JBJS | The Influence of Active Shear or Compressive Motion on Fracture-Healing*

The Journal of Bone & Joint Surgery, Volume 80, Issue 6

Articles | June 01, 1998

The Influence of Active Shear or Compressive Motion on Fracture-Healing*

SANG-HYUN PARK, PH.D.†; KIM O'CONNOR, PH.D.‡; HARRY MCKELLOP, PH.D.†; AUGUSTO SARMIENTO, M.D.†, LOS ANGELES, CALIFORNIA

Investigation performed at the J. Vernon Luck Sr., M.D., Orthopaedic Research Center and the University of Southern California, Los Angeles

The Journal of Bone & Joint Surgery. 1998; 80:868-78

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Abstract

The effects of interfragmentary sliding (shear) motion, axial motion, and locked external fixation on the healing of mid-tibial closed fractures were studied in fifty-six skeletally mature New Zealand White rabbits. The fractures were fixed with use of a four-pin, double-bar frame and were allowed to heal for either two or four weeks. Four experimental conditions were evaluated: transverse and oblique fractures treated with a locked external fixator (Groups 1 and 3, respectively), transverse fractures treated with an axially telescoping fixator (Group 2), and oblique fractures treated with a sliding oblique fixator (Group 4).The maximum interfragmentary motion, recorded in vivo with an electronic motion sensor that was attached to the fixator, was 0.6 millimeter in Group 2 during the first week and then declined rapidly. In contrast, the motion in Group 4 exceeded 1.5 millimeters during the first week. The circumference of the callus in Group 4 was 11 to 23 per cent greater than that in the other groups at both two and four weeks (p = 0.02). At two weeks, torsional stiffness, strength, and energy absorption were comparable among Groups 1, 2, and 3. The increase in healing was most rapid for Group 4; by four weeks, the torsional strength and energy to failure of the fractures in Group 4 exceeded those in the other groups (p = 0.025) and reached or exceeded those of intact bone. Apparently, oblique sliding (shear) motion promoted greater cartilage differentiation and expansion of the peripheral callus than did axial motion or locked external fixation.CLINICAL RELEVANCE: These results contradict the widely held opinion that interfragmentary sliding (shear) motion is detrimental to the repair of diaphyseal fractures. Rather, interfragmentary shear motion induces abundant cartilage differentiation in the periosteal callus and is not a principal cause of delayed union or non-union of these fractures.

Figures in this Article

Introduction

Introduction | Materials and Methods | Results | Discussion | References

The presence or absence of interfragmentary motion influences the healing process that leads to consolidation of diaphyseal fractures^1,2,4,5,7,24. The elimination of interfragmentary motion suppresses the formation of external callus; in this situation, fracture repair occurs through the primary process of contact and gap-healing²⁸. Interfragmentary motion at the site of the fracture promotes the formation of a circumferential cartilaginous callus that mineralizes to provide intrinsic stability before the completion of primary cortical repair. However, the type and amount of interfragmentary motion that optimize callus formation and fracture consolidation have been a subject of controversy for many years.

Although it is widely accepted in the orthopaedic literature that interfragmentary sliding (shear) motion impairs fracture-healing^18,30, this belief has not been confirmed in a controlled experimental study, to our knowledge. Rather, clinical experience with functional bracing of tibial fractures has raised questions as to whether shear motion is indeed detrimental. Recent studies of cadavera^10,15 and patients²⁷ have demonstrated that as much as four millimeters of shear displacement occurred parallel to the surfaces of oblique tibial fractures that were stabilized with a functional brace. Other studies have demonstrated that, despite the presence of shear motion, oblique tibial fractures that are treated with a functional brace undergo rapid natural healing and are associated with a low prevalence of delayed union and non-union^21,23,26.

We hypothesized that interfragmentary shear motion in response to early weight-bearing and muscle activity promotes rapid biomechanical consolidation and exuberant callus formation at the site of oblique diaphyseal fractures. We tested this hypothesis with use of an experimental model in which the healing patterns of mid-tibial transverse fractures that were supported by either a locked or an axial telescoping external fixator were compared with those of mid-tibial oblique fractures that were supported by either a locked or an oblique sliding external fixator.

*Although none of the authors has received or will receive benefits for personal or professional use from a commercial party related directly or indirectly to the subject of this article, benefits have been or will be received but are directed solely to a research fund, foundation, educational institution, or other non-profit organization with which one or more of the authors is associated. Funds were received in total or partial support of the research or clinical study presented in this article. The funding sources were the Doctor's Education and Research Fund of Los Angeles Orthopaedic Hospital, the Los Angeles Orthopaedic Hospital Foundation, and the Zumberge Faculty Research and Innovation Fund of the University of Southern California, Los Angeles.

†J. Vernon Luck Sr., M.D., Orthopaedic Research Center, Orthopaedic Hospital, 2400 South Flower Street, Los Angeles, California 90007-2697.

‡Department of Biokinesiology and Physical Therapy, University of Southern California, 1540 East Alcazar Street, CHP 155, Los Angeles, California 90033.

†J. Vernon Luck Sr., M.D., Orthopaedic Research Center, Orthopaedic Hospital, 2400 South Flower Street, Los Angeles, California 90007-2697.

‡Department of Biokinesiology and Physical Therapy, University of Southern California, 1540 East Alcazar Street, CHP 155, Los Angeles, California 90033.

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Fig. 1 Drawings showing the orientation of the fracture and the fixator from anterior to posterior. Unilateral transverse fractures were stabilized with a locked (Group 1) or an axial telescoping (Group 2) external fixator. Unilateral oblique fractures were stabilized with a locked (Group 3) or a sliding oblique (Group 4) external fixator.

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Figs. 2-A and 2-B: Graphs depicting the changes in the in vivo motion of the fracture fragments over time. The connecting lines are intended only to aid in visualizing the changes for each fracture over time; they do not imply a mathematical relationship between motion and time to healing. Fig. 2-A: Transverse fractures fixed with a locked external fixator (Group 1, three animals) or an axial telescoping external fixator (Group 2, four animals).

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Fig. 2-B Oblique fractures fixed with a locked external fixator (Group 3, four animals) or a sliding oblique external fixator (Group 4, four animals). The maximum excursion of the proximeter was 1.8 millimeter. (Each set of closed circles represents a different animal.)

