JBJS | Intrasynovial Flexor Tendon Repair : An Experimental Study Comparing Low and High Levels of in Vivo Force During Rehabilitation in Canines

The Journal of Bone & Joint Surgery, Volume 83, Issue 6

Articles | June 01, 2001

Intrasynovial Flexor Tendon Repair : An Experimental Study Comparing Low and High Levels of in Vivo Force During Rehabilitation in Canines

Martin I. Boyer, MD; Richard H. Gelberman, MD; Meghan E. Burns, BS; Haralambos Dinopoulos, MD; Rosemarie Hofem, MD; Matthew J. Silva, PhD

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Investigation performed at the Department of Orthopaedic Surgery, Barnes-Jewish Hospital at Washington University, St. Louis, Missouri
Martin I. Boyer, MD
Richard H. Gelberman, MD
Meghan E. Burns, BS
Haralambos Dinopoulos, MD
Rosemarie Hofem, MD
Matthew J. Silva, PhD
Department of Orthopaedic Surgery, Barnes-Jewish Hospital at Washington University, One Barnes Hospital Plaza, Suite 11300, St. Louis, MO 63110

No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was Grant AR33097 from the National Institutes of Health.

A commentary is available with the electronic versions of this article, on our web site (www.jbjs.org) and on our CD-ROM (call 781-449-9780, ext. 140, to order).

The Journal of Bone & Joint Surgery. 2001; 83:891-899

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Abstract

Background: Rehabilitation methods that generate increased tendon force and motion have been advocated to improve results following intrasynovial flexor tendon repair. However, the effects of rehabilitation force and motion on tendon-healing may be masked by the high stiffness produced by newer suture methods. Our objective was to determine whether the biomechanical properties of tendons repaired by one of two multistrand suture methods were sensitive to an increased level of applied rehabilitation force.

Methods: Two hundred and fourteen flexor digitorum profundus tendons from 107 adult dogs were transected and repaired. Dogs were assigned to one of four groups based on the rehabilitation method (low force [<5 N] or high force [17 N]) and the repair technique (four-strand or eight-strand core suture) and were killed between five and forty-two days after the procedure. Repair-site structural properties were determined by tensile testing, and digital range of motion was assessed with use of a motion-analysis system.

Results: Tensile properties did not differ between the low and high-force rehabilitation groups, regardless of the repair technique (p > 0.05). In contrast, tensile properties were strongly affected by the repair technique, with tendons in the eight-strand group having an approximately 35% increase in ultimate force and rigidity compared with those in the four-strand group (p < 0.05). Ultimate force did not change significantly with time during the first twenty-one days (p > 0.05); there was no evidence of softening in either of the repair or rehabilitation groups. Force increased significantly from twenty-one to forty-two days, while rigidity increased throughout the forty-two-day period (p < 0.05).

Conclusions: Increasing the level of force applied during postoperative rehabilitation from 5 to 17 N did not accelerate the time-dependent accrual of stiffness or strength. Suture technique was of primary importance in providing a stiff and strong repair throughout the early healing interval.

Clinical Relevance: Our findings suggest that there be a reexamination of the concept that increases in force produced by more vigorous mobilization protocols are beneficial to tendon-healing. While more vigorous rehabilitation may help to improve hand function, we found no evidence that it enhances tissue-healing or strength in the context of a modern suture repair.

Figures in this Article

Introduction

In an effort to improve the results of intrasynovial flexor tendon repair, authors have advocated rehabilitation methods that generate increased levels of applied in vivo force and increased levels of intrasynovial tendon excursion^1-7. The clinical success of rehabilitation protocols employing early passive motion has encouraged surgeons to prescribe protocols that further increase the "motion stress" on the repair site in order to stimulate healing⁸. The potential success of these rehabilitation methods is based, in part, on the availability of multistrand suture techniques that minimize repair-site deformation in the early stages of rehabilitation^9-13. However, high-stiffness suture methods may attenuate the responsiveness of the repair site to increased force by reducing the strain imposed on the tendon cells and their matrix. Until recently, interactions between suture technique and the rehabilitation variables of repair-site excursion and applied force have not been investigated.

In an experimental study, Lieber et al.¹⁴ provided a quantitative basis for evaluating the force and excursion components of rehabilitation as independent variables following tendon repair. The described methodology was used recently in an animal model of flexor tendon injury and repair to determine the effects of varying levels of repair-site excursion applied at the same level of force¹⁵. While 1.7 mm of repair-site excursion was found to be sufficient to minimize the formation of intrasynovial adhesions, levels of excursion beyond 1.7 mm had no significant beneficial effect on either the functional or the structural properties of the repair.

Our objective in the current study was to complement the previous investigation on tendon excursion by assessing the effects of variations in applied in vivo force on the strength and range of motion of repaired intrasynovial tendons. We hypothesized that, during the first six weeks of healing, intrasynovial flexor tendons would be sensitive to varying levels of applied postoperative force in both a repair-dependent and a time-dependent fashion. To our knowledge, this experiment is the first to assess the effects of applied in vivo force as an independent variable in a clinically relevant model of tendon repair.

