Scandinavian Journal of Plastic and Reconstructive Surgery and Hand Surgery
ISSN: 0284-4311 (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/iphs19
Intercalary Flexor Tendon Grafts: A Morphological Study of Intrasynovial and Extrasynovial Donor Tendons Richard H. Gelberman, John G. Seiler, Andrew E. Rosenberg, Philip Heyman & David Amiel To cite this article: Richard H. Gelberman, John G. Seiler, Andrew E. Rosenberg, Philip Heyman & David Amiel (1992) Intercalary Flexor Tendon Grafts: A Morphological Study of Intrasynovial and Extrasynovial Donor Tendons, Scandinavian Journal of Plastic and Reconstructive Surgery and Hand Surgery, 26:3, 257-264, DOI: 10.3109/02844319209015268 To link to this article: http://dx.doi.org/10.3109/02844319209015268
Published online: 08 Jul 2009.
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%arid J Plast Reconstr Hand Surg 26: 257-264, 1992
INTERCALARY FLEXOR TENDON GRAFTS A Morphological Study of' Intrasynovial and Extrasynovial Donor Tendons
Richard H. Gelberman,' John G. Seiler, 111,' Andrew E. Rosenberg,2 Philip Heyman,' David A n ~ i e l , ~ From the Department of 'Orthopaedic Surgery and the Department of 'Pathology, Massachusetts General Hospital Boston, M A 02114. und the Department of 'Orthopaedics- Connective Tissue Biochemistry, University of Calgornia, La Jolla, CA 92093, USA
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(Submitted for publication November 5, 1991)
Abstract. Intercalary intrasynovial and extrasynovial flexor tendon graft donors were placed within the synovial sheaths of the medial and lateral forepaw digits of 22 dogs and treated with early controlled passive mobilization. Specimens were studied by light and transmission electron microscopy at 10 and 21 days. Early repair in the extrasynovial tendons occurred by an ingrowth of connective tissue from the digital sheath. Adhesions obliterated the gliding surface and occupied the space between the tendon's gliding surface and surrounding tissues. There was no epitenon response noted in the extrasynovial tendon grafts. While there was considerable new collagen fibril formation within the repair site at the ultrastructural level, there was a lack of longitudinal remodeling. In contrast, the intrasynovial tendon grafts showed early healing, with minimal adhesion formation, by a proliferation and migration of cells from the epitenon. These cells showed greater cellular activity and collagen production at 10 and 21 days compared to cells in extrasynovial tendons at the same intervals. The findings of this study suggest that the use of intrasynovial autogenous tendon graft donors, coupled with early controlled motion, stimulates an intrinsic repair process in both the tendon stump and autogenous tendon graft. These findings differ significantly from the experimental findings in which extrasynovial, pardtenon-covered grafts are used.
Key words: intrasynovial, extrasynovial, tendon graft, passive motion.
Previous studies have concluded that transected flexor tendons within the synovial sheath that are repaired by the tendon grafting technique and treated with total immobilization lack significant repair potential and rely primarily on the ingrowth of extrinsic vessels and cells for healing (20, 27, 36, 38,40,42). While investigators have considered the formation of mesotenon-like connections from surrounding tissues to the surface Of grafts a necessary component for healing, they have noted that adhesions to surrounding structures significantly restrict gliding
(20.36,38-40). Efforts to isolate the tendon graft from surrounding connective tissues have resulted in failure of the tendon to heal, or necrosis of the isolated tendon segment (6,20,21,25,45,46). The concept that a flexor tendon graft is a devascularized, nonviable structure that serves as a matrix for the ingrowth of viable tissue is based o n observations that transected and repaired extrasynovial, paratenon-covered homografts heal by adhesions from the periphery (9. 12). Clinically, when extrasynovial grafts are used, the formation of extensive adhesions has contributed to a high incidence of poor digital function. The number of cases which require tenolysis has been so high that recent reports have suggested that numerous operative procedures be anticipated when flexor tendon grafting is required (25). Recent studies have shown that intrasynovial flexor tendons survive initially by synovial fluid convection through a series of transverse and longitudinal canaliculae, with long-term survival dependent upon revascularization (30,31,40). The purpose of this study was to determine if the healing response of intrasynovial donor flexor tendon grafts which are morphologically and metabolically similar to recipient intrasynovial flexor tendons, differ significantly from that of extrasynovial donor autografts. The characteristics of the healing intrasynovial and extrasynovial autogenous grafts were studied by light and transmission electron microscopic techniques. MATERIAL(S) AND METHOD(S) Twenty-two adult mongrel dogs, weighing 25 to 35 kg, were used as experimental animals. A11 procedures were performed under sterile conditions in an animal operating facility. The dogs were initially anesthetized with an Scand J Piasr Reconstr Hand Surg 26
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intravenous dose of sodium Thiarnylal (0.5 cc/kg), which was supplemented by intermittent injections of Atropine (0.5 cc) and Acepromazine (0.02 cc I.M.). The animals were or0 tracheally intubated. General anesthesia was maintained with 1% Halothane and oxygen. The flexor tendons of the left second and fifth forepaw toes were approached through separate midlateral incisions. The flexor tendon sheaths were incised between the A-2 and A-4 pulleys. The flexor digitorum profundus tendon was transected distally at the level of the proximal interphalangeal joint and proximally in the region of the mesotenon attachment. Two and one-half centimeters of flexor digitorum profundus tendon was excised from each digit. Through midlateral incisions, autogenous intrasynovial flexor tendon grafts were obtained from the ipsilateral hindpaw second and fifth toes. The extrasynovial tendon grafts were harvested through a lateral leg incision isolating a 7crn segment of the peroneus longus tendon above its intrasynovial portion at the ankle. Each graft was transferred to a forepaw digit and sutured as described by Kessler et al. with 4-0 braided dacron suture under 3.5X loupe magnification (22). A 6-0 nylon epitendinous suture was subsequently placed invaginating each repair site (Fig. la). The sheath defects were not repaired. Hemostasis was obtained with an electrocautery device. The wounds were closed with a running 3-0 nylon suture. Postoperatively, the animals were placed in a polyurethane shoulder-spica cast with the elbow at 90" and the wrist at 60". The animals were divided into two groups. Group-I animals underwent flexor tendon grafting with intrasynovial flexor donor tendons. Group-I1 animals had flexor tendon grafting with extrasynovial tendon donors (Fig. 1 b). Postoperatively, all animals were treated with controlled passive motion for five minutes twice a day. For protected passive mobilization the volar one-half of the forelimb portion of the cast was cut away, the remaining
half of the cast was preserved to serve as an extension block. The wrist and digits were passively flexed and extended to the limits of the dorsal extension block 40-50 times over a five minute period twice daily beginning on the first postoperative day. Animals in both groups were euthanized at 10 and 21 days. At the time of sacrifice, the flexor apparatus was excised en-bloc from the musculotendinous junction to the base of the distal phalanx. Tendons were preserved immediately in neutral buffered formaline for standard histologic examination and in a solution of 4% peri formaldehyde and 2% glutaraldehyde for electron microscopy. The specimen orientation was held constant by application of the specimen to a modified glass slide with Keith needles. Light microscopy The specimens were bisected longitudinally to maximize visualization of the healing response and to control orientation. One-half was then processed routinely and embedded in paraffin. Sections, 5 microns thick, were cut with a conventional microtome and stained with hematoxylin and eosin for light microscopy. Transmission electron microscopy
Flexor tendon and sheath were preserved in a phosphate buffered fixative ph 7.4 for two hours and then cooled to 4°C for storage. 0.25 x 1.O x 4.0 mm samples were harvested from the repair site and at 1-2 mm intervals along the tendon graft. All samples were washed overnight in phosphate buffer and then post-fixed in a Millonig phosphate buffered 2% osmium tetroxide solution, ph 7.4. The samples were again washed in phosphate buffer before dehydration in a graded series of ethanols and propylene oxide, and then embedded in Araldite 502. Thick sections ( 1 micron) were cut and stained with methylene blue for light microscopic examination. Thin sections (60- 80
Extensor
Flexor ( Intraiynovial)
(Eatraiynovial)
Fig. 1. Schematic drawing depicting ( a ) the intercalary tendon graft; ( b ) Use of extensor (extrasynovial) and flexor (intrasynovial) autogenous tendon grafts and early controlled passive motion rehabilitation. Siiiiil
J Plus/ Rtwmvrr Hund Sirrg 26
Inlercalary ,flexor tendon grafts nanometers) were cut and mounted on formvar supported grids and stained with uranyl acetate and lead citrate. Specimens were reviewed with a Philips 301 Transmission Electron Microscope.