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Fig. 3 Graph illustrating the torsional properties (maximum torque, stiffness, angular displacement at failure, and energy required for failure) of the healing tibial fractures in the different treatment groups at two and four weeks. The values are normalized relative to those for the contralateral, intact tibia. The bars represent the mean and the standard error.

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Figs. 4-A and 4-B: Photomicrographs showing peripheral callus adjacent to the medial cortex of rabbit tibiae after two weeks of healing of transverse fractures (undecalcified sections stained with toluidine blue O; original magnification, x 54; bar = 0.5 millimeter). Fig. 4-A: The callus surrounding a fracture that was treated with a locked external fixator is bridged by immature trabeculae forming through intramembranous ossification.

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Fig. 4-B The callus surrounding a fracture that was treated with an axial telescoping fixator is bridged with fibrous tissue. Small areas of cartilage (arrows) have formed along the interface between the osseous tissue and the fibrous tissue.

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Fig. 5 Photomicrograph showing peripheral callus adjacent to the lateral cortex of the tibia of a rabbit that was treated with an oblique sliding fixator for two weeks. The fracture is bridged by a large mass of fibrocartilaginous tissue. Endochondral ossification is seen at the interface between the cartilage and the trabecular bone (arrow) (undecalcified section stained with toluidine blue O; original magnification, x 20; bar = one millimeter).

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Figs. 6-A and 6-B: Photomicrographs showing peripheral callus adjacent to the medial cortex of rabbit tibiae after four weeks of healing (undecalcified sections stained with toluidine blue O; original magnification, x 21; bar = one millimeter). Fig. 6-A: A transverse fracture that was treated with a locked fixator. The fracture is bridged by well formed trabeculae that are thickened by lamellar bone formation. Delamination between the callus and the cortex is an artifact due to sectioning.

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Fig. 6-B The callus surrounding an oblique fracture that was treated with a sliding fixator is bridged with a large mass of relatively thin osseous trabeculae containing residual spicules of cartilage.

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TABLE I CIRCUMFERENCE OF THE CALLUS AND EX VIVO AXIAL MOTION OF THE FRACTURE*

*The values are given as the mean and the standard deviation, in millimeters, with the number of fractures given in parentheses. †The values are given only for the specimens that were tested biomechanically. ‡Group 1 = transverse fractures treated with a locked fixator, Group 2 = transverse fractures treated with an axial telescoping fixator, Group 3 = oblique fractures treated with a locked oblique fixator, and Group 4 = oblique fractures treated with a sliding oblique fixator. a = Group 1 differs from Group 2 (p = 0.001), b = Group 2 differs from Group 3 (p = 0.09), c = Group 4 differs from all other groups (0.004 = p = 0.02), and d = Group 4 differs from all other groups (0.04 = p = 0.07).

	Circumference of Callus	Ex Vivo Axial Motion of Fracture at 15N†
2 wks. after fracture‡
Group 1	38.8 ± 1.8 (n = 6)	0.03 ± 0.01 (n = 4)
Group 2	43.3 ± 2.6 (n = 7)^a,b	0.02 ± 0.01 (n = 4)
Group 3	40.3 ± 3.0 (n = 6)	0.04 ± 0.03 (n = 3)
Group 4	47.9 ± 4.4 (n = 8)^c	0.12 ± 0.08 (n = 5)^d
4 wks. after fracture‡
Group 1	38.4 ± 6.4 (n = 8)	0.01 ± 0.01 (n = 5)
Group 2	38.1 ± 4.0 (n = 8)	0.01 ± 0.01 (n = 5)
Group 3	36.8 ± 2.2 (n = 5)	0.01 ± 0.01 (n = 2)
Group 4	44.8 ± 4.7 (n = 8)^c	0.01 ± 0.01 (n = 5)

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TABLE I CIRCUMFERENCE OF THE CALLUS AND EX VIVO AXIAL MOTION OF THE FRACTURE*

	Circumference of Callus	Ex Vivo Axial Motion of Fracture at 15N†
2 wks. after fracture‡
Group 1	38.8 ± 1.8 (n = 6)	0.03 ± 0.01 (n = 4)
Group 2	43.3 ± 2.6 (n = 7)^a,b	0.02 ± 0.01 (n = 4)
Group 3	40.3 ± 3.0 (n = 6)	0.04 ± 0.03 (n = 3)
Group 4	47.9 ± 4.4 (n = 8)^c	0.12 ± 0.08 (n = 5)^d
4 wks. after fracture‡
Group 1	38.4 ± 6.4 (n = 8)	0.01 ± 0.01 (n = 5)
Group 2	38.1 ± 4.0 (n = 8)	0.01 ± 0.01 (n = 5)
Group 3	36.8 ± 2.2 (n = 5)	0.01 ± 0.01 (n = 2)
Group 4	44.8 ± 4.7 (n = 8)^c	0.01 ± 0.01 (n = 5)

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TABLE II TORSIONAL PROPERTIES AND BIOMECHANICAL STAGE OF FRACTURE REPAIR

*The values are given as the mean and the standard deviation, according to the per cent ratio of the paired fractured and contralateral, intact tibiae. †Group 1 = transverse fractures treated with a locked fixator, Group 2 = transverse fractures treated with an axial telescoping fixator, Group 3 = oblique fractures treated with a locked oblique fixator, and Group 4 = oblique fractures treated with a sliding oblique fixator. a = Group 3 differs from Group 2 (p = 0.12), b = Group 4 differs from Group 1 (p = 0.12) and Group 2 (p = 0.056), c = Group 4 differs from Group 3 (p = 0.008), d = Group 4 differs from all other groups (0.01 = p = 0.14), e = Group 4 differs from Group 1 (p = 0.14) and Group 2 (p = 0.2), f = Group 4 differs from all other groups (0.004 = p = 0.025), and g = Group 4 differs from Group 1 (p = 0.18) and Group 3 (p = 0.13).