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Fig. 1-A:: Figs. 1-A through 1-D Postoperative passive-rehabilitation protocols. Fig. 1-A With the dorsal and volar blocks removed from the distal end of the cast, the canine forelimb was initially positioned with the wrist flexed and the digits extended.

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Fig. 1-B:: Fig. 1-B The digits were then brought into full flexion.

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Fig. 1-C:: For the dogs in the low-force group, the wrist was then brought into extension while the digits were maintained in flexion. The motion cycle was then repeated (Figs. 1-A, 1-B, and 1-C).

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Fig. 1-D:: For the dogs in the high-force group, the wrist and digits were simultaneously brought into full extension. The motion cycle was then repeated (Figs. 1-A, 1-B, and 1-D).

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Fig. 2:: Comparison of ultimate force versus time between rehabilitation protocols for tendons repaired with use of the four-strand technique. There were no significant differences between the effects of high and low-force rehabilitation. Similar findings were observed for the eight-strand repair group.

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Fig. 3:: Comparison of ultimate force versus time between suture techniques. From zero to twenty-one days, tendons repaired with the eight-strand technique were significantly stronger than those repaired with the four-strand technique. Data from low and high-force rehabilitation groups are pooled. The asterisks denote a significant difference between the eight and four-strand techniques (p < 0.05).

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Fig. 4:: Repair-site rigidity versus time. Rigidity increased significantly with time for both the four and the eight-strand repair group. Data from low and high-force rehabilitation groups are pooled. The asterisks denote a significant difference from the value at the preceding time-point (p < 0.05).

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TABLE I: Tensile Properties of Canine Flexor Digitorum Profundus Tendons*

*The values are given as the average and the standard deviation.

Parameter	Rehabilitation	0 Days		5 Days		10 Days		21 Days		42 Days
4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand
Ultimate force (N)	Low force	48.7 ± 7.5	70.8 ± 16.6	60.7 ± 5.7	79.3 ± 7.0	49.7 ± 10.3	69.8 ± 10.3	60.7 ± 12.4	75.4 ± 24.1	102.2 ± 27.8	118.6 ± 23.6
	High force	51.3 ± 8.6	77.6 ± 11.8	52.7 ± 7.7	79.4 ± 16.6	57.3 ± 11.9	83.3 ± 9.8	95.6 ± 29.8	102.2 ± 24.6
Repair-site rigidity (N/[mm/mm])	Low force	???223 ± 88	???305 ± 91	741 ± 161	956 ± 149	612 ± 345	813 ± 273	854 ± 262	1373 ± 342	1952 ± 828	1897 ± 733
	High force	653 ± 260	884 ± 244	655 ± 196	784 ± 290	894 ± 376	1230 ± 372	2029 ± 906	2077 ± 629
Repair-site strain at 20 N (%)	Low force	12.0 ± 3.2	?9.3 ± 2.0	5.4 ± 1.0	5.4 ± 1.0	6.8 ± 2.5	5.2 ± 1.0	5.2 ± 1.6	4.4 0.9	3.2 ± 0.8	2.8 ± 0.5
	High force	6.6 ± 1.1	6.3 ± 1.2	6.3 ± 1.7	5.4 ± 1.1	5.0 ± 1.5	4.3 1.0	2.9 ± 1.2	3.7 ± 1.5
Repair-site strain at failure (%)	Low force	32.6 ± 10.5	37.7 ± 10.3	11.6 ± 2.2	12.6 ± 1.5	13.9 ± 4.4	11.4 ± 2.0	12.4 ± 3.7	10.3 3.1	7.4 ± 1.8	9.3 ± 1.9
	High force	13.5 ± 2.7	14.4 ± 2.8	12.8 ± 4.6	14.4 ± 3.3	11.2 ± 3.4	12.4 4.3	7.0 ± 1.9	8.7 ± 2.9

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TABLE I: Tensile Properties of Canine Flexor Digitorum Profundus Tendons*

*The values are given as the average and the standard deviation.

