The Pathology o f Hexor Tendon Repair Phillip Matthews
T H E P A T H O L O G Y OF F L E X O R T E N D O N R E P A I R P H I L L I P M A T T H E W S , Swansea SUMMARY This paper discusses the problems of failure after tendon repair. For a long time the subject has been dominated by the problem of adhesion formation. Recent work has s h o w n that this is not inevitable, and consideration of other factors, particularly the nutrition of tendon tissue is leading to the possibilities of other methods of treatment. INTRODUCTION Few surgeons dealing with hand t r a u m a would disagree that the cut digital flexor tendon still poses a most difficult problem in management. Over the past half century, controversy has continued as to the most suitable form of treatment with the trend swinging firstly from suture towards delayed tendon grafting and then, in recent years, back to direct repair. Apart from such radical changes of concept, the literature has abounded with various technical innovations, each claimed, in its turn, to improve the outlook after surgical treatment. It would be foolish to deny that there have been significant steos forward in the management o f flexor tendon injuries, but it would be equally wrong to assume that we have yet reached the stage where treatment is ideal. From even the best centres the reported results of treatment are deemed satisfactory in only, perhaps, seventy-five per cent of cases, but on the other side of the coin, this still leaves an unhappy twenty-five per cent who, aftei" months of treatment, are left with impaired hand function and permanent disability. It might be expected that in less specialised units the results of surgery would leave even more to be desired. The situation certainly leaves no r o o m for complacency and much effort will be needed if we are to make further progress in the management o f this difficult injury. As the first step in this, it would seem essential that we apt/reciate the processes which are involved in tendon physiology and healing and from here recognize why it is that current methods of treatment are still inadequate. FACTOR CAUSING DIFFICULTY Whereas simple methods of repair generally yield good results in the extensor tendons of the hand and most other sites in the body the same cannot be said o f the digital flexor tendons. This is due in large extent to complexities o f the anatomical and functional arrangement peculiar to the flexor tendons and once these are fully understood it is no longer surprising that their surgical repair should so often fail to restore active flexion. The amplitude o f motion of the flexor tendons is long-nearly twice that of the extensors - - and this and their close proximity to the ohalan~es has demanded a specialised anatomical arrangement with a synovial lined fibro-osseous sheath and strategically placed pulleys to prevent bow-stringing. The tendons must be capable of withstanding very high tension during muscle contraction and, at the same time, of undergoing repeated angular distortions during finger flexion and extension. It must also be borne in mind that since the tendons are living structures with metabolic needs, provision has to be made for their nourishment and Phillip Matthews, F.R.C.S. (Edinburgh), F.R.C.S. (England). St. David's House, 1, Uplands Terrace, Uplands, Swansea. The Hand--Volume 11
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Fig. 1. Longitudinal section through the healing area of a cut flexor tendon at eight days. In the lower part of the illustration (A) are intact tendon fibres which had been left in continuity during the incomplete transection procedure. On a more superficial plane there is a zone of very active tenoblast proliferation (B) which is later responsible for bringing about repair of the defect. (Haemotoxylin and eosin x 480) movement simultaneously. Although there was a time when tendons were thought to be avascular, this is now known to be incorrect and that, although it may be slow, there is a definite bloodflow through tendon tissue. Numerous accounts have been published describing the vascular arrangements of the flexor tendons and the intricacies of the extrinsic and intrinsic circulations are well recognized. In addition to the bloodflow there is also evidence that diffusion of metabolites across the synovial fluid is involved in the nutrition of the tendon in a manner analogous to joint cartilage nutrition. (Potenza 1963, Eiken, Lundborg and Rank 1975, Matthews 1976). The significance of this synovial mode of nutrition is still a matter of speculation, though it seems likely to be more important for the superficial and volar parts of the tendon and necessary to ensure its nutrition during phases of prolonged tension in the tendon when its blood circulation may be compromised. Lundborg and Myrhage (1977) have extended the analogy to joint cartilage nutrition and compare the flexor system to a specialised joint, sliding longitudinally and exhibiting an extremely long range of motion. Whether this comparison is valid or not, the flexor apparatus is certainly superbly designed for function and it is readily understandable why repair after injury should pose so much of a problem. FORMATION & ADHESIONS
