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The determinants of flexor tendon fibrosis following trauma: An experimental study in rabbits
The Determinants of,Flexor Tendon Fibrosis Following Trauma: An Experimental Study in Rabbits Michael Watson
THE D E T E R M I N A N T S OF F L E X O R T E N D O N FIBROSIS F O L L O W I N G T R A U M A : A N E X P E R I M E N T A L STUDY IN RABBITS M I C H A E L WATSON, L O N D O N SUMMARY Twenty-six rabbits were subjected to various types o f forepaw flexor tendon laceration. After two weeks the tendons were examined. Fibrosis was densest around the proximal stump of the divided profundus tendon. Double partial transverse nicks, designed to induce local ischaemia, caused no more fibrosis than a single longitudinal slit of the same length. Rendering the proximal stump ischaemic with a snare caused no increase in fibrosis. It was concluded that movement and tissue trauma are more important than ischaemia in determining the degree o f fibrosis around the injured flexor tendon in the rabbit forepaw. INTRODUCTION The crippling effects of accidental division of a flexor tendon in a finger have taxed surgeons for generations. In order to overcome the almost universal late suture-line fibrosis following direct suture Bunnell (1922) developed a technique of free tendon graftirig. However, even in the most experienced hands this technique does not give universally good results (Pulvertaft, 1973). To overcome the common cause of failure of this procedure, graft fibrosis, various techniques have been tried. Paneva-Holevich (1969) described a method of pedicle grafting. Some (but not all) of the results were spectacularly good. Hunter and Salisbury (1971) evolved a method of producing a gliding pseudo-sheath for the graft. In most surgeons' hands this technique has not proved completely reliable either. Recently interest has been revived in direct early suture: Matthews and Richards (1974) have shown that tendons are capable of repairing themselves in rabbits without exogenous fibrosis. For this reason they advise atraumatic direct suture of the accidentally divided tendon in man. There are two basic determinants of tendon suture-line fibrosis. Both ischaemia and trauma of the tendon ends must elicit a local inflammatory response. This nonspecific tissue reaction is the final common path by which tendon suture-lines become fibrosed (Potenza, 1963). In planning a rational method of tendon suture the surgeon needs to know the relative importance of ischaemia and trauma in eliciting the tissue reaction. To this end the present experiments were planned. The flexor tendons to a single digit in rabbit forepaws were surgically divided in various ways. The animals were killed when the resulting fibrosis bad developed and the tendons were examined for variations in the degree of fibrosis induced. MATERIAL AND METHODS Twenty six adult New Zealand rabbits were used. They were divided into three groups. In the first group ten rabbits were used. The superficialis and profundus tendons were both divided transversally at the same level, over the apex of the prominence of the metacarpophalangeal joint in the palm. At this level in the rabbit the superficialis tendon is of thread-like proportions, and it decussates a further two or three millimetres distally. The fibrous flexor sheath in the rabbit is represented by a narrow pulley, a condensation of palmar fascia, over the metacarpophalangeal prominence. The surgical division was Michael Watson, M.A., M.R.C.P., F.R.C.S., Guy's Hospital, London, S.E. 1. 150
The Hand--Vol. 10
No. 2
1978
The Determinants of Flexor Tendon Fibrosis Following Trauma: An Experimental Study in Rabbits Miehael Watson
.__~-
__---.
.
.
.
--
tl
5ram.
