation. In the Ilizarov fixator group, the external fixator was removed when three new cortices were visible on plain radiographs¹⁷. In the intramedullary nail group, the ring fixator was removed after completion of the distraction period and the distal interlocking screws were inserted. These patients in the intramedullary nailing group were permitted full weight-bearing when at least two cortices were visible radiographically¹⁸.

Evaluation Technique

All patients were evaluated clinically and radiographically every two weeks during the distraction period and every four weeks during the consolidation period. All of the radiographs were digital (STAR PACS Pi view, STAR 5.0.6.1 software; INFINITT, Seoul, South Korea) and were made at a distance of 1 m with the patella facing forward, as per standard protocol, resulting in a comparable magnification of 1.2, which was accounted for during the measurement of callus distraction.

The radiographs were evaluated with regard to five parameters: (1) the tibiofibular distraction difference (calculated by subtracting total fibular distraction from total tibial distraction at the end of the distraction period) (Fig. 1), (2) proximal tibiofibular joint distraction (calculated by measuring the distal migration of the fibular head by comparing the positions of the fibular head relative to the tibial plateau¹³ on the preoperative radiograph and the radiograph made at the end of the distraction period) (Fig. 2), (3) distal tibiofibular joint distraction (calculated by measuring proximal migration of the distal part of the fibula by comparing the amount of the lateral malleolus that projected distal to the medial malleolus on the preoperative radiograph and on the radiograph made at the end of the distraction period¹²) (Fig. 3), (4) tibial valgus angulation (calculated by comparing the orientation of the joint lines of the knee and ankle on preoperative radiographs with those on the postoperative and follow-up radiographs) (Fig. 4), and (5) heel malalignment (evaluated by comparing the tibiocalcaneal angle on calcaneal axial radiographs made preoperatively and at the time of the latest follow-up) (Fig. 5). For the parameter of tibial valgus angulation, a value of >10° was assumed to be clinically important because a residual deformity of such magnitude might warrant surgical correction¹⁹.

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Fig. 1: The tibiofibular distraction difference was calculated by subtracting total fibular distraction from total tibial distraction.

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Fig. 2: Proximal tibiofibular joint distraction was calculated by measuring migration of the fibular head as seen on preoperative and postoperative radiographs with use of the tibial plateau as the reference point.

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Fig. 3: Distal tibiofibular joint distraction was measured by comparing the amount of the lateral malleolus projecting distal to the medial malleolus on preoperative and postoperative radiographs.

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Fig. 4: Tibial valgus angulation was calculated by comparing the orientation of the knee and ankle joint lines on preoperative and postoperative radiographs.

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Fig. 5: Calcaneal axial view radiographs were used to measure the tibiocalcaneal angle preoperatively and postoperatively.

The results of the clinical examination at the time of fixator removal were obtained from the medical records, and all patients were examined at the time of the latest follow-up by at least two of the authors (A.K.S. and H.-R.S.). Knee and ankle joint stiffness was recorded, and muscle power across the respective joints was assessed along with any knee or ankle malalignment. Instability at the proximal tibiofibular joint was indicated by elicitation of abnormal fibular head movement with the knee in 90° of flexion, localized tenderness at the proximal tibiofibular joint, restriction of range of knee motion (especially extension), or tingling sensations in the distal part of the leg^16,20. Laxity at the knee at 0° of extension and 30° of flexion was assessed and graded according to the amount of joint opening as zero, 1+ (=5 mm), 2+ (6 to 10 mm), or 3+ (>10 mm)²¹. Ankle joint laxity was also assessed clinically with the anterior drawer test and medial and lateral stress tests.

Study Design

We focused on factors affecting distraction-resisting forces by analyzing the tibiofibular distraction difference, tibial valgus angulation, proximal tibiofibular joint distraction, distal tibiofibular joint distraction, and heel malalignment. The changes during the distraction period were the main focus of our study.

