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Effects of hydroxyapatite and alumina sheaths on postoperative peritendinous adhesions in chickens

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Two experimental methods for restoring flexor tendon sheath integrity and preventing adhesions around traumatized flexor tendons utilizing artificial tendon sheaths made of either hydroxyapatite (HAp) or alumina were studied in a flexor tendon-trauma
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  Effects of Hydroxyapatite and Alumina Sheaths on Postoperative Peritendinous Adhesions in Chickens Najam A. Siddiqi,* Yoshiki Hamada,t Takatoshi Ide,t and Noriya Akamatsut zyx Department of Orthopedic Surgery, Johns Hopkins University School of Medicine, Baltimore, Maryland and +Department of Orthopedic Surgery, Yamanashi Medical University, Japan zyxwvut Two experimental methods for restoring flexor tendon sheath integrity and preventing adhe- sions around traumatized flexor tendons utilizing artificial tendon sheaths made of either hy- droxyapatite (HAp) or alumina were studied in a flexor tendon-trauma model and compared to a standard tendon sheath repair and a control. Eighty toes were divided equally into a control group, a sheath repair group, an HAp group, and an alumina group. Profundus tendons in zone zy 1 were divided and repaired after sublimis excision in all groups. In the sheath repair group, the flexor sheath was also repaired after suturing the tendon. In artificial sheath groups, sheaths made of HAP and alumina were placed over the repair sites to protect them from the surrounding tissues. In the control group, after repairing the tendon, the flexor sheath was excised and no artificial sheaths were used. Each toe was immobilized in a plaster cast for 3 weeks. After three weeks, the plaster cast was removed followed by the removal of the sheaths in the artificial sheath groups through a small incision in the skin in zone 11. Active mobilization was encouraged in each group. Postoperative adhesions were examined at 3 6 9 and 12 week intervals by using light microscopic techniques. To further explore the effects of artificial sheaths on tendon healing, transmission electron microscopy was done for the HAp and alu- mina groups at 3 6 and 2 week intervals. Results demonstrated decreased severity of postop- erative adhesions in the HAp as well as in the alumina groups in comparison with the sheath repair and controls. A space resembling the fibro-osseous canal was formed around the tendon after removing the sheaths. This space remained patent until 12 weeks, 9 weeks after removing the sheaths, and a newly formed tendon sheath-like structure lined by synovial cells and with a peritenon-like structure over the tendon surface was observed. In the sheath repair and control groups, the severity of adhesions was decreased with the passage of time, to some extent due to unrestricted mobility. However, a newly formed tendon sheath or peritenon-like structure was not observed. Electron microscopic studies confirmed good healing at the suture in the HAp and alumina groups with no evidence of necrosis. These results are qualitative in nature as no statistical tests were performed. From these results we conclude that if the tendon is separated from the surrounding granulation tissue by a barrier with good biocompatibility, the tendon can heal with fewer adhesions. Artificial sheaths may be used to reduce adhesions in severe injuries of the hand where postoperative immobilization is necessary due to fractures, vascular, or nerve injuries. zyxwvuts   995 John Wiley Sons Inc. INTRODUCTION Hand injuries often result in lacerated flexor tendons and sheaths in zone 11. The restoration of normal function af- ter these injuries is often unsatisfactory because of the for- mation of adhesions around the repair site that restrict the gliding of the tendons. These peritendinous adhesions de- velop due to the healing of the tendon, subcutaneous tis- sue, and the skin as a single compartment because there is no barrier between these tissues. The result is contracture Requests for reprints should be sent to Najam A. Siddiqi, M.D., Ph.D., Dept. of Orthopedic Surgery, Johns Hopkins University School of Medicine, The Ross Research Building, 720 Rutland Ave., Baltimore, MD 2 1205. Journal of Applied Biomaterials. Vol. zyxwvutsrq .43-53 (1995) 995 ohn Wiley Sons, Inc. CCC 1045-4861/95/010043-1 formation and decreased range of motion of the digit. Al- though anatomic repair of the tendon sheath would seem to restore the normal environment for tendon gliding, nar- rowing of the fibro-osseous canal (FOC) restricts tendon gliding.'