2m--_m~ -___
t-4mm-z Fig. 1. A diagram to show the surgical lacerations in the profundustendons in the secondgroup of rabbits. The transverse nicks were designedto induce an ischaemic segment between them. performed at the proximal mouth of this pulley. The skin wounds were sutured with nylon and the rabbits were left free in their cages. After ten tojfourteen days the animals were killed. The paws were carefully dissected and representative samples of tissue were taken for histology. All the dissections were photographed. In the second group a further ten animals were used. Only the profundus tendon was cut. The cut was placed at the same level as in the previous group. Five rabbits had longitudinal incisions four millimetres long made in the mid-line of the tendon. In the other five animals the tendons were cut twice in the same region: each cut was two millimetres deep and was orientated across the tendon from the same side. The cuts were four millimetres apart (Figs. la and b). In the third group six animals were used. The profundus tendons were cut across completely at the same level as that in the first two groups. Nylon snares were then tied as tightly as possible around the profundus tendons three millimetres proximal to the cuts. RESULTS
In the first group two wounds became infected. The animals were killed and diffuse soft fibrous tissue was found to have invaded the whole palm at ten and twelve days 9respectively. It was impossible to differentiate the degree of fibrosis around the cut tendon in these animals. In the remaining eight animals the wounds healed well. After fourteen days there was a plaque of tough fibrous tissue around the cut tendons. Dissection revealed that almost all the fibrous tissue lay between the pulley and the proximal stump of the profundus. The superficialis stumps could be pulled from the mass of fibrous tissue with few or no adhesions, The distal profundus stump was stuck to the pulley by fibrinous exudate but there was little true fibrosis (Fig. 2). There was little separation of the divided ends of either the superficialis or profundus tendons. In the second group none of the wounds became infected. Careful examination of the fibrosis at fourteen days revealed no more than trivial differences in the degree of fibrosis around the injured profundus in any of the animals: the longitudinal and transverse cuts elicited the same degree of fibrosis. The superficialis was only lightly stuck to the fibrous tissue and could be pulled free easily. In the third group the nylon snare appeared to have made no difference to the outcome: there was no distinguishable difference in the degree and distribution of fibrosis when compared with that in the other two groups. The Hand--Vol. lO
No. 2
1978
151
The Determinants of Flexor Tendon Fibrosis Following Trauma: An Experimental Study in Rabbits, Michael Watson
Fig. 2. A photograph to show the fibrosis around the profundus ten'don. The thin superfieialis tendon can be seen running through the young fibrosis surrounding the profundus tendon. DISCUSSION
In the first group of rabbits the experiment showed that there was an obvious difference in the propensity of the profundus tendon and the superficialis tendon to elicit a fibrous reaction following damage. The reasons for this are not clear, but may be simply a measure of the volume of tissue damage, since the profundus is many times thicker than the superficialis. However, this does not explain the difference in the degree of fibrosis found around the proximal and distal stumps of the profundus. It seems unlikely that the proximal stump is more ischaemic than the distal one since the lumbrical is attached to the length of the tendon in the palm proximal to the division and must receive a good deal of its blood supply thereby. The only extrinsic difference in the two stumps following division of the tendon is that the proximal one moves with the action of its muscle belly and the distal one does not. By a process of exclusion therefore, it appears that movement of the damaged stump must be important in eliciting a fibrous reaction. This reinforces the view of Verdan who emphasised the importance of immobilisation of the suture line following direct tendon suture (1972). In the second group an effort was made to cause different amounts of ischaemia with the same amount of tissue damage. The total length of the cuts was the same whether either two transverse nicks or one longitudinal one was made. It was assumed that the blood vessels were predominantly longitudinal, as in man (Brockis, 1953), and that two transverse nicks would render the section of tendon between them ischaemic. In fact there was no difference in the degree of fibrosis elicited. This suggested that ischaemia was much less important than tissue damage as a determinant of fibrosis. However, the experiment used an unsubstantiated assumption (the orientation of the intratendinous vasculature), so a third experiment was designed. In the third group of six rabbits the proximal stump of the completely divided profundus tendon was rendered unequivocally ischaemic by ligating it three millimetres proximal to the surgical division. This caused no more fibrosis than simple surgical division. 152
The Hand--Vol. 10
No. 2
1978
The Determinants of Flexor Tendon Fibrosis Following Trauma: An Experimental Study in Rabbits Michael Watson