In the patients in whom lengthening was performed over an intramedullary nail, the nail was not locked distally during the distraction period and was not in contact with the distraction apparatus; thus, there should have been no difference in the distraction-resisting forces for these patients as compared with those in whom lengthening was performed without an intramedullary nail. Hence, all cases of lengthening over a nail and lengthening without a nail were pooled together, and the entire patient population was studied to assess how the study variables were affected by seven factors: (1) the security of proximal tibiofibular joint fixation (with nonsecure fixation being defined as that in patients with wire removal, wire breakage, or wire cutout because of distal migration of the fibular head), (2) diagnosis, (3) sex, (4) skeletal maturity as measured with the method of Greulich and Pyle²², (5) the type of lengthening (with or without the use of a nail), (6) the magnitude of lengthening, and (7) the combination of proximal tibiofibular joint fixation and the use of an intramedullary nail.

Statistical Methods

The use of a large sample size allowed the assumption of normal sample distribution according to the central limit theorem, thus allowing the use of more sensitive parametric methods for statistical analysis. Means and standard deviations of continuous outcome measurements and the frequency of categorical outcome measurements for each group were presented. Because segments were observed twice in most subjects, the response variables measured within the same subject were very likely to be correlated. In order to compare various study groups after accounting for the within-subject correlation, we used linear mixed models, which can effectively model the correlation structure among repeated measures. When outcome variables were binary, marginal models with a generalized estimating equation were used for the comparison. The marginal models also effectively accounted for the correlations among repeated categorical measures. As the nominal level of significance decreases as the number of simultaneous comparisons increases in post hoc analyses, we used the Bonferroni multiple comparison correction method. The level of significance was set at 0.05.

Source of Funding

We did not have a funding source for this study.

Results

For the entire group, the mean amount of lengthening was 8 ± 2.8 cm (range, 1.9 to 13 cm) and the mean percentage lengthening was 34.5% (range, 5% to 86%) of the original tibial length. The mean duration of follow-up was thirty-five months (range, twenty-five to eighty months). The mean tibiofibular distraction difference was 19.1 ± 10.6 mm (range, 2 to 51 mm), and the mean amount of proximal tibiofibular joint distraction was 10.1 ± 6.8 mm (range, 0 to 33 mm). The tibia was found to be angulated into valgus in all cases, and the mean amount of tibial valgus angulation was 8.7° ± 4.4° (range, 2° to 18°). The mean amount of distal tibiofibular joint distraction was 2.4 ± 3.3 mm (range, 0 to 13 mm); however, sixty-eight segments (61%) had no distal tibiofibular joint distraction and only twenty-one segments (19%) had distraction of >5 mm. The mean tibiocalcaneal angle was 1.7° ± 8.46° of varus (range, 21° of varus to 23° of valgus).

On clinical examination at the time of the latest follow-up, twenty-eight segments (25%) had lateral knee joint laxity at 30° of knee flexion; twenty-four segments had 1+ laxity, and four segments had 2+ laxity. No patient had knee ligament laxity at full extension, and no patient had ankle joint or distal tibiofibular joint laxity. Also, eight segments (7%) had fibular head subluxation (defined as excessive anteroposterior mobility without dislocation¹⁶) at 90° of knee flexion, and one patient had a palpable and audible click originating from the proximal tibiofibular joint when active flexion and extension of the knee joint was performed. No patient reported pain or tenderness at the fibular head with direct palpation or rotation of the foot. No patient reported a subjective sense of instability at the knee joint during walking or running. No peroneal nerve abnormality was found, with all patients recovering full range of motion and power at the knee and ankle joints at the end of the extensive rehabilitation period. Sixty-five segments had an Achilles tendon lengthening procedure to restore ankle range of motion. No surgical soft-tissue release was performed for the treatment of knee stiffness because stiffness consistently responded well to physiotherapy.

The results among the various subgroups are described below.

Fixation of the Proximal Tibiofibular Joint

With patient age and the amount of lengthening being comparable between the two groups, the tibiofibular distraction difference, proximal tibiofibular joint distraction, and tibial valgus angulation were significantly higher in the group without fixation of the proximal tibiofibular joint (Table II). We could not identify a difference between the two groups with regard to knee laxity or fibular head subluxation.