-4 Sometimes repairing the sheath is not possible either due to large defects in the substance of the sheath after injury or it is crushed so badly that it has to be re- sected. Attempts have been made in the past to protect the te- norrhaphy site by using many types of barriers such as fas- cia,' fat, pentenon, stainless steel sheaths, silastic sheaths,6 veins, polyethylene tubes,' cellulose filter tubes (Milli- pore-Microweb sheaths),8 Teflon,@,' silicone rubber enve- lopes, tantalum foil, synthetic polytetraflorethylene (PTFE) surgical membrane3 etc., but none of these meth- ods proved to be clinically successful. This study attempts to decrease postoperative flexor tendon adhesions by using tunnel shaped barriers made of 43  44 zyxwvusrqpo IDDIQI zyxwvu T AL. 4 0mm Alumina artificial Hydroxyapatite artificial tendon sheath tendon sheath Figure 1 zyxwvuts ydroxyapatite and alumina sheaths. either HAp or alumina and to compare these results to controls of flexor sheath repair or excision. Synthetic hy- droxyapatite ceramic was chosen for this experiment be- cause it has been recently developed as a biomaterial and has been noted for its excellent biocompatibility and os- teoconduction when employed in bone tissue. -I4 Peri- tendinous adhesions were evaluated by studying the inter- faces between the artificial sheaths, tendons, and the sub- cutaneous tissues. Furthermore, to assess the degree of healing at the suture site, electron microscopic studies were also conducted. MATERIALS AND METHODS Tunnel-shaped HAp (Bone cearum-P) and alumina test pieces were prepared (Sumotomo Pharmaceutical Com- pany) measuring 15 mm in length, 1 mm in thickness and 2 mm in inner diameter (Fig. l), according to the size of the chicken tendon. The HAp was prepared by the wet method by mixing (H,PO,) into a container containing calcium hydroxide (CA(OH)2). 10Ca(OH)2 + 6H3P04 t Ca 10(P04)6(OH)2 + 18H20. The mixture was thoroughly mixed with the help of a pro- peller and the HAp was then collected on a mesh filter. The powder was dried to obtain HAp and the powder was then filled under compression in special containers shaped like a tunnel to form the test pieces. Pores were obtained by mixing polymethylmethacrylate (PMMA) in the HAp powder. After the tunnel was formed, the PMMA was burned under high temperature to form pores. The size of the pores (200-250 pm) depended on the size of the PMMA. The test pieces were then sintered at 1 150 C for 3 h. Eighty tendons (40 chickens) of the middle digits of white, adult female Leghorn chickens weighing an average of 1.2 kg were randomly selected for this experiment. Each tendon was assigned to the specific group according to the nature of the treatment it received. No blinding was in- volved either at the time of surgery nor at the evaluation. Operative Technique Anesthesia was achieved with pentobarbital 1 mL/kg body weight (Nembutal 50 mg/mL), administered intramuscu- larly and the operation was conducted using aseptic tech- niques. A zigzag volar incision was made on the planter surface of the foot starting from zone zy   and extending to the distal interphalangeal joint. Subcutaneous tissues were dissected to expose the flexor sheath. Eighty digits were equally divided into four groups: control group, 20 toes: sheath repair group, 20 toes; HAp group, 20 toes; and alu- mina group, 20 toes. In the control group the flexor sheath was excised between the proximal and distal pulleys in  HYDROXYAPATITE AND ALUMINA SHEATHS 45 Figure 2. zyxwvutsrqp A) HAp sheath placed over the site of tenorrhaphy. (B) After removing the sheath at 3 weeks, good healing at the suture site without adhesions to the surrounding tissues were observed, however, mild adhesions to the bony floor and at the ends of the sheath were observed. (C) Alumina sheath cov- ering the site of tenorrhaphy. (D) At 3 weeks after removing he sheath good healing with fewer adhesions between the ventral surface of the tendon and the surrounding tissues was evident, however, mild to moderate adhesions to the bony floor and the ends of the sheath were observed. zone zyxwvuts   to create a window in the FO tunnel, and the pro- fundus tendon was exposed by resecting the sublimis ten- don. The profundus tendon was then severed proximal to the vinculum longus and repaired by Tsuge's tech- niq~e,'~.'