Thus it seems that tissue t r a u m a is a more important determinant of fibrosis around a damaged rabbit flexor tendon than ischaemia. Moreover, although the significance of movement of the damaged tendon has not been fully elucidated, it does seem from this experiment that m o v e m e n t per se increases peritendinous fibrosis following tendon trauma. There are m a n y differences between rabbit forepaw flexors and h u m a n finger flexors. Rabbit tendons do not run in long sheaths, they are well vascularised along their lengths by numerous vascular connections, their excursion is very small in proportion to their length and they are not moved individually. Rabbit flexor tendons are therefore more similar to extrasynovial h u m a n tendons (e.g. palmaris longus) than to intrasynovial ones (Chaplin, 1973). In spite of these differences, however, some extrapolation of the results to h u m a n s is justified. Rabbit and h u m a n tendons share basic biological properties. They are living tissues specialised to transmit tensile loads in varying positions of flexion. We m a y therefore predict that careful atraumatic suture of divided tendons is likely to result in less fibrosis at the suture-line than complex suture techniques involving m a n y perforations of the tendon near the suture-line. W e m a y also predict that immobilisation of the sutureqine will result in less suture-line fibrosis than early passive mobilisation provided all other determinants remain equal. REFERENCES
BUNNELL, S. (1922). Repair of Tendons in the Fingers. Surgery, Gynecology and Obstetrics, 35: 88-97. BROCKIS, J. G. (1953). The Blood Supply Of The Flexor And Extensor Tendons Of The Fingers In Man. The Journal of Bone and Joint Surgery, 35 B: 131- 138. CHAPLIN, D. M. (1973). The Vascular Anatomy within Normal Tendons, DividedTendons, Free Tendon Grafts and PedicleTendon Grafts in Rabbits. A MicroradioangiographicStudy. The Journal of Bone and Joint Surgery, 55 B" 369-389. HUNTER, J. M. and SALISBURY, R. E. (1971). Flexor-Tendon Reconstruction in Severely Damaged Hands. A Two-Stage Procedure Using a Silicone-Dacron Reinforced Gliding Prosthesis Prior to Tendon Grafting. The Journal of Bone and Joint Surgery, 53 A: 829-858. MATTHEWS, P. and RICHARDS, H. (1974). The Repair Potential of Digital Flexor Tendons. An Experimental Study, The Journal of Bone and Joint Surgery, 56 B" 618-625. PANEVA-HOLEVICH, E. (1969). Two-Stage Tenoplasty in Injury of the Flexor Tendons of the Hand. The Journal of Bone and Joint Surgery, 51 A: 21-32. POTENZA, A. D. (1963). Critical Evaluation of Flexor-TendonHealing and Adhesions Formation within Artificial Digital Sheaths. An Experimental Study. The Journal of Bone and Joint Surgery, 45 A: 1217-1233. PULVERTAFT, R. G. (1973). Twenty-Five Years of Hand Surgery. Personal Reflections.The Journal of Bone and Joint Surgery. 55 B: 32-55. VERDAN, C. E. (1972). Half a Century of Flexor-TendonSurgery. Current Status and Changing Philosophies. The Journal of Bone and Joint Surgery. 54 A: 472-491.
The Hand--Vol. 10
No. 2
1978
153
THE D E T E R M I N A N T S OF F L E X O R T E N D O N FIBROSIS F O L L O W I N G T R A U M A : A N E X P E R I M E N T A L STUDY IN RABBITS M I C H A E L WATSON, L O N D O N SUMMARY Twenty-six rabbits were subjected to various types o f forepaw flexor tendon laceration. After two weeks the tendons were examined. Fibrosis was densest around the proximal stump of the divided profundus tendon. Double partial transverse nicks, designed to induce local ischaemia, caused no more fibrosis than a single longitudinal slit of the same length. Rendering the proximal stump ischaemic with a snare caused no increase in fibrosis. It was concluded that movement and tissue trauma are more important than ischaemia in determining the degree o f fibrosis around the injured flexor tendon in the rabbit forepaw. INTRODUCTION The crippling effects of accidental division of a flexor tendon in a finger have taxed surgeons for generations. In order to overcome the almost universal late suture-line fibrosis following direct suture Bunnell (1922) developed a technique of free tendon graftirig. However, even in the most experienced hands this technique does not give universally good results (Pulvertaft, 1973). To overcome the common cause of failure of this procedure, graft fibrosis, various techniques have been tried. Paneva-Holevich (1969) described a method of pedicle grafting. Some (but not all) of the results were spectacularly good. Hunter and Salisbury (1971) evolved a method of producing a gliding pseudo-sheath for the graft. In most surgeons' hands this technique has not proved completely reliable either. Recently interest has been revived in direct early suture: Matthews and Richards (1974) have shown that tendons are capable of repairing themselves in rabbits without exogenous fibrosis. For this reason they advise atraumatic direct suture of the accidentally divided tendon in man. There are two basic determinants of tendon suture-line fibrosis. Both ischaemia and trauma of the tendon ends must elicit a local inflammatory response. This nonspecific tissue reaction is the final common path by which tendon suture-lines become fibrosed (Potenza, 1963). In planning a rational method of tendon suture the surgeon needs to know the relative importance of ischaemia and trauma in eliciting the tissue reaction. To this end the present experiments were planned. The flexor tendons to a single digit in rabbit forepaws were surgically divided in various ways. The animals were killed when the resulting fibrosis bad developed and the tendons were examined for variations in the degree of fibrosis induced. MATERIAL AND METHODS Twenty six adult New Zealand rabbits were used. They were divided into three groups. In the first group ten rabbits were used. The superficialis and profundus tendons were both divided transversally at the same level, over the apex of the prominence of the metacarpophalangeal joint in the palm. At this level in the rabbit the superficialis tendon is of thread-like proportions, and it decussates a further two or three millimetres distally. The fibrous flexor sheath in the rabbit is represented by a narrow pulley, a condensation of palmar fascia, over the metacarpophalangeal prominence. The surgical division was Michael Watson, M.A., M.R.C.P., F.R.C.S., Guy's Hospital, London, S.E. 1. 150
The Hand--Vol. 10
No. 2
1978
The Determinants of Flexor Tendon Fibrosis Following Trauma: An Experimental Study in Rabbits Miehael Watson