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TABLE II Comparison According to Fixation of Proximal Tibiofibular Joint

Fixation of Proximal Tibiofibular Joint	No. of Segments	Percent Tibial Lengthening*	Tibiofibular Distraction Difference†(mm)	Proximal Tibiofibular Joint Distraction†(mm)	Tibial Valgus Angulation†(deg)	Knee Laxity (no. of segments)	Fibular Head Subluxation (no. of segments)
Proximal tibiofibular joint fixed	59	34.3%	14.8 ± 7.2	6.6 ± 4.6	8.1 ± 4.4	12	3
Proximal tibiofibular joint not fixed	52	34.6%	24.5 ± 11.8	13.6 ± 6.1	10.5 ± 6.6	16	5
P value			<0.05‡	<0.05‡	<0.05‡	0.30§	0.65§

The values are given as the mean.The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

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TABLE II Comparison According to Fixation of Proximal Tibiofibular Joint

Fixation of Proximal Tibiofibular Joint	No. of Segments	Percent Tibial Lengthening*	Tibiofibular Distraction Difference†(mm)	Proximal Tibiofibular Joint Distraction†(mm)	Tibial Valgus Angulation†(deg)	Knee Laxity (no. of segments)	Fibular Head Subluxation (no. of segments)
Proximal tibiofibular joint fixed	59	34.3%	14.8 ± 7.2	6.6 ± 4.6	8.1 ± 4.4	12	3
Proximal tibiofibular joint not fixed	52	34.6%	24.5 ± 11.8	13.6 ± 6.1	10.5 ± 6.6	16	5
P value			<0.05‡	<0.05‡	<0.05‡	0.30§	0.65§

The values are given as the mean.The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

Diagnosis

The tibiofibular distraction difference varied significantly among the etiological groups (p < 0.01), but, with the numbers available, tibial valgus angulation and proximal tibiofibular joint distraction did not (Table I). Bonferroni multiple comparison correction showed that the mean tibiofibular distraction difference and the mean amount of proximal tibiofibular joint distraction in patients with hypochondroplasia and the mean tibial valgus angulation in patients with achondroplasia were significantly (p < 0.05) higher than in other patients. The prevalence of knee laxity was found to be significantly higher in patients with achondroplasia (p < 0.001); however, with the numbers available, no significant difference with regard to fibular head instability was noted.

Skeletal Maturity, Sex, and Lengthening Over a Nail (Table III)

Twenty-four (86%) of the twenty-eight cases of lateral knee laxity were noted in the skeletally immature group. No significant difference was noted among the two sexes with regard to measured parameters. Knee laxity was observed in only three (9%) of thirty-five segments in the group in which an intramedullary nail was used, compared with twenty-five (33%) of seventy-six segments in the group in which a nail was not used (p < 0.05). The mean amount of tibial valgus angulation was less when an intramedullary nail was used (6.8° ± 3.8° compared with 9.7° ± 5.9°; p < 0.05).

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TABLE III Comparison According to Skeletal Maturity, Sex, and Presence of Intramedullary Nail

Variable	No. of Segments	Percent Tibial Lengthening*	Tibiofibular Distraction Difference†(mm)	Proximal Tibiofibular Joint Distraction†(mm)	Tibial Valgus Angulation†(deg)	Knee Laxity (no. of segments)	Fibular Head Subluxation (no. of segments)
Skeletal maturity
Immature	65	41.4%	19.9 ± 11.2	9.2 ± 6.9	9.8 ± 6.2	24	5
Mature	46	23.6%	18.6 ± 10.1	10.8 ± 5.4	8.6 ± 4.8	4	3
P value			0.70‡	0.23‡	0.44‡	<0.01§	0.84§
Sex
Males	61	32.9%	21.3 ± 10.6	10.3 ± 6.4	10.1 ± 4.8	15	4
Females	50	34.8%	16.9 ± 10.5	9.4 ± 6.3	8.3 ± 6.6	13	4
P value			0.16‡	0.68‡	0.23‡	0.90§	0.82§
Intramedullary nailing
With nail	35	23.2%	16.5 ± 8.7	9.7 ± 5.1	6.8 ± 3.8	3	3
Without nail	76	39.8%	20.4 ± 10.7	10.3 ± 7.4	9.7 ± 5.9	25	5
P value			0.20‡	0.84‡	<0.05‡	<0.05§	0.67§