~ sing 5-0 nylon suture. The skin was then closed without repairing the tendon sheath. The tendon sheath repair group differed from the control group in that the sheath was carefully incised between the proximal and distal pullies and after suturing the profundus tendon the sheath was repaired using continuous 7-0 Prolene suture. In the HAp and alumina groups, the flexor sheath was re- sected between the proximal and distal pulleys and the HAP and alumina sheaths were then placed over the te- norrhaphy site to close the window in the FO tunnel cov- ering the proximal and distal pulleys [Fig. 2(a,c)]. Fixation of the sheaths was achieved by suturing the subcutaneous tissue over them with zyxwvutsrq  0 Dexon. Care was taken not to displace the tunnel from the tendon nor to allow gaps be- tween the tunnel and the dorsal phalanx. In all of the groups after suturing the skin, the toes were immobilized in a plaster cast for zyxwvutsrq   weeks in a tension-reducing position (flexion). The casts were applied so that the tunnel could remain in position without any movement. The casts were removed 3 weeks after the operation in each group, and in the HAp and alumina groups the sheaths were removed through a small skin incision. The digits in each group were then allowed to move unrestricted. Chickens were sacrificed at 3, 6, 9, and 12 week in- TABLE 1 Tendon Sheath Repair (TSR) and Excision Control) Groups Weeks Severe Moderate Mild Postop Groups (>66 ) (66-33 ) (<33 ) None 3 Control 5 0 0 0 TSR 2 3 0 0 6 control 4 1 0 z SR 2 3 0 0 9 Control 3 2 0 0 TSR 3 1 0 12 Control 2 3 0 0 TSR 0 3 2 Groups were quantified according to four-grade classification. Ten slides were prepared at 2-mm intervals for each specimen, and the area of tendon with adhe- sions was estimated. Each slide was graded and the average grade from 10 slides was finally used to assign a grade to each digit.  46 zyxwv IDDIQI zyxwvu T AL. Figure 3. zyxwvutsr   Weeks: (A) Control group: severe adhesions (Ad) between the tendon T) and the surround- ing tissues (ST). (B) Sheath repair group: severe adhesions could be observed between the tendon, sheath (ts), and the surrounding tissues (H E stain x40). (C) HAp sheath group: after removing the sheath, a wide space could be observed between the tendon and the surrounding tissues lined by a layer of cells. (D) Alumina sheath group: almost the same findings as in the HAp group. tervals providing five specimens in each group. The digits of the chickens were resected at metacarpophalangeal and proximal interphalangeal joints thus localizing the suture site approximately in the center of the specimens. Each specimen was divided into two equal halves (dividing line close to the suture site). Ten slides were prepared at 2-mm intervals, five sections on each half of the specimen, start- ing from the suture side. All specimens were fixed in for- malin and decalcified. Histological sections were stained with hematoxylin and eosin (H&E) stain and the area of tendon ventral surface with adhesions was estimated. Ad- hesions were classified into four grades on the basis of this histological study (cross sections): severe, adhesions > 66% of the tendon ventral surface; moderate, adhesions between 66-33% of the ventral surface; mild, adhesions < zyxwvutsr 3 of the ventral surface; and none, no adhesions. A final grade of adhesion severity was assigned to each ten- don based on the average grade derived from examination of all 10 sections. Adhesion formation on the dorsal sur- face of the tendon was excluded from the study because there was no sheath used between the tendon and the pha- lanx. This study is qualitative in nature because no statis- tical analysis was performed. To study the healing process at the cellular level after using artificial sheaths and especially to assess necrosis at the suture