Parameter	Rehabilitation	0 Days		5 Days		10 Days		21 Days		42 Days
4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand
Ultimate force (N)	Low force	48.7 ± 7.5	70.8 ± 16.6	60.7 ± 5.7	79.3 ± 7.0	49.7 ± 10.3	69.8 ± 10.3	60.7 ± 12.4	75.4 ± 24.1	102.2 ± 27.8	118.6 ± 23.6
	High force	51.3 ± 8.6	77.6 ± 11.8	52.7 ± 7.7	79.4 ± 16.6	57.3 ± 11.9	83.3 ± 9.8	95.6 ± 29.8	102.2 ± 24.6
Repair-site rigidity (N/[mm/mm])	Low force	???223 ± 88	???305 ± 91	741 ± 161	956 ± 149	612 ± 345	813 ± 273	854 ± 262	1373 ± 342	1952 ± 828	1897 ± 733
	High force	653 ± 260	884 ± 244	655 ± 196	784 ± 290	894 ± 376	1230 ± 372	2029 ± 906	2077 ± 629
Repair-site strain at 20 N (%)	Low force	12.0 ± 3.2	?9.3 ± 2.0	5.4 ± 1.0	5.4 ± 1.0	6.8 ± 2.5	5.2 ± 1.0	5.2 ± 1.6	4.4 0.9	3.2 ± 0.8	2.8 ± 0.5
	High force	6.6 ± 1.1	6.3 ± 1.2	6.3 ± 1.7	5.4 ± 1.1	5.0 ± 1.5	4.3 1.0	2.9 ± 1.2	3.7 ± 1.5
Repair-site strain at failure (%)	Low force	32.6 ± 10.5	37.7 ± 10.3	11.6 ± 2.2	12.6 ± 1.5	13.9 ± 4.4	11.4 ± 2.0	12.4 ± 3.7	10.3 3.1	7.4 ± 1.8	9.3 ± 1.9
	High force	13.5 ± 2.7	14.4 ± 2.8	12.8 ± 4.6	14.4 ± 3.3	11.2 ± 3.4	12.4 4.3	7.0 ± 1.9	8.7 ± 2.9

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TABLE II: Tensile Properties of Canine Flexor Digitorum Profundus Tendons Depending on Gap Size*

*The values are given as the average and the standard deviation. Data from all experimental groups are pooled. †The value was significantly different from that in the group with a gap of =3 mm (p < 0.001).

Parameter	Gap Size
=3 mm	>3 mm
Ultimate force (N)	?74.3 ± 25.9	?48.1† ± 14.3
Repair-site rigidity (N/[mm/mm])	1129 ± 709	?525† ± 283
Repair-site strain at 20 N (%)	?5.0 ± 1.8	?7.7† ± 2.2
Repair-site strain at failure (%)	11.4 ± 3.9	15.6† ± 7.2

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TABLE II: Tensile Properties of Canine Flexor Digitorum Profundus Tendons Depending on Gap Size*

Parameter	Gap Size
=3 mm	>3 mm
Ultimate force (N)	?74.3 ± 25.9	?48.1† ± 14.3
Repair-site rigidity (N/[mm/mm])	1129 ± 709	?525† ± 283
Repair-site strain at 20 N (%)	?5.0 ± 1.8	?7.7† ± 2.2
Repair-site strain at failure (%)	11.4 ± 3.9	15.6† ± 7.2

Materials and Methods

Two hundred and fourteen flexor digitorum profundus tendons from the right forelimbs of 107 adult mongrel dogs (20 to 30-kg body mass) were transected and immediately repaired. Dogs were assigned to one of four groups based on the suture technique (four strands or eight strands) and rehabilitation (low force or high force) that had been used, and they were killed at five, ten, twenty-one, or forty-two days. All operations, postoperative care, and rehabilitation were performed in a licensed animal-care facility and were approved by our institutional animal studies committee.

For surgery, the animals were anesthetized with an initial intravenous dose of thiopental sodium (0.5 mL/kg), supplemented by intermittent injections of atropine (0.5 mL) and acepromazine (0.2 mL). They were intubated and were maintained on 1% halothane anesthesia. The forelimbs were shaved, washed with Betadine (povidone-iodine), and exsanguinated, and the surgery was performed under tourniquet control. The sheaths of the second and fifth digits in the region between the annular pulleys proximal and distal to the proximal interphalangeal joint were exposed through midlateral incisions. The sheaths were entered, and the flexor digitorum profundus tendons were cut transversely. The tendons were repaired with either a four or an eight-strand core-suture technique, although the repair technique was not varied between tendons in the same dog. The four-strand technique consisted of a modified Kessler repair^4,15 performed with use of double-stranded 4-0 Supramid suture (S. Jackson, Alexandria, Virginia), supplemented with a 6-0 nylon running peripheral suture. The eight-strand technique consisted of two orthogonally placed, four-strand repairs performed with use of a continuous loop¹⁶. The sheaths were not repaired, and the skin was closed with use of a running suture of 4-0 nylon. An additional thirty-two tendons from sixteen dogs were repaired post mortem to provide time-zero tensile data.

After surgery, the right forelimbs were immobilized with use of fiberglass shoulder spica casts with the elbows flexed 90Â° and the wrists flexed 70Â°. The distal ends of the casts were removable to allow for controlled passive mobilization during two five-minute rehabilitation sessions performed five days a week starting on the first postoperative day. Rehabilitation in the low-force group consisted of flexing and extending the digits with the wrist flexed, followed by digital flexion as the wrist was synergistically extended (Figs. 1-A, 1-B, and 1-C). Rehabilitation in the high-force group was performed by simultaneously flexing and extending the wrist and four digits ((Figs. 1-A, 1-B, and 1-D). We have previously demonstrated in vivo that the low-force protocol produces an average force on the flexor digitorum profundus tendon of <5 N, whereas the high-force protocol produces an average of 17 N (p < 0.05)^14,17. Both protocols were performed at a rate of 1 Hz, resulting in approximately 600 cycles of loading per day. At the time of death, the right (repaired) and left (control) forelimbs were disarticulated at the elbow and were stored at 4Â°C until range-of-motion testing.