.__~-
__---.
.
.
.
--
tl
5ram.
2m--_m~ -___
t-4mm-z Fig. 1. A diagram to show the surgical lacerations in the profundustendons in the secondgroup of rabbits. The transverse nicks were designedto induce an ischaemic segment between them. performed at the proximal mouth of this pulley. The skin wounds were sutured with nylon and the rabbits were left free in their cages. After ten tojfourteen days the animals were killed. The paws were carefully dissected and representative samples of tissue were taken for histology. All the dissections were photographed. In the second group a further ten animals were used. Only the profundus tendon was cut. The cut was placed at the same level as in the previous group. Five rabbits had longitudinal incisions four millimetres long made in the mid-line of the tendon. In the other five animals the tendons were cut twice in the same region: each cut was two millimetres deep and was orientated across the tendon from the same side. The cuts were four millimetres apart (Figs. la and b). In the third group six animals were used. The profundus tendons were cut across completely at the same level as that in the first two groups. Nylon snares were then tied as tightly as possible around the profundus tendons three millimetres proximal to the cuts. RESULTS
In the first group two wounds became infected. The animals were killed and diffuse soft fibrous tissue was found to have invaded the whole palm at ten and twelve days 9respectively. It was impossible to differentiate the degree of fibrosis around the cut tendon in these animals. In the remaining eight animals the wounds healed well. After fourteen days there was a plaque of tough fibrous tissue around the cut tendons. Dissection revealed that almost all the fibrous tissue lay between the pulley and the proximal stump of the profundus. The superficialis stumps could be pulled from the mass of fibrous tissue with few or no adhesions, The distal profundus stump was stuck to the pulley by fibrinous exudate but there was little true fibrosis (Fig. 2). There was little separation of the divided ends of either the superficialis or profundus tendons. In the second group none of the wounds became infected. Careful examination of the fibrosis at fourteen days revealed no more than trivial differences in the degree of fibrosis around the injured profundus in any of the animals: the longitudinal and transverse cuts elicited the same degree of fibrosis. The superficialis was only lightly stuck to the fibrous tissue and could be pulled free easily. In the third group the nylon snare appeared to have made no difference to the outcome: there was no distinguishable difference in the degree and distribution of fibrosis when compared with that in the other two groups. The Hand--Vol. lO
No. 2
1978
151
The Determinants of Flexor Tendon Fibrosis Following Trauma: An Experimental Study in Rabbits, Michael Watson
Fig. 2. A photograph to show the fibrosis around the profundus ten'don. The thin superfieialis tendon can be seen running through the young fibrosis surrounding the profundus tendon. DISCUSSION
In the first group of rabbits the experiment showed that there was an obvious difference in the propensity of the profundus tendon and the superficialis tendon to elicit a fibrous reaction following damage. The reasons for this are not clear, but may be simply a measure of the volume of tissue damage, since the profundus is many times thicker than the superficialis. However, this does not explain the difference in the degree of fibrosis found around the proximal and distal stumps of the profundus. It seems unlikely that the proximal stump is more ischaemic than the distal one since the lumbrical is attached to the length of the tendon in the palm proximal to the division and must receive a good deal of its blood supply thereby. The only extrinsic difference in the two stumps following division of the tendon is that the proximal one moves with the action of its muscle belly and the distal one does not. By a process of exclusion therefore, it appears that movement of the damaged stump must be important in eliciting a fibrous reaction. This reinforces the view of Verdan who emphasised the importance of immobilisation of the suture