It was long ago realized that the usual cause o f failure to restore normal active movement after repair of divided flexor tendons was the development of adhesions 234
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Fig. 2. Longitudinal section through the cut end of a h u m a n digital flexor tendon three weeks after the injury. The s t u m p was found lying free o f adhesions within an undisturbed area o f the synovial sheath. Note that the cut tendon fibres (A) are capped with a highly cellular tissue (B) consisting mainly of fibroblasts. Through the deposition o f new collagen fibres the s t u m p becomes remodelled into a smoothly rounded form. (Haemotoxylin and eosin x 70)
between the site of suture and the surrounding fibrous and bony structures. The tethering effect of the resulting scar blocked the essential gliding motion of the tendon and thus rendered active finger flexion impossible. This clinical predicament stimulated interest in the subject of tendon healing and led to the experimental study of the processes involved. Of the numerous facets of this research, the one which caused most debate concerned the origin of the cells responsible for healing of the injured tendon. One of the most important contributions in this field was that of Austin Potenza (1962), then a captain in the United States Army, into the mode of healing of flexor tendons in the dog. After detailed and meticulous studies, he was able to demonstrate conclusively that when a severed tendon was repaired by suture and then immobilised, healing came about through the ingrowth of granulation tissue derived from outside the tendon. It was noted that there was an intense proliferation of the tissues surrounding the tendon and the resulting adhesions matured to a fibrous scar which restored tendon continuity. During this process the tendon tissue itself remained inert and Potenza inferred from this that it lacked any intrinsic healing properties of its own. Potenza's work on tendon healing had certain fundamental clinical implications. If tendon lacks any properties of repair then it must be entirely reliant on the formation of adhesions in order to heal. On this basis, adhesions, however undesirable they might be, would be essential for union of the tendon and inevitable irrespective of the degree of surgical skill or the ingenuity of the method of repair The Hand-- Volume l l
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Fig. 3. Injection specimen of stump of a rabbit profundus tendon four weeks after simple tenotomy~ The cut end has become a little swollen, but the most striking feature is the greatlyincreased vascularity of the tip due to the formation of many fine new blood vessels. (Colloidal silver-iodidetechnique) Fig. 4. Injection specimen of adherent stump of rabbit profundus tendon three weeks after simple tenotomy. The tendon itself is avascular, but within the adhesion formed at its tip there is a leash of new blood vessels running towards the tendon and representing, presumably, an attempt to bring about its revascularization. (Colloidal silver-iodidetechnique) e m p l o y e d . This c o n c e p t , i n c i d e n t a l l y , was to p r o v i d e s t r o n g t h e o r e t i c a l s u p p o r t for t h e a d v o c a c y o f d e l a y e d g r a f t i n g r a t h e r t h a n r e p a i r in the m a n a g e m e n t o f flexor tendon injuries. PREVENTION OF ADHESION A l t h o u g h P o t e n z a ' s e x p e r i m e n t a l findings a r e a c c e p t e d , his c o n c l u s i o n t h a t the t e n d o n l a c k s a n y c a p a c i t y for r e p a i r has c o m e u n d e r challenge. It has been p o i n t e d o u t t h a t t h e p r e s e n c e o f such f a c t o r s as s u t u r e a n d s p l i n t a g e in his s t u d y m a y have a d v e r s e l y a f f e c t e d t h e r e p a i r p r o c e s s a n d the a i m o f recent studies has been to e x a m i n e t e n d o n h e a l i n g u n d e r m o r e ideal c o n d i t i o n s . These later e x p e r i m e n t s , ( M a t t h e w s a n d R i c h a r d s 1974, M c D o w e l l a n d S n y d e r 1977), using r a b b i t s a n d d o g s , h a v e e m p l o y e d t h e t e c h n i q u e o f i n c o m p l e t e t e n d o n division in o r d e r to exclude the effects o f e x t r a n e o u s f a c t o r s w h i c h m i g h t a f f e c t t h e healing p r o c e s s . But c u t t i n g a l m o s t , b u t n o t quite, t h r o u g h the t e n d o n , the need to suture m e ends t o g e t h e r a n d 236