The second and fifth digits were disarticulated at the metacarpophalangeal joint, and the flexor digitorum profundus tendons were transected proximally at the musculotendinous junction. The range of motion of both the control and the repaired digits was assessed within forty-eight hours post mortem with use of a computerized motion-analysis system (PC-Reflex; Qualisys, Glastonbury, Connecticut)^15,18. Tests were conducted at room temperature (23Â°C). Two cameras with infrared light sources were placed 1 m from the region of interest with their axes 60Â° apart. The system was calibrated with use of a three-dimensional frame with six reflective markers at known coordinate locations. A circle of reflective tape (2.5 mm in diameter) was glued to the flexor tendon proximal to the A2 pulley with use of cyanoacrylate glue. Two pairs of reflective hemispherical markers (4 mm in diameter) were pinned to the middle and distal phalanges of each digit. The specimen was then held in neutral position with the proximal phalanx oriented vertically, and 0.15-N weights were suspended from the flexor digitorum profundus and extensor digitorum tendon stumps. The coordinates of the markers were sampled for five seconds. The digit was then flexed by increasing the flexor-tendon weight to 1.5 N, and the marker coordinates were resampled. Three motion parameters were calculated on the basis of the differences between the neutral and flexed positions: flexion of the distal interphalangeal joint, flexion of the proximal interphalangeal joint, and displacement of the flexor tendon. On the basis of repeated trials, the precision of this technique was 7% for flexion of the distal interphalangeal joint, 11% for flexion of the proximal interphalangeal joint, and 13% for displacement of the tendon. Following range-of-motion testing, the digits were stored at -20Â°C until tensile testing¹⁹.

The digits were thawed to 23Â°C, and each repair site was exposed through a midlateral incision, with care taken not to disrupt the intact pulley system or any adhesions between the tendon and the intrasynovial sheath. We observed that nineteen tendons from eighteen dogs were ruptured. There were zero ruptures, four ruptures, zero ruptures, and one rupture at five, ten, twenty-one, and forty-two days, respectively, in the four-strand, low-force group. The corresponding values were zero, four, one, and two in the four-strand, high-force group; one, two, one, and two in the eight-strand, low-force group; and zero, zero, zero, and one in the eight-strand, high-force group. The length of the gap between the original cut ends of each nonruptured tendon was measured with use of digital calipers¹⁸. In the four-strand, low-force group, one tendon, three tendons, one tendon, and two tendons had a gap of >3 mm at five, ten, twenty-one, and forty-two days, respectively. The corresponding values were zero, zero, one, and six in the four-strand, high-force group; zero, two, two, and zero in the eight-strand, low-force group; and zero, one, zero, and one in the eight-strand, high-force group.

The flexor digitorum profundus tendon with the attached distal phalanx was then isolated from each of the digits that had been operated on and was tested in tension with use of a materials testing machine (8500R; Instron, Canton, Massachusetts). Ruptured tendons and those from the control digits were not tested. Two reflective markers, centered at the repair site 15 mm apart, were glued onto the volar surface of each tendon. The specimens were tested in a neutral position, with the distal phalanx clamped in a rigid fixture and the tendon aligned vertically and held in a dry-ice freeze-clamp²⁰. The distal phalanx was displaced axially at a rate of 0.5% of the specimen length per second until failure. Synchronized force and marker data were collected during the tests with use of the motion-analysis system to monitor tendon elongation¹⁸. On the basis of the positions of the two markers, we calculated repair-site elongation per unit length (millimeters/millimeter), with the unit length defined as initial distance between the markers. Four outcome parameters were determined from plots of force versus elongation per unit length: ultimate (maximum) force (in newtons), repair-site rigidity (the slope of the curve, newtons/[millimeters/millimeter]), repair-site strain (as a percentage) at a 20-N force, and repair-site strain (as a percentage) at failure. Rigidity provides a measure of repair-site stiffness, and strain at a 20-N force provides a measure of repair-site elongation at a force level associated with active digital motion in humans^21,22. Data from three tendons were lost as a result of technical errors.