line following direct tendon suture (1972). In the second group an effort was made to cause different amounts of ischaemia with the same amount of tissue damage. The total length of the cuts was the same whether either two transverse nicks or one longitudinal one was made. It was assumed that the blood vessels were predominantly longitudinal, as in man (Brockis, 1953), and that two transverse nicks would render the section of tendon between them ischaemic. In fact there was no difference in the degree of fibrosis elicited. This suggested that ischaemia was much less important than tissue damage as a determinant of fibrosis. However, the experiment used an unsubstantiated assumption (the orientation of the intratendinous vasculature), so a third experiment was designed. In the third group of six rabbits the proximal stump of the completely divided profundus tendon was rendered unequivocally ischaemic by ligating it three millimetres proximal to the surgical division. This caused no more fibrosis than simple surgical division. 152
The Hand--Vol. 10
No. 2
1978
The Determinants of Flexor Tendon Fibrosis Following Trauma: An Experimental Study in Rabbits Michael Watson
Thus it seems that tissue t r a u m a is a more important determinant of fibrosis around a damaged rabbit flexor tendon than ischaemia. Moreover, although the significance of movement of the damaged tendon has not been fully elucidated, it does seem from this experiment that m o v e m e n t per se increases peritendinous fibrosis following tendon trauma. There are m a n y differences between rabbit forepaw flexors and h u m a n finger flexors. Rabbit tendons do not run in long sheaths, they are well vascularised along their lengths by numerous vascular connections, their excursion is very small in proportion to their length and they are not moved individually. Rabbit flexor tendons are therefore more similar to extrasynovial h u m a n tendons (e.g. palmaris longus) than to intrasynovial ones (Chaplin, 1973). In spite of these differences, however, some extrapolation of the results to h u m a n s is justified. Rabbit and h u m a n tendons share basic biological properties. They are living tissues specialised to transmit tensile loads in varying positions of flexion. We m a y therefore predict that careful atraumatic suture of divided tendons is likely to result in less fibrosis at the suture-line than complex suture techniques involving m a n y perforations of the tendon near the suture-line. W e m a y also predict that immobilisation of the sutureqine will result in less suture-line fibrosis than early passive mobilisation provided all other determinants remain equal. REFERENCES
BUNNELL, S. (1922). Repair of Tendons in the Fingers. Surgery, Gynecology and Obstetrics, 35: 88-97. BROCKIS, J. G. (1953). The Blood Supply Of The Flexor And Extensor Tendons Of The Fingers In Man. The Journal of Bone and Joint Surgery, 35 B: 131- 138. CHAPLIN, D. M. (1973). The Vascular Anatomy within Normal Tendons, DividedTendons, Free Tendon Grafts and PedicleTendon Grafts in Rabbits. A MicroradioangiographicStudy. The Journal of Bone and Joint Surgery, 55 B" 369-389. HUNTER, J. M. and SALISBURY, R. E. (1971). Flexor-Tendon Reconstruction in Severely Damaged Hands. A Two-Stage Procedure Using a Silicone-Dacron Reinforced Gliding Prosthesis Prior to Tendon Grafting. The Journal of Bone and Joint Surgery, 53 A: 829-858. MATTHEWS, P. and RICHARDS, H. (1974). The Repair Potential of Digital Flexor Tendons. An Experimental Study, The Journal of Bone and Joint Surgery, 56 B" 618-625. PANEVA-HOLEVICH, E. (1969). Two-Stage Tenoplasty in Injury of the Flexor Tendons of the Hand. The Journal of Bone and Joint Surgery, 51 A: 21-32. POTENZA, A. D. (1963). Critical Evaluation of Flexor-TendonHealing and Adhesions Formation within Artificial Digital Sheaths. An Experimental Study. The Journal of Bone and Joint Surgery, 45 A: 1217-1233. PULVERTAFT, R. G. (1973). Twenty-Five Years of Hand Surgery. Personal Reflections.The Journal of Bone and Joint Surgery. 55 B: 32-55. VERDAN, C. E. (1972). Half a Century of Flexor-TendonSurgery. Current Status and Changing Philosophies. The Journal of Bone and Joint Surgery. 54 A: 472-491.
The Hand--Vol. 10
No. 2
1978
153