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Fig. 5. Healing of an injured flexor tendon in the presence of suture, sheath excision, and immobilisation. The area of injury has become enveloped in a dense scar which prevents all useful movement. then to i m m o b i l i s e the digit c o u l d be a v o i d e d . In a d d i t i o n , the m e t h o d o f e x p o s i n g the t e n d o n in the e x p e r i m e n t s was so d e s i g n e d t h a t h e a l i n g o f the cut was a b l e t o t a k e p l a c e w i t h i n an u n d i s t u r b e d a r e a o f the f i b r o - s y n o v i a l s h e a t h . A t v a r y i n g intervals a f t e r the o p e r a t i o n the a n i m a l s were killed a n d the i n j u r e d t e n d o n s e x a m i n e d . It was f o u n d t h a t in all cases the w o u n d in the t e n d o n s h e a l e d in g r a d u a l l y a n d , c o n t r a r y to w h a t m i g h t have been e x p e c t e d if P o t e n z a ' s t h e o r y were correct, no a d h e s i o n s f o r m e d . I n s t e a d , the g a p b e t w e e n the cut t e n d o n fibres filled in steadily f r o m q t s base with a glistening, t r a n s l u c e n t r e p a i r tissue, which, in t i m e ,
Fig. 6. Injection study of cut profundus tendon two days after suture. There is failure of filling of the blood vessels within the sutured zone. (Colloidal silver-iodidetechnique) The Hand--Volume 11
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Fig. 7. Longitudinalsection through a severed profundus tendon four days after it has been apposed by a Bunnell type suture of fine braided Dacron. The fibres of the suture material are readily visible in the lower left of the photograph. Note the relative paucity of tenocytes in the vicinity of the suture. Under higher power microscopy, even those cells which still remain show severe degenerative changes. (Haemotoxylin and eosin x 182) matured so that by the end of the experiment the macroscopic appearances of the tendon were normal. The repair tissue appeared, histologically, to be derived from the tenocytes through their transformation into active tenoblasts which then proliferated and synthesised new collagen fibres. (Fig. 1). These studies have shown that, under certain specified experimental conditions, flexor tendon, as a tissue, possesses properties of repair and remodelling and is able to heal defects in its structure without adhesion formation. It is important to appreciate, however, that one cannot infer from the results that totally divided tendons might also be made to join without adhesions. As will later become apparent, there are practical reasons why this may prove an impossibility. BEHAVIOUR OF CUT TENDONS
This experimental work on partly cut tendons is of great theoretical interest but in clinical practice such injuries are u n c o m m o n and they do not constitute any real management problem. Difficulty arises only when the tendons have been totally transected and it is these which are our main clinical concern. Before progressing further it is well first to consider what happens to the cut ends of a tendon in the absence of any treatment. At one time, it was thought that after section, the cut ends of the tendon would 238
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always become re-attached to surrounding immoveable structures and it was taught that the stumps were "unsatisfied" until this had occurred. Clinical observation, however, has made it clear that in most cases this does not happen and instead the cut ends retract into an undamaged portion of the sheath where they become smoothly rounded off. This rounding o f f was initially regarded as due simply to atrophy, but Furlow (1976) and Richards (1977) have now shown that it is the result of active cellular remodelling. The process is accompanied by a marked increase in the vascularity of the tendon stump. (Fig. 3). While the great majority o f cut ends do seem to behave in this fashion, it is also true that there are a few stumps which behave differently and become densely adherent. This irregular behaviour may, it has been suggested (Matthews 1977), be related to cessation of the bloodflow to the tendon end consequent on its division and that the stump attaches itself to surrounding tissues in order to regain a blood supply. (Fig. 4). Such alterations in bloodflow after division might, theoretically, occur as a consequence of