Eight, sixteen, nineteen, and twenty-one intact tendons remained in the four-strand, low-force group at five, ten, twenty-one, and forty-two days, respectively, whereas eight, sixteen, fifteen, and twenty-two tendons remained in the four-strand, high-force group; seven, ten, seven, and five intact tendons remained in the eight-strand, low-force group; and eight, fifteen, eight, and seven tendons remained in the eight-strand, high-force group. Paired t tests were used to compare the motion parameters of control and repaired digits (Statview 4.5; Abacus Concepts, Berkeley, California). Three-way analysis of variance was used to compare the effects of rehabilitation (low force compared with high force), repair technique (four strands compared with eight strands), and time (at zero, five, ten, twenty-one, or forty-two days) on range-of-motion and tensile properties. Post hoc comparisons between groups were made with use of the Tukey test. Range-of-motion values for digits with ruptured tendons and tensile values for tendons with a gap of >3 mm were excluded from the statistical analysis. We eliminated tendons with a gap of >3 mm because, in a previous study, we had determined that such tendons have significantly reduced tensile properties and delayed healing compared with tendons with a gap of = 3 mm¹⁸ (p < 0.05). Thus, exclusion of tendons with a large gap eliminated the confounding effect of gap size on tensile properties. Chi-square analysis was used to determine the effects of rehabilitation, repair technique, and time on the prevalence of ruptures and of gaps of <1 mm, 1 to 3 mm, and >3 mm.

Results

Effects of Rehabilitation

The rehabilitation method did not significantly affect ultimate force (p = 0.48), repair-site rigidity (p = 0.96), strain at 20 N (p = 0.29), or strain at failure (p = 0.22) (Fig. 2 and Table I). For example, in the four-strand group, tendons treated with high-force rehabilitation had an average ultimate force of 95.6 N at forty-two days, which was not significantly different from the average of 102.2 N for the low-force rehabilitation group.

The method of rehabilitation also had no significant effect on flexion of the distal (p = 0.91) or proximal (p = 0.87) interphalangeal joint, but it did significantly affect tendon displacement (p = 0.024). Tendons treated with high-force rehabilitation had, on the average, 10% less displacement when loaded with a 1.5-N ex vivo force than tendons treated with low-force rehabilitation (see Appendix). Repaired digits had approximately the same range of motion as contralateral, control digits. Flexion of the proximal interphalangeal joint (p = 0.20) and tendon displacement (p = 0.58) were not significantly different between the repaired and control digits. Flexion of the distal interphalangeal joint was significantly reduced in the repaired digits but by only 11% compared with the control (28.4Â° for the control digits compared with 25.2Â° for the repaired digits; p < 0.001).

The prevalence of ruptures was not significantly affected by the rehabilitation method (p = 0.45). Eleven (10%) of the 106 tendons treated with low-force rehabilitation ruptured, whereas eight (7%) of the 108 tendons treated with high-force rehabilitation ruptured. Similarly, the rehabilitation method did not affect gap size (p = 0.81). Sixty-seven, seventeen, and eleven tendons in the low-force group had gaps of <1 mm, 1 to 3 mm, and >3 mm in length, respectively, whereas seventy-one, twenty, and nine tendons in the high-force group had gaps of those sizes.

Effects of Repair Technique

The repair technique had a highly significant effect on tensile properties, with tendons in the eight-strand repair group having increased ultimate force (p < 0.001) and rigidity (p = 0.009) and decreased strain at 20 N (p < 0.001) compared with tendons in the four-strand group. The differences in ultimate force between the repair groups were significant at each time-point from zero to twenty-one days, with the eight-strand repairs failing at a force that was an average of 42% greater than the force at which the four-strand repairs failed (Fig. 3). Similarly, during the first twenty-one days, rigidity was an average of 35% greater in the eight-strand group than it was in the four-strand group. Strain at failure was not affected by the repair technique (p = 0.055).

The repair technique had no significant effect on the joint flexion angle (measured ex vivo) of either the distal (p = 0.91) or the proximal (p = 0.62) interphalangeal joint, but it did have a significant effect on tendon displacement (p = 0.010). Tendons repaired with the eight-strand technique had an average of 9% less displacement than tendons repaired with the four-strand technique (see Appendix).

The rupture rate was not significantly affected by the repair technique (p = 0.90). Twelve (9%) of the 138 tendons repaired with four strands ruptured, whereas seven (9%) of the seventy-six tendons repaired with eight strands ruptured. The repair technique did have a significant effect on gap size (p = 0.016), with the four-strand group having a greater prevalence of gaps of >1 mm than the eight-strand group. Eighty-one, thirty-one, and fourteen four-strand repairs had gaps of <1 mm, 1 to 3 mm, and >3 mm in length, respectively, whereas fifty-seven, six, and six eight-strand repairs had gaps of those sizes.

Effects of Time

With increasing time, repaired tendons became stronger and stiffer and sustained less elongation at 20 N and at failure (p < 0.001). The ultimate force did not change significantly from zero to twenty-one days, but it increased significantly from twenty-one to forty-two days (p < 0.05). In contrast, repair-site rigidity increased from zero to five days and increased further from ten to twenty-one days and from twenty-one to forty-two days (p < 0.05; Fig. 4). On the average, tendons at forty-two days had 70% higher force and 650% greater rigidity compared with tendons at zero days. Similarly, repair-site strain at 20 N decreased significantly from zero to five days and decreased further from ten to twenty-one days and from twenty-one to forty-two days, whereas repair-site strain at failure decreased significantly from zero to five days and from twenty-one to forty-two days (p < 0.05). Taken together, these data indicate that ultimate force changed significantly only after twenty-one days of in vivo healing, while other tensile properties (rigidity, strain at 20 N, and strain at failure) changed significantly in the first five days of in vivo healing and continued to change with time.