The values are given as the mean.The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

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TABLE III Comparison According to Skeletal Maturity, Sex, and Presence of Intramedullary Nail

Variable	No. of Segments	Percent Tibial Lengthening*	Tibiofibular Distraction Difference†(mm)	Proximal Tibiofibular Joint Distraction†(mm)	Tibial Valgus Angulation†(deg)	Knee Laxity (no. of segments)	Fibular Head Subluxation (no. of segments)
Skeletal maturity
Immature	65	41.4%	19.9 ± 11.2	9.2 ± 6.9	9.8 ± 6.2	24	5
Mature	46	23.6%	18.6 ± 10.1	10.8 ± 5.4	8.6 ± 4.8	4	3
P value			0.70‡	0.23‡	0.44‡	<0.01§	0.84§
Sex
Males	61	32.9%	21.3 ± 10.6	10.3 ± 6.4	10.1 ± 4.8	15	4
Females	50	34.8%	16.9 ± 10.5	9.4 ± 6.3	8.3 ± 6.6	13	4
P value			0.16‡	0.68‡	0.23‡	0.90§	0.82§
Intramedullary nailing
With nail	35	23.2%	16.5 ± 8.7	9.7 ± 5.1	6.8 ± 3.8	3	3
Without nail	76	39.8%	20.4 ± 10.7	10.3 ± 7.4	9.7 ± 5.9	25	5
P value			0.20‡	0.84‡	<0.05‡	<0.05§	0.67§

The values are given as the mean.The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

Magnitude of Lengthening

The tibiofibular distraction difference, proximal tibiofibular joint distraction, tibial valgus angulation, and severity of knee laxity all were found to increase with an increase in the percentage of lengthening (Table IV). The varied pattern of increase among these variables is shown in Figure 6. When Bonferroni multiple comparison correction was applied, the group with <25% lengthening had a significantly lower mean tibiofibular distraction difference, the group with 25% to 50% lengthening had a significantly higher mean amount of proximal tibiofibular joint distraction, and the group with >50% lengthening had a significantly higher mean amount of tibial angulation. Knee laxity differed significantly among the groups (p < 0.05), with the number of cases with laxity increasing as the amount of lengthening increased.

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Fig. 6: The graph shows trends in the magnitude of the tibiofibular distraction difference (TFDD), the proximal tibiofibular joint distraction (PTFD), and the tibial valgus angulation (TVA) as a function of percentage tibial lengthening.

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TABLE IV Comparison According to Percentage Lengthening

Percentage Lengthening	No. of Segments	Percent Tibial Lengthening*	Tibiofibular Distraction Difference†(mm)	Proximal Tibiofibular Joint Distraction†(mm)	Tibial Valgus Angulation†(deg)	Knee Laxity (no. of segments)	Fibular Head Subluxation (no. of segments)
<25%	44	17.7%	15.5 ± 8.0	7.7 ± 5.4	8.0 ± 4.0	3	4
25% to 50%	45	35.6%	22.7 ± 11.9	12.9 ± 7.2	8.1 ± 4.4	12	2
>50%	22	65.21%	22.5 ± 7.6	10.1 ± 5.7	12.3 ± 7.7	13	2
P value			<0.01‡	<0.01‡	<0.05‡	<0.05§	0.39§

The values are given as the mean.The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

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TABLE IV Comparison According to Percentage Lengthening

Percentage Lengthening	No. of Segments	Percent Tibial Lengthening*	Tibiofibular Distraction Difference†(mm)	Proximal Tibiofibular Joint Distraction†(mm)	Tibial Valgus Angulation†(deg)	Knee Laxity (no. of segments)	Fibular Head Subluxation (no. of segments)
<25%	44	17.7%	15.5 ± 8.0	7.7 ± 5.4	8.0 ± 4.0	3	4
25% to 50%	45	35.6%	22.7 ± 11.9	12.9 ± 7.2	8.1 ± 4.4	12	2
>50%	22	65.21%	22.5 ± 7.6	10.1 ± 5.7	12.3 ± 7.7	13	2
P value			<0.01‡	<0.01‡	<0.05‡	<0.05§	0.39§