the segmental nature of the tendon circulation. Whether or not this is so, the fact that a minority o f stumps show a tendency to adhere has some practical implications. It would indicate that there may be a small group of tendon injuries in which failure would result irrespective o f the excellence o f treatment and would go some way to explain the unpredictability of the results in tendon repair. If this small group is excluded it will be apparent that the initial injury to the tendon could not be the stimulus for the formation of adhesions since in most cases the stumps separate from each other under the influence of proximal muscle pull and then become smoothly rounded off. The adhesive response is a regular feature only when surgical repair is undertaken and one is led to the conclusion that it is certain factors integral to the treatment which are responsible for the adhesions rather than any inherent failing of the tendon tissue. If the component parts of surgical tendon repair are analysed, it will be seen that basically they comprise exposure of the tendon ends, apposition, usually by some form o f suture, and finally, protection of the junction by splintage until healing is advanced. Experimental studies have shown (Matthews and Richards 1976) that, far from being harmless, these factors combine together in varying degree to trigger o f f a process whereby the site of division becomes enveloped in scar tissue. (Fig. 5). TENDON STUMP APPOSITION The presence of a suture, even in an intact tendon, is sufficient to excite an adhesive response (Lindsay and Thomson 1960) and there is no doubt that it must bear much of the blame for the tendency to scar tissue production. The avoidance o f an inflammatory reaction by using some non-irritant suture material is certainly to be recommended in repair procedures, but cannot be regarded as the complete answer since adhesions still form even when inert suture such as stainless steel is employed. It is probable that the explanation for the ill effects of suture lies in its strangulating effect on the parts o f the tendon which it encloses. Such areas o f circulatory impairment have been demonstrated (Bergljung 1968, Matthews 1977) (Fig. 6) and the reduced viability o f the tendon tissue (Fig. 7) would readily account for the inert behaviour of its cells during healing. On this basis, the development o f adhesions is an attempt not so much to bring about repair, but rather to support the The Hand-- Volume 11
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ingrowth of new blood vessels which run in to revascularize the ischaemic tendon. The maintenance of stump apposition will always be an essential step in repair if continuity of the tendon is to be restored. However harmful sutures m a y be one cannot envisage a method by which they could be eliminated entirely and perhaps the most that can be hoped for is that in their design as much account will be taken o f their possible effects on tendon physiology as on their simple mechanical strength. THE INFLUENCE OF THE SYNOVIAL S H E A T H
The evidence relating to the effect of damage to or excision of the overlying synovial sheath on the healing of a tendon is less conclusive than that of suture. There is, however, experimental work both f r o m this country (Matthews and Richards 1976) and J a p a n (Tokita, Y a m a y a and Yabe 1974) which suggests that careful preservation of the digital theca m a y improve the prospects of restoring gliding function. Attempts have been made to explain the diminished adhesion f o r m a t i o n noted in these experiments and it has been suggested that if the area of tendon regeneration is in contact with an intact mesothelial layer it is less likely to adhere than if the sheath is excised. In the latter circumstance the injured tendon is in contact with healing perisheath structures and, as Peacock (1964) has emphasised, forms but one element in a single pool of granulation tissue which must inevitably heal as a single scar. The role of the synovial fluid in tendon nutrition may also have some bearing on adhesion formation. Excision o f the sheath would, presumably, interrupt this diffusion pathway and further embarrass the viability of tendon ends already strangulated by sutures and so increase the stimulus for adhesions to develop. In clinical practice the consensus of opinion has been that the overlying sheath should be excised in association with tendon repair on the basis that if adhesions are to form it is better that they should be to relatively mobile subcutaneous fat rather than to the inelastic theca. In recent years, however, good results have also been reported (Miller 1971, Richards 1977) after tendon