Effects of Gap Size

Gap size had a significant effect on tensile properties. Tendons with a gap of >3 mm had, on the average, 35% lower ultimate force, 53% less rigidity, 54% higher strain at 20 N, and 37% higher strain at failure compared with tendons with no gap or a gap of =3 mm (p < 0.001; Table II). These findings indicate that tendons with a large gap were markedly less stiff and strong and had correspondingly increased deformation during tensile testing.

Discussion

Authors of previous experimental studies have described the site of an immature tendon repair as a gelatinous exudate extending between two tendon stumps²³. Labeled the exudative stage of repair, the first sixteen to twenty-one days was considered an interval during which repair tissue was incapable of responding positively to externally applied loads. Furthermore, it was observed that there was a consistent interval, five to nine days following repair, during which the repair site softened and ultimate force decreased significantly^23-25. Recent studies challenging this view have demonstrated that the early repair process is an active one consisting of an upregulation of compounds known to be responsible for transduction of extracellular matrix signals to the cell interior (integrins) and for angiogenesis^26-30. Moreover, tendon cells and explants have been observed in vitro to respond to increased levels of mechanical stress^31-33. On the basis of these recent studies, we hypothesized that intrasynovial flexor tendons treated with protective passive mobilization would be responsive to variations in applied in vivo force during the early intervals following repair.

Our results during the first twenty-one days of healing confirm some of the findings of previous investigators and extend those findings in important ways. First, we did not observe a significant increase in ultimate force (strength) from zero to twenty-one days, an observation that is consistent with those of previous studies^9,23. Second, we did not observe a significant decrease in force (that is, softening) in the first ten days, a finding that differs from those of some earlier reports^23,25,34 but that correlates well with the observations of others who stated that little or no softening occurs when passive-motion rehabilitation is used in the early period following repair^9,24. To our knowledge, ours is the first report demonstrating an absence of softening when multistrand suture repair was followed by clinically relevant passive-motion rehabilitation. Third, in addition to a lack of softening, we observed significant increases in repair-site rigidity (stiffness) and concurrent decreases in strain at 20 N during the first twenty-one days. These data indicate that not only was the early softening phenomenon obviated but functional changes in the repair tissue that increased the resistance to deformation were taking place during this time interval. The finding that increases in rigidity preceded increases in ultimate force has not been noted previously in studies of tendon-healing, to our knowledge, but it is analogous to changes reported during fracture-healing, in which bone stiffness recovers more quickly than does bone strength³⁵.

In contrast to our finding that there were no increases in strength during the first three weeks, all of the experimental groups, irrespective of the repair or rehabilitation technique, demonstrated an accrual of repair-site strength and rigidity between the third and sixth weeks. These data support the findings of previous authors who indicated that, beginning at twenty-one days, the repair was sufficiently well differentiated with regard to the level of tissue maturity to be able to respond positively to applied stress and motion^23,24. Despite these changes in tensile properties with time, however, we did not observe additional increases in tendon stiffness or strength as a result of increased levels of rehabilitation force. These findings suggest that, provided that minimal levels of motion and force are applied, the stiffness and strength of the repair site do not increase in proportion to clinically relevant increases in the level of passive rehabilitation force during the first six weeks of healing.

While the magnitude of applied force in the first six weeks following repair was not a significant independent variable insofar as the accrual of tendon strength was concerned, the technique of repair was highly significant. The eight-strand suture method resulted in superior strength and rigidity compared with the four-strand method, with an average difference of approximately 35% (Fig. 3). Moreover, we observed no important change in the range of motion and no evidence of softening or necrosis in the eight-strand group. This finding indicates that the increased number of core strands in the eight-strand repair does not interfere with healing, as has been suggested by others⁸. Finally, the eight-strand repairs resulted in fewer tendon gaps of >1 mm. This finding is clinically important, given that we demonstrated a strong negative effect of increased gap size on tendon strength in this study as well as in an earlier study¹⁸. While it has been demonstrated previously that increasing the number of suture strands increases stiffness and strength during the first six weeks of healing^12,13, our results indicate that these beneficial effects are maintained independent of the rehabilitation force. This finding further highlights the critical importance of the repair technique in achieving and maintaining a stiff and strong repair throughout the early healing phase.