	Torsional Properties* (per cent)
	Strength	Stiffness	Angular Displacement	Energy to Failure	Biomechanical Stage of Fracture Repair³²(no. of fractures)
	I	II	III	IV
2 wks. after fracture†
Group 1 (n = 4)	28 ± 9	39 ± 21	116 ± 65	40 ± 23	0	4	0	0
Group 2 (n = 4)	23 ± 10	43 ± 18	71 ± 21	21 ± 10	0	4	0	0
Group 3 (n = 3)	41 ± 13^a	49 ± 9	83 ± 5	40 ± 10	0	3	0	0
Group 4 (n = 5)	26 ± 13	17 ± 13^b,c	186 ± 60^d	54 ± 23	3	2	0	0
4 wks. after fracture†
Group 1 (n = 5)	59 ± 13	96 ± 28	71 ± 32	51 ± 27	0	0	3	2
Group 2 (n = 5)	65 ± 26	112 ± 41	60 ± 20	56 ± 27	0	0	3	2
Group 3 (n = 2)	52 ± 12	97 ± 5	47 ± 17	31 ± 10^e	0	1	1	0
Group 4 (n = 5)	108 ± 23^f	122 ± 31^g	102 ± 23^d	114 ± 33^f	0	0	0	5

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TABLE II TORSIONAL PROPERTIES AND BIOMECHANICAL STAGE OF FRACTURE REPAIR

	Torsional Properties* (per cent)
	Strength	Stiffness	Angular Displacement	Energy to Failure	Biomechanical Stage of Fracture Repair³²(no. of fractures)
	I	II	III	IV
2 wks. after fracture†
Group 1 (n = 4)	28 ± 9	39 ± 21	116 ± 65	40 ± 23	0	4	0	0
Group 2 (n = 4)	23 ± 10	43 ± 18	71 ± 21	21 ± 10	0	4	0	0
Group 3 (n = 3)	41 ± 13^a	49 ± 9	83 ± 5	40 ± 10	0	3	0	0
Group 4 (n = 5)	26 ± 13	17 ± 13^b,c	186 ± 60^d	54 ± 23	3	2	0	0
4 wks. after fracture†
Group 1 (n = 5)	59 ± 13	96 ± 28	71 ± 32	51 ± 27	0	0	3	2
Group 2 (n = 5)	65 ± 26	112 ± 41	60 ± 20	56 ± 27	0	0	3	2
Group 3 (n = 2)	52 ± 12	97 ± 5	47 ± 17	31 ± 10^e	0	1	1	0
Group 4 (n = 5)	108 ± 23^f	122 ± 31^g	102 ± 23^d	114 ± 33^f	0	0	0	5

Materials and Methods

Introduction | Materials and Methods | Results | Discussion | References

Experimental Design

Sixty-four female New Zealand White rabbits (retired breeders weighing between thirty-nine and forty-three newtons) were used for this study. A unilateral mid-tibial transverse fracture was created in thirty-two rabbits, and a unilateral oblique fracture was created in the remaining thirty-two. Each fracture was anatomically reduced and was fixed with use of a four-pin, double-bar external fixator. The animals were divided into four groups according to the shape of the fracture and the method of fixation (Fig. 1). The rabbits in Group 1 had a transverse fracture that was fixed with a locked external fixator; those in Group 2, a transverse fracture that was fixed with a telescoping fixator that permitted interfragmentary axial motion during limb-loading; those in Group 3, an oblique fracture that was fixed with a locked fixator; and those in Group 4, an oblique fracture that was fixed with a sliding oblique fixator that permitted shear displacement parallel to the fracture surfaces. In each group, eight rabbits were followed for two weeks and eight were followed for four weeks. Five of the eight rabbits from each subgroup were randomly selected for biomechanical testing. All eight fractures in each subgroup were evaluated histologically.

Fractures and Fixation

Each animal was anesthetized with ketamine (fifty milligrams per kilogram of body weight) and xylazine (ten milligrams per kilogram of body weight), administered subcutaneously, and the left hindlimb was prepared for the operation according to routine aseptic procedure. Four Steinmann transfixation pins, two millimeters in diameter and 5.5 centimeters long, were placed in the tibia with use of an air-drill with alternating forward-reverse direction to minimize soft-tissue wrapping. A template was used to ensure accurate and parallel placement of the pins. A transverse or oblique fracture was then created. First, the limb was placed in a prefabricated bivalve cast¹⁷. A unicortical 1.5-millimeter hole was drilled in the lateral tibial cortex, 0.5 centimeter distal to the tibiofibular junction, to serve as a stress-riser. The limb then was mounted on a three-point-bending arbor press with the center loading anvil placed opposite the cortical defect. Displacement of the center anvil was limited to eight millimeters. A transverse or oblique angle was created by appropriate alignment of the cortical defect relative to the center loading point. A transverse fracture was created by placing the cortical defect in direct alignment with the center loading point, whereas an oblique fracture was created by placing the cortical drill-hole one centimeter distal to the center loading point. All fractures were initiated at the lateral cortical defect and extended to the level of the anvil at the medial cortex (Fig. 1). The angle of the oblique fractures averaged 49 degrees (range, 35 to 60 degrees) from the transverse axis of the bone.

The fractures were anatomically reduced and were fixed with use of a four-pin, double-bar external fixator. In Groups 1 and 3, the external bars were locked. In Group 2, the external bars were unlocked to permit axial telescoping motion. Compressive motion during limb-loading was limited by contact of the transverse fracture surfaces. In Group 4, the external bars were aligned parallel to the fracture plane and were unlocked to permit the fracture surfaces to slide over each other in the medial-lateral direction with minimum surface compression. Two springs (spring constant, five newtons per millimeter for each) were used to prevent permanent displacement of the fracture fragments by restoring anatomical alignment when the limb was unloaded (Fig. 1). The sliding fixators allowed maximum downsliding of two millimeters and unrestricted upsliding of the fracture fragments during activity.

The alignment of the fracture was confirmed with use of anteroposterior radiographs that were made after application of the fixator. Morphine (4.5 milligrams per kilogram of body weight) was administered for three days postoperatively. The rabbits were housed in standard cages and were maintained on a nutritionally balanced diet of pellets and water ad libitum. They were examined daily for signs of pin-track infection and for functional recovery of the fractured limb. The pin sites were lavaged twice weekly. Calcein and tetracycline (both administered at a dose of twenty-five milligrams per kilogram of body weight) were injected intraperitoneally, seven and three days, respectively, before the animals were killed, to label sites of new-bone formation.