repairs during which the sheath had been preserved or even repaired. Provided that the hazards o f impaction of the sutured tendon against the rigid sheath can be avoided, such techniques may have an important part to play in limiting adhesions. EFFECT OF TENDON SPLINTAGE There is a natural tendency to believe that if, after a tendon has been repaired, active movements could be started early on, then this movement would be retained and a good functional result assured. Nevertheless, m a n y years ago, it was realised that the reverse applied and active motion did not reduce adhesions and was m o r e liable to cause complete incarceration of the repair in scar. It is not difficult to see why this should be so since repeated cycles of high and low tension in the tendon would inevitably lead to gap formation and increase the strangulating effect of the suture, both of which would encourage an excessive adhesive response. These undesirable secondary effects are unfortunately inevitable if motion o f the healing tendon is achieved through active contraction of the flexors. Although experimental studies (Matthews and Richards 1976) have indicated that the immobility of the repair zone enforced by splintage is a contributory factor in adhesion formation, 240
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early active movement would seem to have even greater disadvantages. A possible way around the problem has been introduced by Kleinert (1973), who advocates early movement after tendon repair but achieves this in a passive m a n n e r by, Using elastic band traction to flex the fingers in conjunction with active finger extension: By this means the contractions o f the flexor muscle are reflexly inhibited and tension within the tendon remains low. CONCLUSIONS Basic studies have served to highlight the predicament with which we are faced when we undertake the treatment of flexor tendon injuries. It would appear that in a minority o f cases one or other o f the stumps is destined to adhere even from the moment o f the injury due to alterations in its blood circulation. Such factors are clearly outside our control so that direct repair in these tendons cannot be expected to succeed. For the remainder, the tendon ends retain excellent vascularity and there is at least the theoretical possibility o f obtaining intrinsic tendon healing. Unfortunately, the techniques which we have, o f necessity, to employ as part o f our treatment regime to expose a n d appose the t e n d o n e n d s are, in themselves, a cause o f adhesions. The clinical goal o f obtaining tendon union without :adhesions seems unlikely to be reached and in the final analysis the success or failure o f a rep/iir.ma.y depend as much on the nature of adhesion~ as On their qUantity- The~pi-gg~ia~e:0f adhesions between the tendon and its surroundings-is not necessarity/a disaster provided that they are "long enough to allow movement.: The iml~brtance:~0f secondary remodelling of scar tissue after tendon repair has been stressed by Peacock (1965) and it is atI the more unfortunate that the process is so POOrLy understood. Basic research has added greatly to our knowledge of tendon healing and has clarified many o f the problems involved. It must be accepted, however, that such research does have its limitations and the results of animal studies cannot be translated directly to man. It may indeed be argued that in the quest for a solution to human ills the best subject for study is man himself. In tendon surgery at the present time are practiced innumerable variations of technique, some minor and s o m e major, most insignificant but some perhaps crucial to success or failure. It is perhaps in the detailed, critical and comparative analysis of our clinical material thai lies the key to improving the outlook in what is 'still a difficult injury. ACKNOWLEDGEMENTS
I am indebted to t h e C l i n i c a l Research Committee o f the Welsh Office for substantial grants to support continuing investigations in this field. I Would like to pay particular thanks to Mr. Harold Richards, F.R.C.S., for many years consultantin-charge of the Hand Unit at Cardiff Royal Infirmary, who first stimulated my interest in tendon healing and has been a constant source o f help and inspiration. I am most grateful to Miss Jayne Gambold for secretarial assistance in the preparation o f this manuscript. REFERENCES
BERGLJUNG, L. (1968). Vascular Reactions After Tendon Suture and Tendon Transplantation, A Sterco-Micro angiographic Study On The Calcaneal Tendon Of the Rabbit. Scandinavian Journal of Plastic and ReconstructiveSurgery, Supplementum4. The Hand-- Volume 11
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