The values are given as the mean.The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

Combined Effect of Proximal Tibiofibular Joint Fixation and Intramedullary Nail (Table V)

In the Ilizarov ring fixator group, the tibiofibular distraction difference and the amount of proximal tibiofibular joint distraction were significantly less when the proximal tibiofibular joint was fixed. The number of segments with a significant tibiofibular distraction difference or knee laxity, however, did not differ. In the intramedullary nail group, the tibiofibular distraction difference and the amount of proximal tibiofibular joint distraction were significantly less when the proximal tibiofibular joint was fixed; however, the number of segments with clinically important tibial valgus angulation of >10° was significantly higher in the group with proximal tibiofibular joint fixation. With the numbers studied, knee joint laxity did not differ significantly between these groups.

Discussion

We attempted to study distraction-resisting forces during distraction osteogenesis. During tibial lengthening, the posterolateral soft tissues and the fibular regenerate contribute to the deforming distraction-resisting forces that cause tibial valgus angulation¹⁰. The angulation can also be secondary to early fixator removal, delayed union, nonunion, or refracture^5,19. Our examination of tibial valgus angulation at the end of the distraction period essentially eliminates these variables and focuses on the tethering effect caused by the distraction-resisting forces. Distal migration of the fibular head during tibial lengthening has been reported in association with distraction osteogenesis with use of a monolateral external fixator^13,23. Distal migration of the fibula even after fixation of the proximal tibiofibular joint with an Ilizarov wire results from the strong tethering effects of the fibular regenerate and the interosseous membrane along with disproportionate soft-tissue tensioning¹³, and hence the amount of proximal tibiofibular joint distraction will increase with the increase in magnitude of the distraction-resisting forces.

The response of connective tissue to distraction osteogenesis was studied in detail in animals by Ilizarov⁸, who observed fibroblast proliferation and the laying down of both elastin and collagen fibers in response to the tension stress effects. Also, tendons were shown to grow proportionately when distracted²⁴. Thus, the lateral collateral ligament and the tendon of the biceps femoris both elongated when the fibular head migrated distally. However, when the distraction-resisting forces decreased during the consolidation period, the ligaments and tendons underwent stress relaxation because of their inherent viscoelastic properties^15,25. This stress relaxation resulted in laxity of the proximal tibiofibular joint capsule and the lateral collateral ligament, thus causing lateral knee joint laxity and fibular head subluxation.

The presence of knee joint laxity during tibial lengthening has been reported anecdotally²⁶, and one case of fibular head subluxation was reported by Hatzokos et al.¹³. In the present series, twenty-eight segments had lateral knee laxity at 30° of knee flexion and eight had fibular head subluxation. All of these patients had had removal of the fixator more than two years previously, and none of them had noted laxity after fixator removal or during the rehabilitation period. This delayed response of the ligaments and joint capsule may be secondary to a creep property of the ligaments as described by Frank²⁷. Creep is deformation (or elongation) that occurs under a constant or cyclically repetitive load. Thus, the delayed knee laxity and fibular head subluxation that we found can be attributed to the creep generated secondary to cyclical loading of the already stretched ligaments. We believe that a combined effect of viscoelastic relaxation and creep deformation led to the delayed knee laxity in our patients.

An analysis of the various subgroups helps us to understand other factors affecting the distraction-resisting forces.

Tibiofibular Joint Fixation

Distraction-resisting forces are generated because the distractive forces are transmitted directly to bone by rigid wire fixation. The intact soft tissues are not fixed rigidly by the wires and are distracted through an indirect pull exerted by the distracting bones. Fixation of the ends of the fibula with the Ilizarov wires helps to decrease the discrepancy in distracting forces by transmitting forces to the soft tissues directly attached to the fibula and also to the fibular regenerate, thus decreasing the tibiofibular distraction difference. In the present study, the tibiofibular distraction difference was less when the fibula was fixed at both ends. The resulting decreases in the amount of proximal tibiofibular joint distraction and tibial valgus angulation are the clinical advantages merited by fixation of both tibiofibular joints.