Several limitations should be noted when interpreting our findings. First, the lack of effect of the rehabilitation force on the repair site strength may have been due to an insufficient difference in force levels between the low-force and high-force groups. However, while higher force levels can be generated in the canine model with the use of electrical muscle stimulation^14,17, the passive-rehabilitation protocols that were used in this experiment were designed to replicate force levels commonly applied in clinical rehabilitation protocols^1,36-38. Comparisons of the in vivo force levels measured in the canine model^14,17 with those measured in human flexor digitorum profundus tendons^21,25 indicate that the low-force canine protocol generates an average force similar to that generated during passive wrist and digital flexion-extension in humans and that the high-force canine protocol generates a force similar to that generated during active unrestrained digital flexion in humans. Thus, the range of rehabilitation forces used in this experiment was similar to ranges that might be achieved with passive and unrestricted active-motion protocols in patients and therefore included clinically relevant levels.

A second possible limitation of our study relates to the relevance of the canine model to human flexor tendon injury and repair. While there are differences regarding nutrition and structure between canine and human intrasynovial tendons, the functional anatomy of the flexor tendon apparatus is similar, as demonstrated by similar relationships between joint rotations and tendon excursions in the two species³⁹ and by similar suture-dependent differences in initial tensile properties following repair¹⁰. Additionally, immobilization following repair of canine flexor tendons results in increased adhesion formation and reduced digital range of motion^3,28, effects that are largely prevented by early mobilization of repaired flexor tendons^9,15,40. The differences between the results of immobilization and those of early mobilization in dogs thus mimic those observed clinically^4,5,7,41. Finally, other animal models of flexor tendon injury and repair, such as the chicken^24,42 and the rabbit²⁷, do not allow for the application of clinically relevant levels of rehabilitation force, a property of the canine model that makes it well suited for the quantitative evaluation of the effects of applied postoperative force.

The lack of a significant effect of rehabilitation on tensile properties raises the issue of statistical power. Our study was designed to detect 25% differences, if they existed, between group averages at a significance level of p = 0.05 and a power level of 0.8 (beta = 0.2). Post hoc calculations indicated that the minimum detectable difference was 22% for ultimate force and 31% for rigidity, expressed as a percentage of the group average at forty-two days; these values are close to our target of 25%. Analysis of tensile properties revealed no consistent trends with respect to the effect of rehabilitation, and differences between low and high-force groups were <15% in the majority of cases. There were only two instances in which the difference between the average values for the low-force and high-force groups was >25% (strain at 20 N for eight-strand repairs at forty-two days, and strain at failure for eight-strand repairs at ten days). Therefore, we believe that our conclusion that rehabilitation had no significant effect on tensile properties was based on adequate statistical power for detecting the minimum differences that we believed might be clinically meaningful.

Several conclusions can be drawn from this study. First, application of increased levels of passive force during the early postoperative period does not appear to accelerate tendon-healing, since the time-dependent accrual of stiffness and strength was not enhanced by increasing the force levels within a clinically relevant range. Second, suture technique was of primary importance in providing a stiff and strong repair throughout the early healing interval, and the benefits of a multistrand repair were observed regardless of the level of rehabilitation force.

Combined with our previous finding that low-force rehabilitation generating 1.7 to 3.5 mm of tendon excursion in healing canine flexor tendons was sufficient to prevent adhesions and to allow a full range of motion¹⁵, our current findings suggest that there should be a reexamination of the widely held concept that increases in force and motion produced by more vigorous mobilization protocols are beneficial to tendon-healing. While more vigorous rehabilitation may help to improve hand function, we found no evidence that it enhanced tissue-healing and strength in the context of a modern suture repair. In order to increase the sensitivity of the repair site to increased force levels, it may be necessary to alter the biochemical milieu to increase expression of integrins or other force-sensitive molecules. Future strategies to accelerate tissue-healing may therefore require manipulation of both biochemical and rehabilitation variables.

Appendix

An additional table, showing range-of-motion values for canine distal and proximal interphalangeal joints and flexor tendon displacement, is available with the electronic versions of this article, on our web site (www.jbjs.org) and on our CD-ROM (call 781-449-9780, ext. 140, to order).

References

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Fig. 1-B:: Fig. 1-B The digits were then brought into full flexion.

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Fig. 1-C:: For the dogs in the low-force group, the wrist was then brought into extension while the digits were maintained in flexion. The motion cycle was then repeated (Figs. 1-A, 1-B, and 1-C).

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Fig. 1-D:: For the dogs in the high-force group, the wrist and digits were simultaneously brought into full extension. The motion cycle was then repeated (Figs. 1-A, 1-B, and 1-D).

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TABLE I: Tensile Properties of Canine Flexor Digitorum Profundus Tendons*

*The values are given as the average and the standard deviation.