Measurement of Fracture Motion in Vivo

Sixteen rabbits (four from each subgroup that was to be followed for the entire four-week recovery period) were randomly selected for monitoring of fracture motion in vivo. Interfragmentary axial or oblique sliding motion was measured indirectly by determining the relative motion of the proximal and distal sections of the external fixator while the rabbits walked inside a large pen. The measurements were obtained with use of a detachable electromagnetic continuous proximeter (7200 series; Bently Nevada, Minden, Nevada) that was attached to the lateral side of the fixator; the measuring device had a resolution of 0.1 millimeter. The output was transferred to a strip-chart recorder through a ten-foot (3.048-meter) lead wire. Fracture movement also was recorded while the knee and ankle joints were moved passively through flexion and extension.

Biomechanical Evaluation

The animals were killed with an intravenous injection of 200 milligrams of sodium pentobarbital. Both tibiae were dissected free of muscle and fibrous tissue, and the circumference of the callus was determined to the nearest millimeter with a tape measure. Both tibiae were transected through the proximal and distal metaphyses to provide 8.5-centimeter lengths of diaphyseal shaft. The ends of each bone were embedded in blocks of polymethylmethacrylate that covered the four pin-holes in order to prevent stress concentration during torsional testing. The central portion of the diaphysis, including the fracture site, was wrapped with a sponge soaked in 2 per cent formalin in normal saline solution to prevent drying while the methylmethacrylate polymerized. The specimen was mounted on a combined axial-motion and torsional-testing jig that was attached to a universal testing machine (MTS, Minneapolis, Minnesota). The axial stiffness of the fractured specimen was determined by measuring the relative axial displacement between the embedding blocks with use of a digital indicator (resolution, 0.01 millimeter) under a static axial compressive load of fifteen newtons (approximately 35 per cent of the rabbit's body weight). The fractured and intact tibiae then were loaded to failure in torsion with use of a slow displacement rate of 15 degrees per minute^2,3,8. Ultimate torsional strength, torsional stiffness, angular displacement at failure, and energy required for failure were calculated with use of load-displacement curves and were normalized to the corresponding values for the contralateral, intact tibia. Normalization of the data served to minimize interanimal variability associated with variations in skeletal dimensions^31-33.

Fracture-healing was classified according to the four biomechanical stages described by White et al.³². Stage-I fractures are rubbery, indicating only soft-callus formation, whereas stage-II, III, and IV fractures exhibit high stiffness, indicating failure through mineralized tissue. Specimens with stage-I and II fractures fail through the original fracture line, specimens with stage-III fractures fail partially through the original fracture line and partially through intact bone, and specimens with stage-IV fractures fail entirely through intact bone. All procedures, including torsional testing, were performed within two hours after the animals were killed. Radiographs of the specimens were made after torsional testing to confirm the location of failure.

Anteroposterior radiographs were made immediately after application of the fixator and after two and four weeks of healing. Lateral radiographs were made after the animals were killed, and the fixator was removed before mechanical testing. The radiographs were examined carefully after completion of mechanical testing to identify any abnormalities that might confound the results of the study. The reviewer was blinded with regard to the experimental condition and the results of the mechanical testing. Eight fractures (two in Group 1, one in Group 2, and five in Group 3) were identified as being atypical in that they included segmental fractures or exhibited vertical cracks that extended from the fracture line to the pin tracks. These atypical fractures were excluded from the analysis because they did not accurately represent the oblique or transverse fracture patterns of interest.

Histological Evaluation

The specimens either were embedded undecalcified in polymethylmethacrylate or were embedded in celloidin after decalcification in nitric acid. Non-consecutive frontal plane sections from the central portion of the diaphysis were examined under light microscopy by a reviewer who was blinded with regard to the type of fixator that had been used. Oblique fractures were oriented so that the plane of obliquity was visible in the sections. Undecalcified sections were stained with either toluidine blue O or Goldner trichrome. Decalcified sections were stained with hematoxylin and eosin. Unstained sections from undecalcified specimens also were examined with ultraviolet fluorescence microscopy to ascertain the distribution of the fluorochrome bone labels in the callus.

The fractures were evaluated qualitatively for the presence of mineralized bone, cartilage, fibrous tissue, osteoid, marrow, and undifferentiated mesenchyme within the periosteal and endosteal callus. The tissue was categorized on the basis of the cell morphology and the staining characteristics of the extracellular matrix. Woven or lamellar bone formation in the callus was confirmed by the distribution of the intravital fluorochrome labels that were injected during the final week of healing. The histological sections were categorized according to their predominant features, which included the angle of the fracture plane, the amount of displacement, the extent and location of fibrous tissue and cartilage in the fracture callus, the pattern of bone formation, and the nature of the tissue that bridged the fracture gap at the medial and lateral cortices.

Statistical Analysis

One-way analysis of variance followed by the least-significant-difference method of multiple comparisons was used to calculate the level of significance of the measured differences among the treatment groups with regard to the biomechanical variables and the size of the callus. P values of 0.05 or less were considered significant. For large differences between means (that is, differences considered large enough to be of biological or biomechanical importance) for which the p value was more than 0.05, the specific p value is given if only two groups were compared and the maximum and minimum p values are provided if several groups were compared.

Results

Introduction | Materials and Methods | Results | Discussion | References

Fracture Motion in Vivo

In Groups 1 and 3, less than 0.2 millimeter of interfragmentary motion was measured in vivo throughout the entire recovery period (Figs. 2-A and 2-B). This amount of motion was permitted by the elastic deformation of the locked fixator. In Group 2, axial motion peaked at 0.6 millimeter between the fourth and sixth days after creation of the fracture and then decreased to levels comparable with those in Group 1 by the eleventh day (Fig. 2-A). In Group 4, sliding displacements exceeded the 1.8-millimeter excursion limit of the proximeter for most fractures during the first week and then decreased markedly after two weeks (Fig. 2-B ). In all groups, the fracture gap closed with weight-bearing during gait as well as when the rabbit held the limb in a flexed position under the body. The gap opened when the limb was unweighted or extended to the side. In all animals, the motion produced by passive flexion and extension of the limb was comparable with that observed during free gait.