site, another series of 24 chickens flexor tendons was equally divided into HAp and alumina groups. The same operation was performed as described above and two chickens from each group were sacrificed at 3, 6, and 12 week intervals, giving us two specimens each for the HAp and alumina groups at each interval. All specimens were obtained at the junction of the repaired ends of the ten- dons and were prepared for electron microscopic exami- nation. The specimens were washed for several days in so- dium cacodylate buffer (pH 7.4) followed by dehydration through a graded series of ethanol and propylene oxide. The specimens were then embedded in Epon 812, thin sections were stained in uranyl acetate and lead citrate, and then viewed using a JEM- 1 OOSX electron microscope (JEOL Co. Ltd., Japan). RESULTS Control Group At 3 weeks, macroscopic examination of the tendons showed them to be covered by thick granulation tissue forming strong adhesions to the surrounding tissue as well as to the bony floor. Histological findings revealed severe adhesions (>66%) between the tendon ventral surface and the surrounding connective tissue thus obliterating the  HYDROXYAPATITE AND ALUMINA SHEATHS 47 Figure 4. zyxwvutsrqp   Weeks: (A) Control group showing adhesions (Ad). 8) Sheath repair group: the tendon sheath (ts) still showed adhesions to the tendon zyxwvu H E stain x40). (C) HAp sheath group: wide space between he tendon T) and the surrounding tissues ST) so called fibro-osseous canal is well preserved even after removing the sheath at 3 weeks. Marked proliferation of cells on the surface and in the sub- stance of the tendon and a layer of synovial cells lining the surrounding tissues could be observed. (D) Alumina sheath group: he space formed at 3 weeks was still patent, however, proliferation of endotenon and epitenon cells were less marked FOC [Table I, Fig. 3(a)]. The invasion of granulation tis- sue into the tendon was also observed. From 6 to 9 weeks, the severity of adhesions was de- creased to some extent (moderate adhesions 66-33%) due to unrestricted mobility, however, the FOC was not totally reformed and synovial tissue on the tendon surface was not apparent [Fig. 4(a)]. Even at 12 weeks moderate adhe- sions could be observed [Table I, Fig. 5(a)]. Tendon Sheath Repair Group Macroscopic examination at 3 weeks revealed adhesions around the repair site. The tendon sheath was adherent to the surrounding tissues and the tendon obliterating the FOC. Histologically moderate adhesions (66-33%) were apparent between the repair sheath, tendon ventral sur- face, and the surrounding tissues [Fig. 3(b)]. From 9 to 12 weeks, mild to moderate adhesions (Table zyxwvu   could be observed and the FOC was partially reformed. However no synovial cells could be seen lining the sheath [Figs. 4(b), 5(b)]. Furthermore, proliferation of peritenon structure on the tendon surface was also absent. At each period studied, adhesions were less severe than those found in the control group. HAp Group Macroscopic examination at 3 weeks revealed that the HAp sheath was not adherent to either the tendon or the surrounding tissues; however, it was covered by a thin layer of granulation tissue. Although there were mild ad- hesions at the two ends of the sheaths, the sheath was re- moved easily by pulling it from one end (Table 11). In some cases, a thin layer of granulation tissue covered the tendon surface; however, in all cases, proliferation of gran- ulation tissue was more marked at the sheath edges. The tendon was adherent to the bony floor at some places be- cause no sheath was used to separate the tendon from the shaft of the phalanx [Fig. 2(b)]. After removing the HAp sheath at 3 weeks, micro- scopic examination around the traumatized tendon re- vealed multilayer cells through the entire length of the ten- don surface protected by the HAp sheath, including the repair site [Fig. 3(c)]. A wide gap formed after the HAp sheath was removed that separated the tendon from the surrounding tissues; the outer boundary of this space was lined by a single layer of cells and a collagenous structure resembling newly formed tendon sheath [Fig. 3(c)]. A thin layer of granulation tissue over the HAp sheath indicated
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