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RESULTS An overview of the healing process of intrasynovial and extrasynovial tendon grafts demonstrates a distinct difference between the two groups. Adhesions formed regularly between the extrasynovial tendon graft suture sites and digital sheaths by 10 days. Those tendon surfaces did not change significantly through 21 days. In contrast, the repair sites of intrasynovial tendons were either free of adhesions or had slight, filmy adhesions attached focally to the repair sites. The intercalary grafts were smooth, shiny and free of adhesions. Intrusynoviul tendon grufls of 10 days The 10 days intrasynovial tendon grafts had smooth surfaces with either no adhesions or slight, filmy adhesions attached directly to the repair site. The healing response at the repair site appeared to be originating primarily from the epitenon. The surface layer, thickened by proliferating fibroblasts and newly formed vessels, extended symmetrically along the surface of both the host tendon and intrasynovial grafts for 5-10mm (Fig. 2a). Greater than 10mm from the repair site, the epitenon thinned
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to a more normal appearing spindle to low cuboidal single cell layer covering both the graft and host tendon circumferentially (Fig. 2b). The reparative fibrovascular tissue that filled the interior portion of the repair site contained extravasated red blood cells, fibrin, small collections of lymphocytes, plasma cells, and hemosiderin laden macrophages. From the center of the repair site, newly formed vessels appeared to extend into the substance of the graft. The endotenon cells immediately adjacent to the repair site were necrotic and the collagen fibers were fragmented and haphazardly arranged with respect to the longitudinal axis of the tendon. The remainder of the graft had viable surface and central fibroblasts and normal appearing surface vessels. On electron microscopy, healthy appearing epitenon cells appeared to be migrating t o the repair site. These cells appeared active, with cytoplasmic profiles of extensive rough endoplasmic reticulum, prominent Golgi, mitochondria, and glycogen. New vessel development was confined to the area of the repair site with little evidence of vessel extension into tendon graft substance. The palmar surface of the tendon graft had woven collagen and cuboidal-appearing cells. Dorsally, there was a layer of collagen with parallel alignment and fusiform-shaped cells. Collagen adjacent to the repair site was fragmented, cells were necrotic in this region, and extravasated blood cells were present.
Fig. 2. Intrasynovial tendon graft at 10 days. (u ) The graft is to the left and flexor digitorum profundus stump to the right. Closed arrows indicate epitenon cell layer on the surface of both graft and host tendon. Open arrow denotes a vessel within the repair site; fragments of dacron core suture can be seen in the lower portion of the figure ( x 125); (b) Tapering epitenon cell layer on the surface of tendon graft, 5 mm from repair site (arrow; x 313). Sccmd J Plast Reconslr Hand Surg 26
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Fig. 3. Intrasynovial tendon graft at 21 days. ( a ) The surface is free of adhesions. The epitenon has hypertrophied and has extended over the graft into the repair site. Arrow denotes nylon suture adjacent to the repair site ( x 50); ( h ) Adhesion-free surface of the tendon graft I cm from the repair shows a single cell epitenon layer. There are viable-appearing fibroblasts within the endotenon ( x 313); (c) Mature. spindle-shaped viable fibroblasts lying between parallel arrays of collagen bundles in the center of an intrasynovial tendon graft ( x 5250).
Intrasynovial tendon grafts at 21 days
There were no surface adhesions noted along the host tendon, repair site, or tendon graft. While there were fewer cells directly over the surface of the repair compared to the 10 day specimens, the epitenon was still thickened in comparison to controls (Fig. 3a). The surface layer extended over the graft from the repair region for 5-7mm, where it gradually thinned to a single cell layer covering the remainder of the graft (Fig. 3h). Endotenon fibroblasts appeared to form new collagen fibers which were not oriented longitudinally, parallel to the longitudinal axis of the tendon. New blood vessels, extravasated red blood cells, and inflammatory cells within the repair were significantly reduced in number, compared to the 10 day specimens. On ultrastructural examination, the repair site contained cuboidal-shaped fibroblasts that were arranged in a tighter configuration than that noted at 10 days. New collagen fibrils were noted to be tightly packed between the cells. Vessels extended from the repair site into the endotenon of both the graft and the host tendon for short distances. Within the endotenon were spindle-shaped, longitudinallyoriented, viable fibroblasts lying between parallel arrays of collagen bundles (Fig. 3c). Cells of the epitenon showed junctional complexes, characteristic of migrating fibroblasts (Fig. 4). Extrusynovial tendon grufts at 10 days
Fibrovascular adhesions obliterated the interface between the digital sheath. flexor digitorum superfi-
cialis, and the tendon graft, firmly anchoring the graft to the surrounding tissues (Fig. 5 ) . Adhesions, which were circumferential and most prominent around the suture site, extended for the length of the graft proximally. The surface laycr could not be distinguished from the inflammatory scar except for small intermittent regions adjacent to the repair site where adhesions from the flexor digitorum superficialis tendons reflected onto the surface of the graft for short distances. The adhesions appeared to enter the repair site. merging with what appeared to be a dominant reparative process by endotenon fibroblasts. The endotenon was more cellular than had been noted in the intrasynovial grafts. Most of the cells at this interval were fibroblasts, haphazardly arranged and admixed with ramifying capillaries and red blood cells. Aside from the region directly bordering the repair site, where endotenon cells were necrotic, the repair site and grafts appeared viable. On electron microscopic study, fibroblasts within the repair site were producing extensive quantities of new colligen fibrils. The fibers within and adjacent to the repair were poorly organized, indicative of short-term assemblage of fibrils at the ultrastructural level (Fig. 6). Adjacent to the repair site there was a band of degenerating, loose, disoriented appearing collagen together with intermittent concentrations of cuboidal fibroblasts. Extrasynovial tendon grafis at 21 days Adhesions, still prominent, extended circumferentially around the tendon graft. The epitenon was
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Intercalary flexor tendon grafts
26 1
Fig. 5. Extrasynovial tendon graft at 10 days. Adhesions (arrow) obliterate the interspace between the flexor digitorum profundus (below) and flexor digitorurn superficialis (above). The dacron core suture (open arrow) is 7 mm from the repair site. ( x 31).