Callus Formation

The circumference of the callus in Group 4 was 11 to 23 per cent greater than that in any of the other groups at both two and four weeks (0.004 = p = 0.02) (Table I). Eight of the sixteen fractures in Group 4 demonstrated 0.5 to 1.5 millimeters of distal-lateral displacement of the proximal fragment as seen on the radiographs; in these eight specimens, the measurement of the circumference of the callus reflected both the size of the callus and the effect of displacement. The circumference of the callus in Group 2 was 12 per cent greater than that in Group 1 at two weeks (p = 0.001), but a difference was no longer apparent at four weeks (Table I).

Biomechanical Properties

The ex vivo axial displacements that were measured during the application of a fifteen-newton static load reflected the same trend among the groups as had the in vivo motion patterns. At two weeks, the mean axial displacements in Groups 1, 2, and 3 were small (0.03, 0.02, and 0.04 millimeter, respectively) (Table I). In contrast, the fractures in Group 4 were unstable, with a mean axial displacement of 0.12 millimeter (0.04 = p = 0.07). All of the axial displacements completely recovered elastically after removal of the load. At four weeks, all of the fractures were stable, with the mean axial displacement being equal to or less than the 0.01-millimeter resolution of the sensor.

At two weeks, the torsional stiffness of the healing fractures was comparable among Groups 1, 2, and 3 (Table II). In contrast, the torsional stiffness of the fractures in Group 4 averaged 35 to 44 per cent of that in the other groups; however, with the numbers available, not all of these differences were found to be significant (0.008 = p = 0.12). Similarly, the mean angular displacement of the fractures in Group 4 was 60 to 162 per cent greater than that in the other groups; however, with the numbers available, not all of these differences were found to be significant (0.01 = p = 0.14).

Although the mean values for torsional strength and stiffness increased in all groups between two and four weeks, the greatest increases occurred in Group 4. At four weeks, the mean torsional strength in Group 4 was 83 and 108 per cent greater than that in Group 1 and Group 3 (p = 0.005 and p = 0.014, respectively) and 66 per cent greater than that in Group 2 (p = 0.025). The mean torsional stiffness in Group 4 was 27 per cent greater than that in Group 1 and 26 per cent greater than that in Group 3 (although, with the numbers available, these differences were not found to be significant [p = 0.18 and p = 0.13, respectively]) and was similar to that in Group 2 (p = 0.67). The energy to failure in Group 4 was 104 to 268 per cent greater than that in the other groups (0.004 = p = 0.01). The fractures in Group 2 averaged 10 and 25 per cent stronger and 17 and 15 per cent stiffer than those in Groups 1 and 3; with the numbers available, these differences were not found to be significant (p = 0.4 and p = 0.45, respectively). At four weeks, all four of the biomechanical parameters for the fractured specimens in Group 4 reached or exceeded those for the contralateral, intact tibiae, whereas in the other three groups only the value for stiffness approached that of intact bone (Fig. 3 and Table II).

At two weeks, all of the fractures in Groups 1, 2, and 3 and two of the fractures in Group 4 had healed to stage II of the biomechanical classification of fracture repair as described by White et al.³² (Table II). The remaining three fractures in Group 4 were rubbery, indicating stage-I repair. By four weeks, all of the fractures in Group 4 but only one-third of those in Groups 1, 2, and 3 were classified as stage IV. The remaining fractures in the first three groups were classified as stage II or III.

Histological Findings

At two weeks, the fractures that had been treated with a locked fixator (Groups 1 and 3) characteristically were bridged by fusiform masses consisting of immature periosteal and endosteal trabecular bone (Fig. 4-A). In a few specimens, small pockets of fibrocartilaginous tissue were located adjacent to the fracture gap, but these areas always were encased peripherally by trabecular bone. The fractures in Group 2 were similar to those that had been treated with a locked fixator except that the periosteal callus consisted of fibrous or fibrocartilaginous tissue at the level of the fracture plane rather than of contiguous osseous bridges (Fig. 4-B). Pockets of cartilage in the callus were more common and were larger than those in the specimens that had been treated with a locked fixator.

The appearance of the fractures in Group 4 was substantially different from that of the fractures in the other three groups after two weeks of healing (Fig. 5). The proximal fragment of eight of the Group-4 fractures was displaced 0.5 to 1.5 millimeters laterally and distally. Large, mushroom-shaped masses of cartilage were present in the medial and lateral periosteal regions at the level of the fracture gap. The cartilaginous masses were covered peripherally by a fibrous layer and were bounded proximally and distally by buttresses of trabecular callus extending from the cortex. A band of tissue containing regions of trabecular bone, cartilage, and mesenchyme crossed the marrow cavity between the fractured cortices. In all four groups, green calcein and yellow tetracycline labels were distributed diffusely within the mineralizing trabecular bone in the callus, indicating that woven bone had formed between the seventh and twelfth days.

At four weeks, the shape and size of the callus surrounding the fractures in Groups 1 and 3 were similar to those observed at two weeks although the trabecular bone was more mature (Fig. 6-A). The trabeculae appeared to be thicker, and lamellar bone formation predominated. Rows of osteoblasts lined the osteoid seams along the edges of the mineralized trabeculae. Calcein and tetracycline labels were deposited in lines along the edges of the bone, indicating lamellar bone formation. The fractures in Group 2 also were bridged by osseous tissue and could no longer be distinguished from the fractures in Group 1.

The periosteal callus surrounding the fractures that had been treated with the oblique sliding fixator differed both quantitatively and qualitatively from that seen in the other groups after four weeks of healing (Fig. 6-B). The callus surrounding the fractures in Group 4 was larger, and trabecular bone filled the peripheral areas adjacent to the fracture gap that had been occupied by cartilage at two weeks. Although residual pockets of cartilage and fibrous tissue were present within the callus in most specimens, the peripheral shell of the callus crossing the fracture plane was composed of mineralized trabecular bone. The trabeculae in the center of the periosteal callus contained residual spicules of calcified cartilage, indicating that they had formed through endochondral ossification rather than primary intramembranous ossification.