The phenomenon of proximal tibiofibular joint distraction has been reported to be unknown in association with distraction osteogenesis with use of the Ilizarov apparatus, presumably because of wire fixation of the proximal tibiofibular joint¹³. In contrast, we found definite proximal tibiofibular joint distraction (mean, 6.6 mm; maximum, 19 mm) in patients in whom the proximal tibiofibular joint was fixed with a single Ilizarov wire. Only ten of the fifty-nine segments with proximal tibiofibular joint fixation had no proximal tibiofibular joint distraction, indicating that single-wire fixation of the proximal tibiofibular joint is inadequate. Kashiwagi et al. concluded that a half pin provided the best fixation for the proximal tibiofibular joint when compared with an AO screw, a Knowles pin, or Ilizarov wire fixation²⁸. The mean amount of distal tibiofibular joint distraction was 2.4 mm in the present study, but 61% of the patients had no distal tibiofibular joint distraction and only twenty-one segments (19%) had distraction of >5 mm. Other studies of distal tibiofibular joint distraction during distraction osteogenesis with fixation with use of a single Ilizarov wire also have demonstrated that single-wire fixation is sufficient to prevent distal tibiofibular joint distraction and heel valgus deformity^12,28.

Etiological Group

Many studies have evaluated distraction osteogenesis in patients with achondroplasia and other skeletal dysplasias^29-34; however, to our knowledge, no study has assessed variation in distraction-resisting forces among disease states. Paley mentioned that the soft tissues in patients with achondroplasia tolerate lengthening with fewer problems, perhaps because the muscle lengths exceed the bone lengths before lengthening³⁵. Our results showed a relatively high tibiofibular distraction difference in patients with achondroplasia and hypochondroplasia, indicating a relatively high magnitude of distraction-resisting forces in association with these disorders; however, this finding also can be explained on the basis of the greater amount of lengthening achieved in both of these groups of patients. Proximal tibiofibular joint distraction was greater in patients with hypochondroplasia, whereas tibial valgus angulation was greater in patients with achondroplasia. This disparity cannot be explained, especially because the achondroplasia and hypochondroplasia groups were found to be closely matched with respect to skeletal maturity, tibiofibular joint fixation, and the frequency of lengthening over an intramedullary nail.

Myers et al. reported increased rates of axial deviation in patients with spondyloepiphyseal dysplasia²⁹, and our results also demonstrated that the average tibial valgus angulation in patients with spondyloepiphyseal dysplasia was 11.3°, second only to the amount of angulation seen in patients with achondroplasia. This finding is important because the amount of lengthening in patients with spondyloepiphyseal dysplasia was only 24.4%, as compared with 54.7% in patients with achondroplasia. Noonan et al. reported that tibial lengthening in patients with idiopathic short stature and limb-length discrepancy was associated with more problems as compared with lengthening in patients with bone dysplasias³⁶; however, Catagni et al. reported no additional difficulties during limb lengthening in patients with idiopathic short stature³⁷. In our series, patients with idiopathic short stature and limb-length discrepancy had mean tibiofibular distraction differences that were significantly less than those in patients with bone dysplasias, indicating a lesser amount of distraction-resisting forces being generated in the soft tissues. However, this finding again may be a function of the amount of lengthening as the amount of lengthening was much less in groups with idiopathic short stature and limb-length discrepancy. More patients with achondroplasia had knee joint laxity that could be attributed to the laxity of ligaments associated with achondroplasia^38,39; however, none of our patients had preoperative knee joint laxity.