Fig. 4. Junctional complexes (arrow) were Seen fiequently in the epitenon, indicating cell coadaptation. This is indicative of cellular migration ( x 76,500).
obliterated by adhesions which blended with a predominant endotenon cellular response within the repair site (Fig. 7). The reparative tissue was composed of intersecting fascicles of fibroblasts which were oriented in a random fashion. The collagen fibers were thinner and blood vessels less numerous than that noted in the 10 day specimens. The effect of this proliferative process was a tendon graft that had a 25% greater diameter than that seen with the intrasynovial tendons at the same interval. On electron microscopy, there was an increased proliferation of fibroblasts in the repair site. These cells were viable and active in the production of new collagen. Blood vessels, which were more numerous, extended from surface adhesions into the repair site. The tendon graft adjacent to the repair had randomly oriented collagen associated with layers of fibroblasts.
DISCUSSION Recent studies have shown that active motion is frequently limited following tendon grafting
and that complications, including extensive adhesion formation, contractures, and ruptures are numerous (1, 1 I , 21,26, 36,41,43). In contrast, recent reports of total active motion following primary tendon repair and early passive motion have noted 83 to 100% good to excellent results (17, 18.28, 38,43,44). I t is surmised that the poorer results achieved with tendon grafts are due, in large part, to the fact that extrasynovial donor autogenous tendon grafts are transferred to an intrasynovial environment and treated by postoperative immobilization. Insight into the fate of extrasynovial autogenous tendon grafts has been provided by investigators studying tendon grafts that were used to replace the anterior cruciate ligament (25, 7, 8, 13, 14, 16, 23, 24, 33, 34). Four stages of autograft transformation (avascular necrosis, revascularization, cellular proliferation and remodeling), have been noted in scientific studies. Extrasynovial autografts, examined as early as two days postoperatively, showed decreased cellularity compared to the tissue of origin (14). Fibroblast configuration changed and fibroblast number diminished by 7 days. Acellularity was noted in the midsubstance of autografts by 14 days with only a peripheral rim of viable fibroblasts present. At 4 weeks, crimping was less distinct and the number of cells had decreased Srand J Plasr Reronsrr Hand Surg 26
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Fig. 7. Extrasynovial tendon graft at 21 days. An adhesion is attached to the surface of the repair site (arrow; x 50).
Fig. 6. The arrangement of collagen fibers within and adjacent to the repair site was poorly organized ( x 12,070).
dramatically. Kleiner et al. and Amiel et al. showed recently, with biochemical, autoradiographic, histological, and vascular injection techniques, that native autogenous patellar tendon grafts underwent necrosis rapidly, and that repopulation occurred from cells of extragraft origin ( 3 , 4 , 2 3 ) . Findings from our study, that both intrasynovial and extrasynovial autogenous tendon grafts placed in the synovial sheath remained viable has had recent experimental support (10, 15, 29-32). Investigators have postulated that flexor tendon grafts may survive initially by synovial fluid diffusion, with ultimate survival dependent upon revascularization ( 5 , 31,35, 36). Evidence for the effectiveness of synovial fluid diffusion comes from histological observations and studies using tritiated proline extraction techniques, a n d in vitro and in vivo culture systems (29,30). Lundborg showed that rabbit flexor tendon segments can survive without peripheral adhesion ingrowth when lying free in the synovial chamber of the knee joint (28). Lindsay and MacDougall observed fibrous tissue revascularization at the sutured ends of chicken flexor tendon grafts, but noted cellular viability without vascular or fibrous tissue invasion within the midportion of the grafts (26). Scuncl J Plusr Reronstr Hand Surg 26
Birdsell, Tustanoff, and Lindsay showed a consistent level of radioactive proline uptake by chicken flexor tendon grafts from 6 through 84 days (10). Manske et al. showed high levels of uptake of tritiated proline by free segments of flexor tendons which were detached from vascular sources, but in contact with synovium (30). Finally, Manske et al. using radioactive tracer materials to investigate the nutrition of tendon grafts, demonstrated that synovial fluid diffusion was the most important initial nutritional source for tendon grafts (30). In the current study, synovial fluid convection may have been facilitated by early controlled passive motion rehabilitation. Alternating flexion and extension of the canine digit may have stimulated the pumping of synovial fluid through the grafts. Manske et al. suggested that, while adhesions were not essential t o initial nourishment, ultimate survival was dependent upon revascularization from peripheral vascular ingrowth. It is possible that the free autogenous graft segments may have spontaneously revascularized, similar to the process of neovascularization noted with transected and repaired intrasynovial flexor tendons described recently ( 18). The repair response of the tendon grafts in this study appeared to be donor site specific. The healing of intrasynovial tendon donors took place primarily by epitenon cell proliferation and migration to the repair site. This mechanism is similar t o that notcd with repair of simple intrasynovial tendon transection and repair, followed by controlled early postopera-
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Intercalary flexor tendon grafts tive mobilization. Previous authors have confirmed a maintenance of normal morphological features in both intratendinous and surface fibroblasts when intrasynovial, rather than extrasynovial tendons, are used as graft donors. In addition, evidence of increased new collagen fibril formation by 10 days, and extensive longitudinal remodeling of collagen fibers by 3 weeks in the intrasynovial tendon grafts, suggests that these grafts are metabolically active and are contributing t o the repair process. The extrasynovial tendon graft donors, in contrast, demonstrated three consistent morphological differences from the intrasynovial donors. There was extensive adhesion formation t o the repair sites and t o the surfaces of the grafts. There was no evidence of surface cell proliferation or migration t o the repair site, and finally, the collagen that was formed within the repair site contained a haphazard orientation with respect t o the longitudinal axis of the tendon at both 10 and 21 days, despite the institution of early controlled mobilization. T h e findings of this study suggest that the use o f intrasynovial autogenous tendon graft donors, coupled with early controlled motion, stimulates an intrinsic repair process in both the distal tendon stump and autogenous donor graft. These findings differ significantly from the experimental findings in which extrasynovial, paratenon-covered grafts have I been used. If these data are confirmed in additional experimental studies, controlled clinical trials utilizing intrasynovial flexor tendon donor grafts and early controlled passive mobilization appears warranted.
ACKNOWLEDGEMENTS This study was supported by NIH Grant 5ROI-AR22097.
REFERENCES Amadio PC, Wood MB. Cooney WP, Bogard SD. Staged flexor tendon reconstruction in the figures and hand. J Hand Surg 1988; 13-A(4): 559-562. Amiel D, Abel MF. Kleiner JB, Akeson WF. Synovial fluid nutrient delivery in the diarthrial joint. An analysis of rabbit knee ligaments. J Orthop Res 1986; 4: 90-95.
Amiel D. Kleiner JB. Akeson WH. The natural history of the anterior cruciate ligament autograft of patellar tendon origin. Am J Sports Med 1986; 14(6): 449-462. Amiel D, Kuiper S. In: Daniel D, Akeson WH, OConnor J, eds. Knee Ligaments: Structure, Function, Injury and Repair: Experimental studies on anterior
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cruciate ligament grafts: Histology and biochemistry. New York: Raven Press 1990; 20: 379-388. 5 Arnoczky SP, Warren RF, Ashlock M A . Replacement of the anterior cruciate ligament using a patellar tendon allograft. J Bone Joint Surg 1986; 68-A: 376385. 6 Ashley FL, Stone RS, Alonso-Artieda
M,et al. Experimental and clinical studies on the application of monomolecular cellulose filter tubes to create artificial tendon sheaths in digits. Plast Reconstr Surg 1959; 23:
526-534. 7. Bair GR. The effect of early mobilization versus cast-
ing on anterior cruciate ligament reconstruction. Trans Orthop Res SOC1980; 5: 108. 8. Ballock RT, Woo S L-Y, Lyon RM, Hollis J. Akeson WH. Use of patellar tendon autograft for anterior cruciate ligament reconstruction in the rabbit: A long term histological and biomechanical study. J Orthop Res 1989; 7: 474-485. 9. Bergljung L. Vascular reactions after tendon suture and tendon transplantation: A stereo-microangiographic study on the calcaneal tendon of the rabbit. Scand J Plast Reconstr Surg 1968; Suppl 4: 7-63. 10. Birdsell DC, Tustanoff ER, Lindsay WK, Collagen production in regenerating tendon. Plast Reconstr Surg 1966; 37: 504.