Discussion

Introduction | Materials and Methods | Results | Discussion | References

In the present study, the fractures that had been stabilized with a locked fixator healed with a more rapid increase in stiffness, reflecting a more rapid intramembranous ossification of a smaller external callus, compared with those that had been stabilized with an unlocked external fixator. However, recovery of strength was slower; at four weeks, the strength of the specimens that had been treated with a locked fixator was only 57 per cent that of the contralateral, intact bone (p < 0.0004). The rate of mechanical recovery of the limbs that had been treated with a locked fixator was comparable with that reported previously after locked fixation of tibial osteotomies in rabbits^6,16,33. These results indicate that at least eight weeks is needed to regain normal strength in skeletally mature rabbits in which a tibial fracture has been treated with a locked external fixator.

The early healing pattern of the fractures that were immobilized with a locked fixator in the present study also was consistent with that described in a previous report that compared healing at the sites of transverse and oblique osteotomies in dogs². In both studies, the sites of transverse and oblique fractures and osteotomies demonstrated comparable stiffness after immobilization with a locked fixator. This similarity among healing patterns apparently was due to the fact that very little peripheral callus forms around fractures and osteotomy sites that are stabilized with a conventional external fixator. In the canine study the sites of the transverse osteotomies exhibited greater strength (maximum torque) than those of the oblique osteotomies², whereas in the present study the sites of the two types of fractures exhibited comparable strength (Table II). These differences in outcome may have occurred because the surfaces of fractures typically are more irregular than those of osteotomy sites, and interlocking of these irregular surfaces may have provided additional stability in the present study. In addition, the double-bar frame used in the present study probably provided greater stability than the unilateral fixator used in the canine study.

In the present study, axial motion that occurred perpendicular to the plane of the transverse fractures apparently did not enhance the process of fracture repair. Rather, it tended to result in delayed mineralization of the bridging callus and to promote the formation of fibrous tissue during the early phase of repair. Possibly, the small magnitude of the axial movements that occurred in Group 2 was responsible for the minimum cartilage differentiation observed in the callus mesenchyme surrounding the fracture gap. It appears, therefore, that small axial movements, in part prevented by interlocking of the cortical fragments, are not sufficient to stimulate the extensive expansion of the external callus that was observed around the fractures in Group 4, which underwent large shear motions. Our findings agree with those of previous investigators who demonstrated, in canine studies, that axial compression of the sites of transverse osteotomies, by conversion of the fixator from a static to a dynamic construct, does not promote the formation of large amounts of peripheral callus or improve the biomechanical properties of healing fractures^3,8.

It is interesting to compare the results of the present study with those reported by Kenwright and Goodship^11,13,14. The interfragmentary motions in their studies consisted of one-millimeter displacements that were applied either to the sites of ovine tibial osteotomies (with a three-millimeter gap between the fragments) or to human tibial fractures with use of a pneumatic pump that was attached to a sliding fixator. The one-millimeter displacements in their models were comparable with the peak axial motions of 0.6 millimeter observed in association with the transverse fractures in Group 2 in the present study. In contrast to our findings, however, Kenwright and Goodship reported that controlled cyclic axial motion enhanced fracture-healing. This difference in outcome may be due to the fact that, in our study, motion was controlled by the activity of the animal rather than by an external mechanical device. In addition, the fractures in our study were anatomically reduced without a major gap being left between the fragments and there were no springs or cushions in the fixator to facilitate opening of the fracture during unloading.

Rather than inhibiting healing, the interfragmentary shear motion of 1.8 millimeters that was induced by weight-bearing enhanced the repair of the diaphyseal fractures that were treated with a sliding oblique fixator in the present study. Shear motion along the oblique surfaces of these fractures apparently stimulated abundant formation of peripheral cartilage and expansion of the external callus during the first two weeks of healing. Although the specimens in Group 4 were weak and rubbery when subjected to torsional testing at two weeks, their biomechanical properties improved rapidly as the large mass of external callus was converted to bone through endochondral ossification. This rapid restoration of strength did not occur in Group 1, 2, or 3, in which the circumference of the callus was not enlarged through cartilage formation.

It has been suggested that interfragmentary shear motion causes delayed union and non-union because it impedes vascularization of the callus and creates a plane of cleavage that promotes the differentiation of fibrous tissue between the fractured ends of the bone^18,30. The basis for this opinion apparently was a study in which Yamagishi and Yoshimura reported that so-called pseudarthroses were produced at the sites of tibial osteotomies in rabbits through the application of shear motion³⁴. In one pseudarthrosis model, a spring-loaded fixator maintained a gap between the surfaces of transverse osteotomies while intermittent, interfragmentary shearing forces were generated by spring-loaded plates that pushed the proximal and distal bone fragments horizontally in opposing directions. The direction of the horizontal forces was switched on a daily basis. Under these conditions, strains in the soft tissues adjacent to the ends of the fragments alternated between compressive and distractive. However, lack of consistency in the direction of movement rather than the presence of shear motion may have been the factor that prevented cartilage differentiation. Because the chondrocyte phenotype is labile, chondrocytes that are exposed to tensile loading revert to the fibroblast phenotype²⁹. As it takes at least three to five days for cartilage to appear near a fracture^4,5,9,12, reversal of the loading pattern at twenty-four-hour intervals, as described by Yamagishi and Yoshimura, may not have provided an adequate stimulus for inducing and maintaining chondrocyte differentiation.

Yamagishi and Yoshimura created a second pseudarthrosis model, in which springs were used to generate axial distraction across oblique osteotomy sites during unloading of the limb³⁴. Although large calluses developed, scarlike tissue rather than cartilage formed at the level of the fracture gap in four of the six animals. A major difference between their model and our sliding oblique fixator model was the direction of spring action. The spring mechanism of our sliding oblique fixator was aligned parallel to the fracture line in order to counter distal-lateral displacement during loading and to restore alignment during unloading. As a result, cartilage formed in the tissues located distal-lateral and proximal-medial to the fracture gap, where the formation of a buttress served to limit excursion. In contrast, the axially oriented springs used by Yamagishi and Yoshimura distracted the fracture fragments during unloading and may have prevented the gap from closing completely during weight-bearing. Thus, interfragmentary shear motions would have occurred only when there was sufficient laxity in the fixation system to permit horizontal displacement following contact of the cortical surfaces during loading. Although specific details regarding the amount of shear displacement that occurred in their model were not provided, it is possible that a pseudarthrosis developed because closing of the gap was prevented while tensile loading predominated and interfragmentary sliding motions were minimized.