Parameter	Rehabilitation	0 Days		5 Days		10 Days		21 Days		42 Days
4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand
Ultimate force (N)	Low force	48.7 ± 7.5	70.8 ± 16.6	60.7 ± 5.7	79.3 ± 7.0	49.7 ± 10.3	69.8 ± 10.3	60.7 ± 12.4	75.4 ± 24.1	102.2 ± 27.8	118.6 ± 23.6
	High force	51.3 ± 8.6	77.6 ± 11.8	52.7 ± 7.7	79.4 ± 16.6	57.3 ± 11.9	83.3 ± 9.8	95.6 ± 29.8	102.2 ± 24.6
Repair-site rigidity (N/[mm/mm])	Low force	???223 ± 88	???305 ± 91	741 ± 161	956 ± 149	612 ± 345	813 ± 273	854 ± 262	1373 ± 342	1952 ± 828	1897 ± 733
	High force	653 ± 260	884 ± 244	655 ± 196	784 ± 290	894 ± 376	1230 ± 372	2029 ± 906	2077 ± 629
Repair-site strain at 20 N (%)	Low force	12.0 ± 3.2	?9.3 ± 2.0	5.4 ± 1.0	5.4 ± 1.0	6.8 ± 2.5	5.2 ± 1.0	5.2 ± 1.6	4.4 0.9	3.2 ± 0.8	2.8 ± 0.5
	High force	6.6 ± 1.1	6.3 ± 1.2	6.3 ± 1.7	5.4 ± 1.1	5.0 ± 1.5	4.3 1.0	2.9 ± 1.2	3.7 ± 1.5
Repair-site strain at failure (%)	Low force	32.6 ± 10.5	37.7 ± 10.3	11.6 ± 2.2	12.6 ± 1.5	13.9 ± 4.4	11.4 ± 2.0	12.4 ± 3.7	10.3 3.1	7.4 ± 1.8	9.3 ± 1.9
	High force	13.5 ± 2.7	14.4 ± 2.8	12.8 ± 4.6	14.4 ± 3.3	11.2 ± 3.4	12.4 4.3	7.0 ± 1.9	8.7 ± 2.9

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TABLE I: Tensile Properties of Canine Flexor Digitorum Profundus Tendons*

*The values are given as the average and the standard deviation.

Parameter	Rehabilitation	0 Days		5 Days		10 Days		21 Days		42 Days
4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand	4-Strand	8-Strand
Ultimate force (N)	Low force	48.7 ± 7.5	70.8 ± 16.6	60.7 ± 5.7	79.3 ± 7.0	49.7 ± 10.3	69.8 ± 10.3	60.7 ± 12.4	75.4 ± 24.1	102.2 ± 27.8	118.6 ± 23.6
	High force	51.3 ± 8.6	77.6 ± 11.8	52.7 ± 7.7	79.4 ± 16.6	57.3 ± 11.9	83.3 ± 9.8	95.6 ± 29.8	102.2 ± 24.6
Repair-site rigidity (N/[mm/mm])	Low force	???223 ± 88	???305 ± 91	741 ± 161	956 ± 149	612 ± 345	813 ± 273	854 ± 262	1373 ± 342	1952 ± 828	1897 ± 733
	High force	653 ± 260	884 ± 244	655 ± 196	784 ± 290	894 ± 376	1230 ± 372	2029 ± 906	2077 ± 629
Repair-site strain at 20 N (%)	Low force	12.0 ± 3.2	?9.3 ± 2.0	5.4 ± 1.0	5.4 ± 1.0	6.8 ± 2.5	5.2 ± 1.0	5.2 ± 1.6	4.4 0.9	3.2 ± 0.8	2.8 ± 0.5
	High force	6.6 ± 1.1	6.3 ± 1.2	6.3 ± 1.7	5.4 ± 1.1	5.0 ± 1.5	4.3 1.0	2.9 ± 1.2	3.7 ± 1.5
Repair-site strain at failure (%)	Low force	32.6 ± 10.5	37.7 ± 10.3	11.6 ± 2.2	12.6 ± 1.5	13.9 ± 4.4	11.4 ± 2.0	12.4 ± 3.7	10.3 3.1	7.4 ± 1.8	9.3 ± 1.9
	High force	13.5 ± 2.7	14.4 ± 2.8	12.8 ± 4.6	14.4 ± 3.3	11.2 ± 3.4	12.4 4.3	7.0 ± 1.9	8.7 ± 2.9

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TABLE II: Tensile Properties of Canine Flexor Digitorum Profundus Tendons Depending on Gap Size*

Parameter	Gap Size
=3 mm	>3 mm
Ultimate force (N)	?74.3 ± 25.9	?48.1† ± 14.3
Repair-site rigidity (N/[mm/mm])	1129 ± 709	?525† ± 283
Repair-site strain at 20 N (%)	?5.0 ± 1.8	?7.7† ± 2.2
Repair-site strain at failure (%)	11.4 ± 3.9	15.6† ± 7.2

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TABLE II: Tensile Properties of Canine Flexor Digitorum Profundus Tendons Depending on Gap Size*

Parameter	Gap Size
=3 mm	>3 mm
Ultimate force (N)	?74.3 ± 25.9	?48.1† ± 14.3
Repair-site rigidity (N/[mm/mm])	1129 ± 709	?525† ± 283
Repair-site strain at 20 N (%)	?5.0 ± 1.8	?7.7† ± 2.2
Repair-site strain at failure (%)	11.4 ± 3.9	15.6† ± 7.2