I I . Boyes JH, Stark HH. Flexor tendon grafts in the fingers and thumb: A study of factors influencing results in 1000 cases. J Bone Joint Surg 1971; 53-A 1332- 1342. 12. Braithwaite F, Brockis JG. The vascularization of a tendon graft. Br J Plast Surg 1957; 4: 130. 13. Burks RT, Daniel DM, Losse G. The effect of continu-
ous passive motion on anterior cruciate ligament reconstruction stability. Am J Sports Med 1984; 12: 323-327. 14. deKorompay VL, Dessouki E. Vascularized versus
nonvascularized patellar tendon for intraarticular cruciate reconstruction. Histological and biomechanical analysis in dogs. Proc of Int’l SOCof the Knee. Am J Sports Med 1987; 15(4): 399. 15. Eiken 0, Lundborg G, Rank F. The role of digital synovial sheath in tendon grafting: An experimental and clinical study on autologous tendon grafting in the digit. Scand J Plast Reconstr Surg 1975; 9: 182. 16. Ferkel RD, Fox JM, DelPizzo W, et al. Reconstruction of the anterior cruciate ligament using a torn meniscus. J Bone Joint Surg 1988; 70-A(5): 715-723. 17. Gelberman RH, Nunley JA, Osterman AL, Breen TF. Dimick MP, Woo S L-Y. Influence of the protected passive mobilization on flexor tendon healing: A prospective randomized clinical study. Clin Orthop Re1 1991; 264: 189-196. 18. Gelberman RH, Khabie V. The revascularization of
healing flexor tendons within the digital sheath in dogs. J Bone Joint Surg 1991; 73-A: 868-881. 19. Gonzalez RI. Experimental tendon repair within the flexor tunnels: Use of polyethylene tubes for improvement of functional results in the dog. Surgery 1949; 26: 181 198. -
Scand J Plast Reconstr Hand Surg 26
Downloaded by [McMaster University] at 17:52 19 May 2016
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R. H . Gelberman et a/.
20. Gueukdjian SA. A new method ofcanalization of tendon sutures with vein grafts. Arch Surg 1956; 73: 1018- 1021. 21. Hunter JM, Salisbury RE. Flexor tendon reconstruction in severely damaged hands. A two-stage procedure using a silicone-dacron reinforced gliding prosthesis prior to tendon grafting. J Bone Joint Surg 1971; 53-A: 829-858. 22. Kessler I, Nissim F. Primary repair without immobilization of flexor tendon division within the digital sheath. Acta Orthop Scand 1969; 40: 587. 23. Kleiner JB, Amid D, Harwood FL, Akeson WH. Early histologic, metabolic, and vascular assessment of anterior cruciate ligament autografts. J Orthop .Res 1989; 7: 235-242. 24. Koth DR, Sewell WH. Freeze-dried arteries used as tendon sheaths. Surg Gynecol Obstet 1955; 101: 615620. 25. LaSalle WB, Strickland JW. An evaluation of the two-stage flexor tendon reconstruction technique. J Hand Surg 1983; 8: 263-267. 26. Lindsay WK, McDougall EP. Digital flexor tendons. An experimental study-111. The fate of autogenous digital flexor tendon grafts. Br J Plast Surg 1961; 13: 293. 27. Lister GD, Kleinert HE, Kutz JE, Atasoy E. Primary flexor tendon repair followed by immediate controlled mobilization. J Hand Surg 1977; 2: 441-451. 28. Lundborg G. Experimental flexor tendon healing without adhesion formation: A new concept of tendon nutrition and intrinsic healing mechanisms. A preliminary report. Hand 1976; 8: 235. 29. Manske PR, Bridwell K, Lesker PA. Nutrient pathways to flexor tendons of chickens using tritiated proline. J Hand Surg 1978; 3: 352. 30. Manske PR, Lesker PA, Bridwell K. Experimental studies in chickens on the initial nutrition of tendon grafts. J Hand Surg 1979; 4(6): 565-574. 31. Matthews P. The fate of isolated segments of flexor tendons within the digital sheath: A study in synovial nutrition. Br J Plast Surg 1976; 29: 216. 32. Newton PO, Horibe S, Woo S L-Y. In: Daniel D, Akeson WH, OConnor J, eds. Knee Ligaments: Structure, Function, Injury and Repair: Experimental studies on anterior cruciate ligament autografts and allografts: Mechanical studies. New York: Raven Press 1990; 21: 389-400.
Scctnd J Plrst Rrconstr Hand Surg 26
33. ODonoghue DH, Frank GR, Jeter GL, Johnson W. Zeiders JW, Kenyon R. Repair and reconstruction of the anterior cruciate ligament in dogs: Factors influencing long term results. J Bone Joint Surg 1971; 53-A: 710-718. 34. Peacock EE. A study of the circulation in normal tendons and healing grafts. Ann Surg 1959; 149: 415. 35. Potenza AD. The healing of autogenous tendon grafts within the flexor digital sheath in dogs. J Bone Joint Surg 1964; 46-A: 1462-1484. 36. Schneider LH. Staged flexor tendon reconstruction using the method of Hunter. Clin Orthop 1982: 171: 164- 171. 37. Smith JW. Blood supply of tendons. Am J Surg 1965; 109: 272. 38. Strickland JW, Glogovac SV. Digital function following flexor tendon repair in Zone 11: a comparison of immobilization and controlled passive motion techniques. J Hand Surg 1980; 5: 537-543. 39. Urbaniak JR, Bright DS, Gill LH, Goldner JL. Vascularization and the gliding surface mechanism of free flexor tendon grafts inserted by the silicone rod method. J Bone Joint Surg 1974; 56-A(3): 473-482. 40. Weber ER. In: Tubiana R, ed. The Hand. Volume 111: Optimizing tendon repairs within the digital sheath. Philadelphia: WB Saunders, 1988. 41. Weeks PM, Wray RC. Rate and extent of functional recovery after flexor tendon grafting with and without silicon rod preparation. J Hand Surg 1976; I : 174180. 42. Wehbe MA, Hunter JM, Schneider LH, Goodwyn BL. Two-stage flexor tendon reconstruction: Ten-year experience. J Bone Joint Surg 1986; 68-A: 752-763. 43. Werntz JR, Chesher SP, Breidenback WC, Kleinert HE, Bissonnette MA. A new dynamic splint for postoperative treatment of flexor tendon injury. J Hand Surg 1989; 14-A(3): 559-566. 44. Wheeldon T. The use of cellophane as a permanent tendon sheath. J Bone Joint Surg 1939; 21: 393-396. 45. Wilmoth CL. Tendinoplasty of the flexor tendons of the hand. Use of tunica vaginalis in reconstructing tendon sheaths. J Bone Joint Surg 1937; 19: 152-156. 46. Wilson RL, Carter MS, Holdeman VA, Lovett WL. Flexor profundus injuries treated with delayed twostage tendon grafting. J Hand Surg 1980; 5: 74-78.