The spring mechanism that was incorporated into our sliding oblique fixator was designed to restore the anatomical alignment of the segments between periods of weight-bearing while permitting a maximum of two millimeters of slide during weight-bearing or muscle contraction. Eight of the sixteen specimens from the group that was treated with the sliding oblique fixator (Group 4) healed with distal-lateral displacement of the proximal fragment because of the relatively weak spring force, and the remaining eight fractures healed in almost perfect alignment. The circumference of the callus around the displaced fractures was greater than that around the fractures that healed in alignment. However, the torsional strength and stiffness overlapped in the fourth week of healing, with both the strongest and the weakest fractures being in the subgroup of fractures that healed in alignment.

In general, increases in torsional stiffness, strength, and energy to failure correspond directly to the biomechanical stages of fracture repair³². In the early stages of healing, however, the soft callus permitted substantial rotational displacement to occur before failure; therefore, the relationship between energy to failure and the stage of healing was not clear. For example, at two weeks, when the biomechanical stage of fracture repair was stage I, a high value for energy to failure was not a clear indicator of the stage of healing. In contrast, by four weeks, when all of the fractures exhibited the high stiffness that is characteristic of failure through mineralized tissue (stages II, III, and IV), a high value for energy to failure corresponded to the particular stage of fracture-healing.

One limitation of the present investigation was that fracture-healing was not assessed after four weeks; therefore, the results do not encompass the final phases of the healing process that include remodeling of the callus and cortical bridging of the fracture. The four-week end point was selected because, by that time, the biomechanical properties of the fractured tibiae in Group 4 were equivalent to those of the intact tibiae—that is, the callus provided sufficient support that the risk of refracture was minimum. This finding was interpreted as being indicative of a functional level of repair that would coincide with cessation of the need for additional treatment with the external fixator.

The use of 2 per cent formalin in the saline solution before mechanical testing may have slightly increased the stiffness and torque of the stage-I fracture sites as these specimens failed through soft callus. In contrast, the intact tibiae and the specimens with stage-II, III, and IV fractures failed through mineralized tissue, which is less likely to be influenced by the short duration of exposure to the fixative. If a fixative effect had occurred, the primary consequence would have been to reduce the magnitude of the differences between the group treated with the sliding oblique fixator (Group 4) and the other groups at two weeks.

The results of the current study, in conjunction with clinical observations regarding the healing of oblique fractures treated with functional bracing^19,20,26,27, support our proposition that sliding shear motions of as much as four millimeters of displacement between oblique fracture surfaces can enhance fracture-healing by promoting callus expansion and osteogenesis^19,20,25,27 and that these motions are not a principal cause of delayed union or non-union of diaphyseal fractures. Neither locked fixation nor axial telescoping motion at the site of transverse fractures appeared to induce a comparable biological response. Of course, excessive interfragmentary sliding motions that are not recovered during unloading may lead to shortening or malalignment at the site of an oblique fracture. This can be prevented by obtaining adequate support from the fixation device and the surrounding soft tissues²².

NOTE: The authors thank Edward Ebramzadeh, Ph.D., Arkady Preger, M.D., and Elizabeth Kunda for their valuable contributions. They also thank Biomet for donating the Steinmann pins.

References

Introduction | Materials and Methods | Results | Discussion | References

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Aro, H. T.; Kelly, P. J.; Lewallen, D. G.; and Chao, E. Y. S.: The effect of physiologic dynamic compression on bone healing under external fixation. Clin. Orthop.,256: 260-273, 1990.256260 1990 [PubMed]

Ashhurst, D. E.: The influence of mechanical conditions on the healing of experimental fractures in the rabbit: a microscopical study. Phil. Trans. Roy. Soc. London,313-B: 271-302, 1986.313-B271 1986

Brighton, C. T.: Principles of fracture healing. Part I. The biology of fracture repair. In Instructional Course Lectures, the American Academy of Orthopaedic Surgeons. Vol. 33, pp. 60-82. St. Louis, C. V. Mosby, 1984.

Carpenter, J. E.; Hipp, J. A.; Gerhart, T. N.; Rudman, C. G.; Hayes, W. C.; and Trippel, S. B.: Failure of growth hormone to alter the biomechanics of fracture-healing in a rabbit model. J. Bone and Joint Surg.,74-A: 359-367, March 1992.74-A359 1992

Chao, E. Y. S.; Aro, H. T.; Lewallen, D. G.; and Kelly, P. J.: The effect of rigidity on fracture healing in external fixation. Clin. Orthop.,241: 24-35, 1989.24124 1989 [PubMed]

Egger, E. L.; Gottsauner-Wolf, F.; Palmer, J.; Aro, H. T.; and Chao, E. Y.: Effects of axial dynamization on bone healing. J. Trauma,34: 185-192, 1993.34185 1993 [PubMed]

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Hoffman, R.; McKellop, H. A.; Sarmiento, A.; Lu, B.; and Ebramzadeh, E.: Dreidimensionale Messung von Frakturspaltbewegungen: biomechanische Studie an experimentellen Unterschenkelfrakturen mit ventralem Klammerfixateur und Ringfixateur. Unfallchirurgie,94: 395-400, 1991.94395 1991

Goodship, A. E., and Kenwright, J.: The influence of induced micromovement upon healing of experimental tibial fractures. J. Bone and Joint Surg.,67-B(4): 650-655, 1985.67-B(4)650 1985

Jingushi, S.; Joyce, M. E.; and Bolander, M. E.: Genetic expression of extracellular matrix proteins correlates with histologic changes during fracture repair. J. Bone and Min. Res.,7: 1045-1055, 1992.71045 1992

Kenwright, J., and Goodship, A. E.: Controlled mechanical stimulation in the treatment of tibial fractures. Clin. Orthop.,241: 36-47, 1989.24136 1989 [PubMed]

Kenwright, J.; Richardson, J. B.; Goodship, A. E.; Evans, M.; Kelly, D. J.; Spriggins, A. J.; Newman, J. H.; Burrough, S. J.; Harris, J. D.; and Rowley, D. I.: Effect of controlled axial micromovement on healing of tibial fractures. Lancet,2: 1185-1187, 1986.21185 1986 [PubMed]