Skeletal Maturity

Young patients have been reported to have fewer complications during limb lengthening⁵. This finding has been attributed to better adaptability of young muscles and soft tissues. Animal experiments have demonstrated that young animals have a significantly greater proliferative response to the distraction stimulus than do mature animals^40,41. We could not demonstrate a significant difference in the distraction-resisting forces generated in the immature and mature soft tissues during the distraction period. Eighty-six percent of the cases of knee joint laxity were seen in the skeletally immature group, a finding that was perhaps attributable to more stretchable ligaments^42,43.

Sex

Almost all studies in the literature have supported the view that sex has no effect on distraction osteogenesis. An exception is the study by Ganel and Horoszowski, who showed growth retardation in skeletally immature female patients with achondroplasia⁴⁴. In our study, no difference was noted between the two sexes.

Intramedullary Nailing

Lengthening over an intramedullary nail prevents axial deviation^18,45,46, and, in our study, tibial valgus angulation was significantly less in patients who underwent lengthening over an intramedullary nail. It seems that the presence of an intramedullary nail does not affect the generation of distraction-resisting forces; however, additional research will be required to explain this observation. Another significant observation was the low rate of knee laxity (9%) in the group treated with lengthening over an intramedullary nail; however, this finding can be explained by the fact that most of the patients with lengthening over a nail were skeletally mature.

Magnitude of Lengthening

It is well accepted in the literature that associated problems increase proportionally as the percentage of lengthening increases^47-50. Antoci et al.⁵⁰ observed a significantly increased complication rate in association with lengthening of >25%. Our study also showed that the tibiofibular distraction difference was significantly lower in association with lengthening of <25% of the original tibial length. Proximal tibiofibular joint distraction increases rapidly in the midrange of 25% to 50% lengthening and then slows, whereas tibial valgus angulation increases steadily in the first two ranges but shows rapid increase beyond 50% lengthening (Fig. 6). This helps us to postulate the events occurring during distraction osteogenesis. The tibiofibular distraction difference in the initial stages puts tension on the ligaments of the proximal tibiofibular joint, causing proximal tibiofibular joint distraction. Later, when the tension in these ligaments is high, tibial valgus angulation starts to increase rapidly. Thus, the distraction-resisting forces can be said initially to pull on the tibiofibular joints and then later to exert a deforming force on the tibia. This assumption is supported by the fact that the number of cases of knee laxity significantly increased with lengthening beyond 25%. Hence, limiting the lengthening to <25% will minimize the number of cases of knee laxity, and limiting lengthening to <50% will significantly limit tibial valgus angulation.

Combined Effect of Proximal Tibiofibular Joint Fixation and an Intramedullary Nail

The tibiofibular distraction difference, and thus the distraction-resisting forces, were significantly reduced by proximal tibiofibular joint fixation in both the Ilizarov group and the intramedullary nail group. An interesting observation was the increase in the number of patients with clinically important tibial valgus angulation in the intramedullary nail group when the proximal tibiofibular joint was fixed (Table V). A possible explanation, based on the assumption stated above, is that distraction-resisting forces first distract the proximal tibiofibular joint and then secondarily deform the tibia. Thus, when the proximal tibiofibular joint is fixed, the distraction-resisting forces generated are directly transferred to the distraction site, deforming it. Hence, to minimize tibial valgus angulation, proximal tibiofibular joint fixation probably should be avoided in cases of lengthening over a nail. No fixation of the proximal tibiofibular joint will cause an increase in proximal tibiofibular joint distraction; however, our results show that this increase in proximal tibiofibular joint distraction did not translate into increased knee laxity in the long term.

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TABLE V Comparison Between Groups with and without Fixation of Proximal Tibiofibular Joint According to Type of Lengthening

Type of Lengthening	Proximal Tibiofibular Joint Not Fixed	Proximal Tibiofibular Joint Fixed	P Value
Ilizarov ring lengthening
No. of segments	37	39
Tibiofibular distraction difference*(mm)	24.9 ± 12.7	15.5 ± 8.0	<0.05†
Proximal tibiofibular joint distraction*(mm)	13.8 ± 6.4	7.5 ± 4.5	<0.001†
Tibial valgus angulation >10° (no. of segments)	17	20	0.65‡
Knee laxity (no. of segments)	13	12	0.80‡
Lengthening over intramedullary nail
No. of segments	15	20
Tibiofibular distraction difference*(mm)	23.3 ± 9.6	13.2 ± 5.5	<0.01†
Proximal tibiofibular joint distraction*(mm)	13.4 ± 4.9	6.9 ± 3.3	<0.001†
Tibial valgus angulation >10° (no. of segments)	1	7	<0.05‡
Knee laxity (no. of segments)	2	1	0.36‡