ISSN: 0284-4311 (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/iphs19
Intercalary Flexor Tendon Grafts: A Morphological Study of Intrasynovial and Extrasynovial Donor Tendons Richard H. Gelberman, John G. Seiler, Andrew E. Rosenberg, Philip Heyman & David Amiel To cite this article: Richard H. Gelberman, John G. Seiler, Andrew E. Rosenberg, Philip Heyman & David Amiel (1992) Intercalary Flexor Tendon Grafts: A Morphological Study of Intrasynovial and Extrasynovial Donor Tendons, Scandinavian Journal of Plastic and Reconstructive Surgery and Hand Surgery, 26:3, 257-264, DOI: 10.3109/02844319209015268 To link to this article: http://dx.doi.org/10.3109/02844319209015268
Published online: 08 Jul 2009.
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Date: 19 May 2016, At: 17:52
%arid J Plast Reconstr Hand Surg 26: 257-264, 1992
INTERCALARY FLEXOR TENDON GRAFTS A Morphological Study of' Intrasynovial and Extrasynovial Donor Tendons
Richard H. Gelberman,' John G. Seiler, 111,' Andrew E. Rosenberg,2 Philip Heyman,' David A n ~ i e l , ~ From the Department of 'Orthopaedic Surgery and the Department of 'Pathology, Massachusetts General Hospital Boston, M A 02114. und the Department of 'Orthopaedics- Connective Tissue Biochemistry, University of Calgornia, La Jolla, CA 92093, USA
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(Submitted for publication November 5, 1991)
Abstract. Intercalary intrasynovial and extrasynovial flexor tendon graft donors were placed within the synovial sheaths of the medial and lateral forepaw digits of 22 dogs and treated with early controlled passive mobilization. Specimens were studied by light and transmission electron microscopy at 10 and 21 days. Early repair in the extrasynovial tendons occurred by an ingrowth of connective tissue from the digital sheath. Adhesions obliterated the gliding surface and occupied the space between the tendon's gliding surface and surrounding tissues. There was no epitenon response noted in the extrasynovial tendon grafts. While there was considerable new collagen fibril formation within the repair site at the ultrastructural level, there was a lack of longitudinal remodeling. In contrast, the intrasynovial tendon grafts showed early healing, with minimal adhesion formation, by a proliferation and migration of cells from the epitenon. These cells showed greater cellular activity and collagen production at 10 and 21 days compared to cells in extrasynovial tendons at the same intervals. The findings of this study suggest that the use of intrasynovial autogenous tendon graft donors, coupled with early controlled motion, stimulates an intrinsic repair process in both the tendon stump and autogenous tendon graft. These findings differ significantly from the experimental findings in which extrasynovial, pardtenon-covered grafts are used.
Key words: intrasynovial, extrasynovial, tendon graft, passive motion.
Previous studies have concluded that transected flexor tendons within the synovial sheath that are repaired by the tendon grafting technique and treated with total immobilization lack significant repair potential and rely primarily on the ingrowth of extrinsic vessels and cells for healing (20, 27, 36, 38,40,42). While investigators have considered the formation of mesotenon-like connections from surrounding tissues to the surface Of grafts a necessary component for healing, they have noted that adhesions to surrounding structures significantly restrict gliding
(20.36,38-40). Efforts to isolate the tendon graft from surrounding connective tissues have resulted in failure of the tendon to heal, or necrosis of the isolated tendon segment (6,20,21,25,45,46). The concept that a flexor tendon graft is a devascularized, nonviable structure that serves as a matrix for the ingrowth of viable tissue is based o n observations that transected and repaired extrasynovial, paratenon-covered homografts heal by adhesions from the periphery (9. 12). Clinically, when extrasynovial grafts are used, the formation of extensive adhesions has contributed to a high incidence of poor digital function. The number of cases which require tenolysis has been so high that recent reports have suggested that numerous operative procedures be anticipated when flexor tendon grafting is required (25). Recent studies have shown that intrasynovial flexor tendons survive initially by synovial fluid convection through a series of transverse and longitudinal canaliculae, with long-term survival dependent upon revascularization (30,31,40). The purpose of this study was to determine if the healing response of intrasynovial donor flexor tendon grafts which are morphologically and metabolically similar to recipient intrasynovial flexor tendons, differ significantly from that of extrasynovial donor autografts. The characteristics of the healing intrasynovial and extrasynovial autogenous grafts were studied by light and transmission electron microscopic techniques. MATERIAL(S) AND METHOD(S) Twenty-two adult mongrel dogs, weighing 25 to 35 kg, were used as experimental animals. A11 procedures were performed under sterile conditions in an animal operating facility. The dogs were initially anesthetized with an Scand J Piasr Reconstr Hand Surg 26
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intravenous dose of sodium Thiarnylal (0.5 cc/kg), which was supplemented by intermittent injections of Atropine (0.5 cc) and Acepromazine (0.02 cc I.M.). The animals were or0 tracheally intubated. General anesthesia was maintained with 1% Halothane and oxygen. The flexor tendons of the left second and fifth forepaw toes were approached through separate midlateral incisions. The flexor tendon sheaths were incised between the A-2 and A-4 pulleys. The flexor digitorum profundus tendon was transected distally at the level of the proximal interphalangeal joint and proximally in the region of the mesotenon attachment. Two and one-half centimeters of flexor digitorum profundus tendon was excised from each digit. Through midlateral incisions, autogenous intrasynovial flexor tendon grafts were obtained from the ipsilateral hindpaw second and fifth toes. The extrasynovial tendon grafts were harvested through a lateral leg incision isolating a 7crn segment of the peroneus longus tendon above its intrasynovial portion at the ankle. Each graft was transferred to a forepaw digit and sutured as described by Kessler et al. with 4-0 braided dacron suture under 3.5X loupe magnification (22). A 6-0 nylon epitendinous suture was subsequently placed invaginating each repair site (Fig. la). The sheath defects were not repaired. Hemostasis was obtained with an electrocautery device. The wounds were closed with a running 3-0 nylon suture. Postoperatively, the animals were placed in a polyurethane shoulder-spica cast with the elbow at 90" and the wrist at 60". The animals were divided into two groups. Group-I animals underwent flexor tendon grafting with intrasynovial flexor donor tendons. Group-I1 animals had flexor tendon grafting with extrasynovial tendon donors (Fig. 1 b). Postoperatively, all animals were treated with controlled passive motion for five minutes twice a day. For protected passive mobilization the volar one-half of the forelimb portion of the cast was cut away, the remaining
half of the cast was preserved to serve as an extension block. The wrist and digits were passively flexed and extended to the limits of the dorsal extension block 40-50 times over a five minute period twice daily beginning on the first postoperative day. Animals in both groups were euthanized at 10 and 21 days. At the time of sacrifice, the flexor apparatus was excised en-bloc from the musculotendinous junction to the base of the distal phalanx. Tendons were preserved immediately in neutral buffered formaline for standard histologic examination and in a solution of 4% peri formaldehyde and 2% glutaraldehyde for electron microscopy. The specimen orientation was held constant by application of the specimen to a modified glass slide with Keith needles. Light microscopy The specimens were bisected longitudinally to maximize visualization of the healing response and to control orientation. One-half was then processed routinely and embedded in paraffin. Sections, 5 microns thick, were cut with a conventional microtome and stained with hematoxylin and eosin for light microscopy. Transmission electron microscopy
Flexor tendon and sheath were preserved in a phosphate buffered fixative ph 7.4 for two hours and then cooled to 4°C for storage. 0.25 x 1.O x 4.0 mm samples were harvested from the repair site and at 1-2 mm intervals along the tendon graft. All samples were washed overnight in phosphate buffer and then post-fixed in a Millonig phosphate buffered 2% osmium tetroxide solution, ph 7.4. The samples were again washed in phosphate buffer before dehydration in a graded series of ethanols and propylene oxide, and then embedded in Araldite 502. Thick sections ( 1 micron) were cut and stained with methylene blue for light microscopic examination. Thin sections (60- 80
Extensor
Flexor ( Intraiynovial)
(Eatraiynovial)
Fig. 1. Schematic drawing depicting ( a ) the intercalary tendon graft; ( b ) Use of extensor (extrasynovial) and flexor (intrasynovial) autogenous tendon grafts and early controlled passive motion rehabilitation. Siiiiil
J Plus/ Rtwmvrr Hund Sirrg 26
Inlercalary ,flexor tendon grafts nanometers) were cut and mounted on formvar supported grids and stained with uranyl acetate and lead citrate. Specimens were reviewed with a Philips 301 Transmission Electron Microscope.