McKellop, H.; Hoffmann, R.; Sarmiento, A.; Lu, B.; and Ebramzadeh, E.: Control of motion of tibial fractures with use of a functional brace or an external fixator. A study of cadavera with use of a magnetic sensor. J. Bone and Joint Surg.,75-A: 1019-1025, July 1993.75-A1019 1993

Panjabi, M. M.; White, A. A., III; and Southwick, W. O.: Temporal changes in the physical properties of healing fractures in rabbits. J. Biomech.,10: 689-699, 1977.10689 1977 [PubMed]

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Sarmiento, A.: A functional below-the-knee cast for tibial fractures. J. Bone and Joint Surg.,49-A: 855-875, July 1967.49-A855 1967

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Sarmiento, A.; Latta, L. L.; and Tarr, R. R.: Principles of fracture healing. Part II. The effects of function in fracture healing stability. In Instructional Course Lectures, the American Academy of Orthopaedic Surgeons. Vol. 30, pp. 83-106. St. Louis, C. V. Mosby, 1984.

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TABLE I CIRCUMFERENCE OF THE CALLUS AND EX VIVO AXIAL MOTION OF THE FRACTURE*

	Circumference of Callus	Ex Vivo Axial Motion of Fracture at 15N†
2 wks. after fracture‡
Group 1	38.8 ± 1.8 (n = 6)	0.03 ± 0.01 (n = 4)
Group 2	43.3 ± 2.6 (n = 7)^a,b	0.02 ± 0.01 (n = 4)
Group 3	40.3 ± 3.0 (n = 6)	0.04 ± 0.03 (n = 3)
Group 4	47.9 ± 4.4 (n = 8)^c	0.12 ± 0.08 (n = 5)^d
4 wks. after fracture‡
Group 1	38.4 ± 6.4 (n = 8)	0.01 ± 0.01 (n = 5)
Group 2	38.1 ± 4.0 (n = 8)	0.01 ± 0.01 (n = 5)
Group 3	36.8 ± 2.2 (n = 5)	0.01 ± 0.01 (n = 2)
Group 4	44.8 ± 4.7 (n = 8)^c	0.01 ± 0.01 (n = 5)

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TABLE I CIRCUMFERENCE OF THE CALLUS AND EX VIVO AXIAL MOTION OF THE FRACTURE*

	Circumference of Callus	Ex Vivo Axial Motion of Fracture at 15N†
2 wks. after fracture‡
Group 1	38.8 ± 1.8 (n = 6)	0.03 ± 0.01 (n = 4)
Group 2	43.3 ± 2.6 (n = 7)^a,b	0.02 ± 0.01 (n = 4)
Group 3	40.3 ± 3.0 (n = 6)	0.04 ± 0.03 (n = 3)
Group 4	47.9 ± 4.4 (n = 8)^c	0.12 ± 0.08 (n = 5)^d
4 wks. after fracture‡
Group 1	38.4 ± 6.4 (n = 8)	0.01 ± 0.01 (n = 5)
Group 2	38.1 ± 4.0 (n = 8)	0.01 ± 0.01 (n = 5)
Group 3	36.8 ± 2.2 (n = 5)	0.01 ± 0.01 (n = 2)
Group 4	44.8 ± 4.7 (n = 8)^c	0.01 ± 0.01 (n = 5)

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TABLE II TORSIONAL PROPERTIES AND BIOMECHANICAL STAGE OF FRACTURE REPAIR

	Torsional Properties* (per cent)
	Strength	Stiffness	Angular Displacement	Energy to Failure	Biomechanical Stage of Fracture Repair³²(no. of fractures)
	I	II	III	IV
2 wks. after fracture†
Group 1 (n = 4)	28 ± 9	39 ± 21	116 ± 65	40 ± 23	0	4	0	0
Group 2 (n = 4)	23 ± 10	43 ± 18	71 ± 21	21 ± 10	0	4	0	0
Group 3 (n = 3)	41 ± 13^a	49 ± 9	83 ± 5	40 ± 10	0	3	0	0
Group 4 (n = 5)	26 ± 13	17 ± 13^b,c	186 ± 60^d	54 ± 23	3	2	0	0
4 wks. after fracture†
Group 1 (n = 5)	59 ± 13	96 ± 28	71 ± 32	51 ± 27	0	0	3	2
Group 2 (n = 5)	65 ± 26	112 ± 41	60 ± 20	56 ± 27	0	0	3	2
Group 3 (n = 2)	52 ± 12	97 ± 5	47 ± 17	31 ± 10^e	0	1	1	0
Group 4 (n = 5)	108 ± 23^f	122 ± 31^g	102 ± 23^d	114 ± 33^f	0	0	0	5

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TABLE II TORSIONAL PROPERTIES AND BIOMECHANICAL STAGE OF FRACTURE REPAIR

	Torsional Properties* (per cent)
	Strength	Stiffness	Angular Displacement	Energy to Failure	Biomechanical Stage of Fracture Repair³²(no. of fractures)
	I	II	III	IV
2 wks. after fracture†
Group 1 (n = 4)	28 ± 9	39 ± 21	116 ± 65	40 ± 23	0	4	0	0
Group 2 (n = 4)	23 ± 10	43 ± 18	71 ± 21	21 ± 10	0	4	0	0
Group 3 (n = 3)	41 ± 13^a	49 ± 9	83 ± 5	40 ± 10	0	3	0	0
Group 4 (n = 5)	26 ± 13	17 ± 13^b,c	186 ± 60^d	54 ± 23	3	2	0	0
4 wks. after fracture†
Group 1 (n = 5)	59 ± 13	96 ± 28	71 ± 32	51 ± 27	0	0	3	2
Group 2 (n = 5)	65 ± 26	112 ± 41	60 ± 20	56 ± 27	0	0	3	2
Group 3 (n = 2)	52 ± 12	97 ± 5	47 ± 17	31 ± 10^e	0	1	1	0
Group 4 (n = 5)	108 ± 23^f	122 ± 31^g	102 ± 23^d	114 ± 33^f	0	0	0	5