The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

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TABLE V Comparison Between Groups with and without Fixation of Proximal Tibiofibular Joint According to Type of Lengthening

Type of Lengthening	Proximal Tibiofibular Joint Not Fixed	Proximal Tibiofibular Joint Fixed	P Value
Ilizarov ring lengthening
No. of segments	37	39
Tibiofibular distraction difference*(mm)	24.9 ± 12.7	15.5 ± 8.0	<0.05†
Proximal tibiofibular joint distraction*(mm)	13.8 ± 6.4	7.5 ± 4.5	<0.001†
Tibial valgus angulation >10° (no. of segments)	17	20	0.65‡
Knee laxity (no. of segments)	13	12	0.80‡
Lengthening over intramedullary nail
No. of segments	15	20
Tibiofibular distraction difference*(mm)	23.3 ± 9.6	13.2 ± 5.5	<0.01†
Proximal tibiofibular joint distraction*(mm)	13.4 ± 4.9	6.9 ± 3.3	<0.001†
Tibial valgus angulation >10° (no. of segments)	1	7	<0.05‡
Knee laxity (no. of segments)	2	1	0.36‡

The values are given as the mean and the standard deviation.Linear mixed model.Marginal model with generalized estimating equation.

The present study had a few limitations. Varus instability of the knee secondary to fibular collateral ligament injury can lead to a varus thrust gait pattern and the potential development of medial meniscal tears or medial compartment arthritis over time because of the increased compressive forces in the medial tibiofemoral compartment⁵¹. Therefore, the clinical importance of lateral knee laxity secondary to gradual stretching of the lateral knee structures seen in the present study requires additional long-term assessment. Fibular head instability was consistently associated with lateral knee laxity. While no patient had symptoms (except for clicking in one patient), additional evaluation of fibular head instability needs to be done. Another shortcoming of the present study is the heterogeneity of the patient population and the lack of exact case matching to minimize these differences.

Our study leads to the following conclusions.

Fixing both tibiofibular joints with single Ilizarov wires decreases proximal tibiofibular joint distraction; however, single-wire fixation of the proximal tibiofibular joint seems to be inadequate, and more secure fixation might decrease this effect even more, thus decreasing the prevalence of knee laxity following tibial lengthening with an Ilizarov ring fixator.

Lengthening over an intramedullary nail decreases tibial valgus angulation significantly as compared with lengthening with the Ilizarov fixator alone. However, our results showed that if the proximal tibiofibular joint is not fixed when the lengthening is performed over an intramedullary nail, the number of cases of clinically important (>10°) tibial valgus angulation decreases significantly.

When planning lengthening beyond 25% and 50% of the initial tibial length, an increased incidence of knee laxity and tibial valgus angulation, respectively, should be anticipated.

A knowledge of the effects of specific diseases and skeletal maturity can be helpful for planning limb lengthening procedures and for anticipating complications arising because of increased distraction-resisting forces. Image Not Available

Acknowledgements

Note: The authors thank Sang-Youn Song, Kyung Hee University, and June Seng Lee, Kyung Bok High School, Seoul, South Korea, for their assistance in the preparation of the manuscript.

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Topics

bone nails ; bone wires ; fibula ; osteogenesis, distraction ; tibia ; proximal tibiofibular joint structure ; intramedullary rods ; knee joint laxity

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Ashok K. Shyam, Hae-Ryong Song, Hyonggin An, Dileep Isaac, Gautam M. Shetty, Seok Hyun Lee; The Effect of Distraction-Resisting Forces on the Tibia During Distraction Osteogenesis. The Journal of Bone & Joint Surgery. 2009 Jul;91(7):1671-1682.

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