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RESULTS An overview of the healing process of intrasynovial and extrasynovial tendon grafts demonstrates a distinct difference between the two groups. Adhesions formed regularly between the extrasynovial tendon graft suture sites and digital sheaths by 10 days. Those tendon surfaces did not change significantly through 21 days. In contrast, the repair sites of intrasynovial tendons were either free of adhesions or had slight, filmy adhesions attached focally to the repair sites. The intercalary grafts were smooth, shiny and free of adhesions. Intrusynoviul tendon grufls of 10 days The 10 days intrasynovial tendon grafts had smooth surfaces with either no adhesions or slight, filmy adhesions attached directly to the repair site. The healing response at the repair site appeared to be originating primarily from the epitenon. The surface layer, thickened by proliferating fibroblasts and newly formed vessels, extended symmetrically along the surface of both the host tendon and intrasynovial grafts for 5-10mm (Fig. 2a). Greater than 10mm from the repair site, the epitenon thinned
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to a more normal appearing spindle to low cuboidal single cell layer covering both the graft and host tendon circumferentially (Fig. 2b). The reparative fibrovascular tissue that filled the interior portion of the repair site contained extravasated red blood cells, fibrin, small collections of lymphocytes, plasma cells, and hemosiderin laden macrophages. From the center of the repair site, newly formed vessels appeared to extend into the substance of the graft. The endotenon cells immediately adjacent to the repair site were necrotic and the collagen fibers were fragmented and haphazardly arranged with respect to the longitudinal axis of the tendon. The remainder of the graft had viable surface and central fibroblasts and normal appearing surface vessels. On electron microscopy, healthy appearing epitenon cells appeared to be migrating t o the repair site. These cells appeared active, with cytoplasmic profiles of extensive rough endoplasmic reticulum, prominent Golgi, mitochondria, and glycogen. New vessel development was confined to the area of the repair site with little evidence of vessel extension into tendon graft substance. The palmar surface of the tendon graft had woven collagen and cuboidal-appearing cells. Dorsally, there was a layer of collagen with parallel alignment and fusiform-shaped cells. Collagen adjacent to the repair site was fragmented, cells were necrotic in this region, and extravasated blood cells were present.
Fig. 2. Intrasynovial tendon graft at 10 days. (u ) The graft is to the left and flexor digitorum profundus stump to the right. Closed arrows indicate epitenon cell layer on the surface of both graft and host tendon. Open arrow denotes a vessel within the repair site; fragments of dacron core suture can be seen in the lower portion of the figure ( x 125); (b) Tapering epitenon cell layer on the surface of tendon graft, 5 mm from repair site (arrow; x 313). Sccmd J Plast Reconslr Hand Surg 26
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Fig. 3. Intrasynovial tendon graft at 21 days. ( a ) The surface is free of adhesions. The epitenon has hypertrophied and has extended over the graft into the repair site. Arrow denotes nylon suture adjacent to the repair site ( x 50); ( h ) Adhesion-free surface of the tendon graft I cm from the repair shows a single cell epitenon layer. There are viable-appearing fibroblasts within the endotenon ( x 313); (c) Mature. spindle-shaped viable fibroblasts lying between parallel arrays of collagen bundles in the center of an intrasynovial tendon graft ( x 5250).
Intrasynovial tendon grafts at 21 days
There were no surface adhesions noted along the host tendon, repair site, or tendon graft. While there were fewer cells directly over the surface of the repair compared to the 10 day specimens, the epitenon was still thickened in comparison to controls (Fig. 3a). The surface layer extended over the graft from the repair region for 5-7mm, where it gradually thinned to a single cell layer covering the remainder of the graft (Fig. 3h). Endotenon fibroblasts appeared to form new collagen fibers which were not oriented longitudinally, parallel to the longitudinal axis of the tendon. New blood vessels, extravasated red blood cells, and inflammatory cells within the repair were significantly reduced in number, compared to the 10 day specimens. On ultrastructural examination, the repair site contained cuboidal-shaped fibroblasts that were arranged in a tighter configuration than that noted at 10 days. New collagen fibrils were noted to be tightly packed between the cells. Vessels extended from the repair site into the endotenon of both the graft and the host tendon for short distances. Within the endotenon were spindle-shaped, longitudinallyoriented, viable fibroblasts lying between parallel arrays of collagen bundles (Fig. 3c). Cells of the epitenon showed junctional complexes, characteristic of migrating fibroblasts (Fig. 4). Extrusynovial tendon grufts at 10 days
Fibrovascular adhesions obliterated the interface between the digital sheath. flexor digitorum superfi-
cialis, and the tendon graft, firmly anchoring the graft to the surrounding tissues (Fig. 5 ) . Adhesions, which were circumferential and most prominent around the suture site, extended for the length of the graft proximally. The surface laycr could not be distinguished from the inflammatory scar except for small intermittent regions adjacent to the repair site where adhesions from the flexor digitorum superficialis tendons reflected onto the surface of the graft for short distances. The adhesions appeared to enter the repair site. merging with what appeared to be a dominant reparative process by endotenon fibroblasts. The endotenon was more cellular than had been noted in the intrasynovial grafts. Most of the cells at this interval were fibroblasts, haphazardly arranged and admixed with ramifying capillaries and red blood cells. Aside from the region directly bordering the repair site, where endotenon cells were necrotic, the repair site and grafts appeared viable. On electron microscopic study, fibroblasts within the repair site were producing extensive quantities of new colligen fibrils. The fibers within and adjacent to the repair were poorly organized, indicative of short-term assemblage of fibrils at the ultrastructural level (Fig. 6). Adjacent to the repair site there was a band of degenerating, loose, disoriented appearing collagen together with intermittent concentrations of cuboidal fibroblasts. Extrasynovial tendon grafis at 21 days Adhesions, still prominent, extended circumferentially around the tendon graft. The epitenon was
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Intercalary flexor tendon grafts
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Fig. 5. Extrasynovial tendon graft at 10 days. Adhesions (arrow) obliterate the interspace between the flexor digitorum profundus (below) and flexor digitorurn superficialis (above). The dacron core suture (open arrow) is 7 mm from the repair site. ( x 31).
Fig. 4. Junctional complexes (arrow) were Seen fiequently in the epitenon, indicating cell coadaptation. This is indicative of cellular migration ( x 76,500).
obliterated by adhesions which blended with a predominant endotenon cellular response within the repair site (Fig. 7). The reparative tissue was composed of intersecting fascicles of fibroblasts which were oriented in a random fashion. The collagen fibers were thinner and blood vessels less numerous than that noted in the 10 day specimens. The effect of this proliferative process was a tendon graft that had a 25% greater diameter than that seen with the intrasynovial tendons at the same interval. On electron microscopy, there was an increased proliferation of fibroblasts in the repair site. These cells were viable and active in the production of new collagen. Blood vessels, which were more numerous, extended from surface adhesions into the repair site. The tendon graft adjacent to the repair had randomly oriented collagen associated with layers of fibroblasts.
DISCUSSION Recent studies have shown that active motion is frequently limited following tendon grafting
and that complications, including extensive adhesion formation, contractures, and ruptures are numerous (1, 1 I , 21,26, 36,41,43). In contrast, recent reports of total active motion following primary tendon repair and early passive motion have noted 83 to 100% good to excellent results (17, 18.28, 38,43,44). I t is surmised that the poorer results achieved with tendon grafts are due, in large part, to the fact that extrasynovial donor autogenous tendon grafts are transferred to an intrasynovial environment and treated by postoperative immobilization. Insight into the fate of extrasynovial autogenous tendon grafts has been provided by investigators studying tendon grafts that were used to replace the anterior cruciate ligament (25, 7, 8, 13, 14, 16, 23, 24, 33, 34). Four stages of autograft transformation (avascular necrosis, revascularization, cellular proliferation and remodeling), have been noted in scientific studies. Extrasynovial autografts, examined as early as two days postoperatively, showed decreased cellularity compared to the tissue of origin (14). Fibroblast configuration changed and fibroblast number diminished by 7 days. Acellularity was noted in the midsubstance of autografts by 14 days with only a peripheral rim of viable fibroblasts present. At 4 weeks, crimping was less distinct and the number of cells had decreased Srand J Plasr Reronsrr Hand Surg 26
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Fig. 7. Extrasynovial tendon graft at 21 days. An adhesion is attached to the surface of the repair site (arrow; x 50).
Fig. 6. The arrangement of collagen fibers within and adjacent to the repair site was poorly organized ( x 12,070).
dramatically. Kleiner et al. and Amiel et al. showed recently, with biochemical, autoradiographic, histological, and vascular injection techniques, that native autogenous patellar tendon grafts underwent necrosis rapidly, and that repopulation occurred from cells of extragraft origin ( 3 , 4 , 2 3 ) . Findings from our study, that both intrasynovial and extrasynovial autogenous tendon grafts placed in the synovial sheath remained viable has had recent experimental support (10, 15, 29-32). Investigators have postulated that flexor tendon grafts may survive initially by synovial fluid diffusion, with ultimate survival dependent upon revascularization ( 5 , 31,35, 36). Evidence for the effectiveness of synovial fluid diffusion comes from histological observations and studies using tritiated proline extraction techniques, a n d in vitro and in vivo culture systems (29,30). Lundborg showed that rabbit flexor tendon segments can survive without peripheral adhesion ingrowth when lying free in the synovial chamber of the knee joint (28). Lindsay and MacDougall observed fibrous tissue revascularization at the sutured ends of chicken flexor tendon grafts, but noted cellular viability without vascular or fibrous tissue invasion within the midportion of the grafts (26). Scuncl J Plusr Reronstr Hand Surg 26
Birdsell, Tustanoff, and Lindsay showed a consistent level of radioactive proline uptake by chicken flexor tendon grafts from 6 through 84 days (10). Manske et al. showed high levels of uptake of tritiated proline by free segments of flexor tendons which were detached from vascular sources, but in contact with synovium (30). Finally, Manske et al. using radioactive tracer materials to investigate the nutrition of tendon grafts, demonstrated that synovial fluid diffusion was the most important initial nutritional source for tendon grafts (30). In the current study, synovial fluid convection may have been facilitated by early controlled passive motion rehabilitation. Alternating flexion and extension of the canine digit may have stimulated the pumping of synovial fluid through the grafts. Manske et al. suggested that, while adhesions were not essential t o initial nourishment, ultimate survival was dependent upon revascularization from peripheral vascular ingrowth. It is possible that the free autogenous graft segments may have spontaneously revascularized, similar to the process of neovascularization noted with transected and repaired intrasynovial flexor tendons described recently ( 18). The repair response of the tendon grafts in this study appeared to be donor site specific. The healing of intrasynovial tendon donors took place primarily by epitenon cell proliferation and migration to the repair site. This mechanism is similar t o that notcd with repair of simple intrasynovial tendon transection and repair, followed by controlled early postopera-
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Intercalary flexor tendon grafts tive mobilization. Previous authors have confirmed a maintenance of normal morphological features in both intratendinous and surface fibroblasts when intrasynovial, rather than extrasynovial tendons, are used as graft donors. In addition, evidence of increased new collagen fibril formation by 10 days, and extensive longitudinal remodeling of collagen fibers by 3 weeks in the intrasynovial tendon grafts, suggests that these grafts are metabolically active and are contributing t o the repair process. The extrasynovial tendon graft donors, in contrast, demonstrated three consistent morphological differences from the intrasynovial donors. There was extensive adhesion formation t o the repair sites and t o the surfaces of the grafts. There was no evidence of surface cell proliferation or migration t o the repair site, and finally, the collagen that was formed within the repair site contained a haphazard orientation with respect t o the longitudinal axis of the tendon at both 10 and 21 days, despite the institution of early controlled mobilization. T h e findings of this study suggest that the use o f intrasynovial autogenous tendon graft donors, coupled with early controlled motion, stimulates an intrinsic repair process in both the distal tendon stump and autogenous donor graft. These findings differ significantly from the experimental findings in which extrasynovial, paratenon-covered grafts have I been used. If these data are confirmed in additional experimental studies, controlled clinical trials utilizing intrasynovial flexor tendon donor grafts and early controlled passive mobilization appears warranted.
ACKNOWLEDGEMENTS This study was supported by NIH Grant 5ROI-AR22097.
REFERENCES Amadio PC, Wood MB. Cooney WP, Bogard SD. Staged flexor tendon reconstruction in the figures and hand. J Hand Surg 1988; 13-A(4): 559-562. Amiel D, Abel MF. Kleiner JB, Akeson WF. Synovial fluid nutrient delivery in the diarthrial joint. An analysis of rabbit knee ligaments. J Orthop Res 1986; 4: 90-95.
Amiel D. Kleiner JB. Akeson WH. The natural history of the anterior cruciate ligament autograft of patellar tendon origin. Am J Sports Med 1986; 14(6): 449-462. Amiel D, Kuiper S. In: Daniel D, Akeson WH, OConnor J, eds. Knee Ligaments: Structure, Function, Injury and Repair: Experimental studies on anterior
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cruciate ligament grafts: Histology and biochemistry. New York: Raven Press 1990; 20: 379-388. 5 Arnoczky SP, Warren RF, Ashlock M A . Replacement of the anterior cruciate ligament using a patellar tendon allograft. J Bone Joint Surg 1986; 68-A: 376385. 6 Ashley FL, Stone RS, Alonso-Artieda
M,et al. Experimental and clinical studies on the application of monomolecular cellulose filter tubes to create artificial tendon sheaths in digits. Plast Reconstr Surg 1959; 23:
526-534. 7. Bair GR. The effect of early mobilization versus cast-
ing on anterior cruciate ligament reconstruction. Trans Orthop Res SOC1980; 5: 108. 8. Ballock RT, Woo S L-Y, Lyon RM, Hollis J. Akeson WH. Use of patellar tendon autograft for anterior cruciate ligament reconstruction in the rabbit: A long term histological and biomechanical study. J Orthop Res 1989; 7: 474-485. 9. Bergljung L. Vascular reactions after tendon suture and tendon transplantation: A stereo-microangiographic study on the calcaneal tendon of the rabbit. Scand J Plast Reconstr Surg 1968; Suppl 4: 7-63. 10. Birdsell DC, Tustanoff ER, Lindsay WK, Collagen production in regenerating tendon. Plast Reconstr Surg 1966; 37: 504.
I I . Boyes JH, Stark HH. Flexor tendon grafts in the fingers and thumb: A study of factors influencing results in 1000 cases. J Bone Joint Surg 1971; 53-A 1332- 1342. 12. Braithwaite F, Brockis JG. The vascularization of a tendon graft. Br J Plast Surg 1957; 4: 130. 13. Burks RT, Daniel DM, Losse G. The effect of continu-
ous passive motion on anterior cruciate ligament reconstruction stability. Am J Sports Med 1984; 12: 323-327. 14. deKorompay VL, Dessouki E. Vascularized versus
nonvascularized patellar tendon for intraarticular cruciate reconstruction. Histological and biomechanical analysis in dogs. Proc of Int’l SOCof the Knee. Am J Sports Med 1987; 15(4): 399. 15. Eiken 0, Lundborg G, Rank F. The role of digital synovial sheath in tendon grafting: An experimental and clinical study on autologous tendon grafting in the digit. Scand J Plast Reconstr Surg 1975; 9: 182. 16. Ferkel RD, Fox JM, DelPizzo W, et al. Reconstruction of the anterior cruciate ligament using a torn meniscus. J Bone Joint Surg 1988; 70-A(5): 715-723. 17. Gelberman RH, Nunley JA, Osterman AL, Breen TF. Dimick MP, Woo S L-Y. Influence of the protected passive mobilization on flexor tendon healing: A prospective randomized clinical study. Clin Orthop Re1 1991; 264: 189-196. 18. Gelberman RH, Khabie V. The revascularization of
healing flexor tendons within the digital sheath in dogs. J Bone Joint Surg 1991; 73-A: 868-881. 19. Gonzalez RI. Experimental tendon repair within the flexor tunnels: Use of polyethylene tubes for improvement of functional results in the dog. Surgery 1949; 26: 181 198. -
Scand J Plast Reconstr Hand Surg 26
Downloaded by [McMaster University] at 17:52 19 May 2016
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20. Gueukdjian SA. A new method ofcanalization of tendon sutures with vein grafts. Arch Surg 1956; 73: 1018- 1021. 21. Hunter JM, Salisbury RE. Flexor tendon reconstruction in severely damaged hands. A two-stage procedure using a silicone-dacron reinforced gliding prosthesis prior to tendon grafting. J Bone Joint Surg 1971; 53-A: 829-858. 22. Kessler I, Nissim F. Primary repair without immobilization of flexor tendon division within the digital sheath. Acta Orthop Scand 1969; 40: 587. 23. Kleiner JB, Amid D, Harwood FL, Akeson WH. Early histologic, metabolic, and vascular assessment of anterior cruciate ligament autografts. J Orthop .Res 1989; 7: 235-242. 24. Koth DR, Sewell WH. Freeze-dried arteries used as tendon sheaths. Surg Gynecol Obstet 1955; 101: 615620. 25. LaSalle WB, Strickland JW. An evaluation of the two-stage flexor tendon reconstruction technique. J Hand Surg 1983; 8: 263-267. 26. Lindsay WK, McDougall EP. Digital flexor tendons. An experimental study-111. The fate of autogenous digital flexor tendon grafts. Br J Plast Surg 1961; 13: 293. 27. Lister GD, Kleinert HE, Kutz JE, Atasoy E. Primary flexor tendon repair followed by immediate controlled mobilization. J Hand Surg 1977; 2: 441-451. 28. Lundborg G. Experimental flexor tendon healing without adhesion formation: A new concept of tendon nutrition and intrinsic healing mechanisms. A preliminary report. Hand 1976; 8: 235. 29. Manske PR, Bridwell K, Lesker PA. Nutrient pathways to flexor tendons of chickens using tritiated proline. J Hand Surg 1978; 3: 352. 30. Manske PR, Lesker PA, Bridwell K. Experimental studies in chickens on the initial nutrition of tendon grafts. J Hand Surg 1979; 4(6): 565-574. 31. Matthews P. The fate of isolated segments of flexor tendons within the digital sheath: A study in synovial nutrition. Br J Plast Surg 1976; 29: 216. 32. Newton PO, Horibe S, Woo S L-Y. In: Daniel D, Akeson WH, OConnor J, eds. Knee Ligaments: Structure, Function, Injury and Repair: Experimental studies on anterior cruciate ligament autografts and allografts: Mechanical studies. New York: Raven Press 1990; 21: 389-400.
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33. ODonoghue DH, Frank GR, Jeter GL, Johnson W. Zeiders JW, Kenyon R. Repair and reconstruction of the anterior cruciate ligament in dogs: Factors influencing long term results. J Bone Joint Surg 1971; 53-A: 710-718. 34. Peacock EE. A study of the circulation in normal tendons and healing grafts. Ann Surg 1959; 149: 415. 35. Potenza AD. The healing of autogenous tendon grafts within the flexor digital sheath in dogs. J Bone Joint Surg 1964; 46-A: 1462-1484. 36. Schneider LH. Staged flexor tendon reconstruction using the method of Hunter. Clin Orthop 1982: 171: 164- 171. 37. Smith JW. Blood supply of tendons. Am J Surg 1965; 109: 272. 38. Strickland JW, Glogovac SV. Digital function following flexor tendon repair in Zone 11: a comparison of immobilization and controlled passive motion techniques. J Hand Surg 1980; 5: 537-543. 39. Urbaniak JR, Bright DS, Gill LH, Goldner JL. Vascularization and the gliding surface mechanism of free flexor tendon grafts inserted by the silicone rod method. J Bone Joint Surg 1974; 56-A(3): 473-482. 40. Weber ER. In: Tubiana R, ed. The Hand. Volume 111: Optimizing tendon repairs within the digital sheath. Philadelphia: WB Saunders, 1988. 41. Weeks PM, Wray RC. Rate and extent of functional recovery after flexor tendon grafting with and without silicon rod preparation. J Hand Surg 1976; I : 174180. 42. Wehbe MA, Hunter JM, Schneider LH, Goodwyn BL. Two-stage flexor tendon reconstruction: Ten-year experience. J Bone Joint Surg 1986; 68-A: 752-763. 43. Werntz JR, Chesher SP, Breidenback WC, Kleinert HE, Bissonnette MA. A new dynamic splint for postoperative treatment of flexor tendon injury. J Hand Surg 1989; 14-A(3): 559-566. 44. Wheeldon T. The use of cellophane as a permanent tendon sheath. J Bone Joint Surg 1939; 21: 393-396. 45. Wilmoth CL. Tendinoplasty of the flexor tendons of the hand. Use of tunica vaginalis in reconstructing tendon sheaths. J Bone Joint Surg 1937; 19: 152-156. 46. Wilson RL, Carter MS, Holdeman VA, Lovett WL. Flexor profundus injuries treated with delayed twostage tendon grafting. J Hand Surg 1980; 5: 74-78.
