- Email: [email protected]
Biomechanical studies of the remodeling of knee joint tendons and ligaments
Pergamon Copyright
OOZl-9290(95)00163-8
ISB KEYNOTE
BIOMECHANICAL
J. Biomchanics, Vol. 29, No. 6, pp. 707-716, 1996 c 1996 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0021-9290/96 $15.00 + .oO
LECTURE
STUDIES OF THE REMODELING TENDONS AND LIGAMENTS
OF KNEE
JOINT
Kozaburo Hayashi Biomechanics Laboratory, Department of Mechanical Engineering, Faculty of Engineering Science, Osaka University, Toyonaka, Osaka 560, Japan Abstract-Living tissues and organs are dynamic and change their mechanical properties and structure in response to stressalteration as a phenomenon of functional adaptation and optimal operation. This phenomenon is called ‘Tissue Remodeling’, and Wolff s law on bone remodeling is widely known. Several recent studies have shown that fibrous connective tissues such as tendons and ligaments also have the ability of remodeling. However, relatively little is known about the stress and motion effects on tissue homeostasis in biological soft tissues. This article primarily deals with changes of the biomechanical properties of knee joint tendons and ligaments through a wide variety of treatment modalities, including stress deprivation, recovery after stress deprivation, and stress enhancement. The experimental results indicate that tendons and ligaments have an ability to adapt in response to the change of stress if the extent of stress alteration is within allowable ranges. Copyright 0 1996 Els&er Science Ltd.Keywords: Tendon; Ligament; Remodeling; Stress deprivation; Stress shielding; Stress enhancement: Immobilization; Remobilization; Exercise.
INTRODUCTION
Living tissues and organs are dynamic and adapt mechanically and structurally to alteration in function. They grow or resorb in response to change in mechanical environment as a phenomenon of functional adaptation and optimal operation (Fung, 1990; Hayashi, 1992). That is, living tissues and organs have an ability to homeostatically respond to mechanical demands. In normal life, almost all biological tissues and organs are always exposed to some forces after birth, and never experience with non-load condition. This phenomenon is essential to living tissues and organs, and does not exist in non-living materials. This kind of biomechanical phenomenon is called ‘Tissue Remodeling’, and Wolffs law on bone remodeling is well known (Fung, 1990). Tissue remodeling occurs during disuse and exercise. In addition, repair of injury and healing of autografts are also associated with tissue remodeling. Although the adaptation of bone to mechanical stress and bone remodeling have been studied extensively (Cowin, 1993; Meade, 1989), relatively little is known about the stress and motion effects on tissue homeostasis in biological soft tissues like tendons and ligaments. However, several recent studies have shown that these soft fibrous connective tissues also have the ability of remodeling. We have been doing a series of studies on the biomechanical, morphometrical, and histological responses of knee joint tendons and ligaments (Fujii, 1993; Hayashi et al., 1991, 1992; Keira et al., 1992, in press; Majima et al., 1992a,b, 1993, 1994, in press; Ohno et al., 1991, 1993; Tohyama et al., 1992; Yamamoto et al., 1989,1992a, 1993, in press; Yasuda and Hayashi, 1994) as well as arterial walls (Hayashi, 1992; Hayashi and Matsumoto, 1994; Matsumoto and Hayashi, 1991, 1994, in press) to stress alter-
Received in jinal form 23 September 1995. Address correspondence to: Kozaburo Hayashi, Ph.D. Department of Mechanical Engineering, Faculty of Engineering Science, Osaka University, Toyonaka, Osaka 560, Japan. 707
tion. This review paper primarily deals with the experimental findings obtained by us and others regarding changes in the biomechanical properties of knee joint tendons and ligaments through a wide variety of treatment modalities, including: (1) stress deprivation by immobilization, disuse, and stress-shielding, (2) reconditioning by remobilization and restressing,and (3) stress enhancement by increased tension and exercise training. Tipton et al. (1986) published a brief review regarding the experimental studies on the effectsof physical activity upon ligaments and tendons. Besides, Woo et al. (1990) wrote a review article on the similar subject, mainly focusing on their own studies. RESPONSE
TO STRESS
DEPRIVATION
Effects of stress deprivation on the biomechnanics of knee joint tendons and ligaments have so far been studied by the experiments of immobilizing or disusing animal knees (Akeson et al., 1980; Binkley and Peat, 1986; Klein et al., 1982; Larsen et al., 1987; Noyes, 1977; Noyes et al., 1974; Woo et al., 1979, 1982, 1987). Although immobilization and disuse decrease both stress and motion, we do not know the exact amount of the reduction of stress. Actually, stress applied to tendons and ligaments during immobilization or disuse is not always zero. As a more direct method for stress deprivation, we developed a novel method of stress shielding by which tension in the patellar tendon can be released completely under the condition of normal knee motion (Ohno et al., 1991; Yamamoto et .al.. __..__.- _. .... 1989). We have been applying this technique to the rabbit patellar tendon. After exposing the patellar tendon in each right knee, a stainless steel pin and a stainless steel screw were transversely inserted into the patella and in the tibia1 tubercle. respectively. Then, the patellar tendon was slackened b; drawing the patella toward the tibia1 tubercle, and this position was maintained with use of a flexible stainless steel wire installed between the pin and the screw (Fig. 1). Postoperatively, no immobilization treatment was applied, and all animals were allowed daily activities in cages. One to 6 weeks after surgery,
708
ISB Keynote
Lecture (Mean+S.E.)
40
T
,^
Control (n-16) Fig. 1. Method for complete stress shielding by which tension in the patellar tendon is released under condition of regular knee motion (Yamamoto et al., 1993).
/"
(MeapSE)
0
2 Strain
Fig. 2. Stress-strain non-treated, control
Control
6
4 E
8
(%)
curves of completely stress-shielded and patellar tendons in the rabbit (Yamamoto et al., 1993).
a patella-patellar tendon-tibia complex was excised from each knee. Tensile testing was carried out on the complex at a cross-head speed of 20mmmin-’ after measuring the cross-sectional area of the patellar tendon with an area micrometer (Yamamoto et al., 1992~). Strain in the tendon was determined using a video dimension analyzer (Hayashi and Nakamura, 1985). We chose the patellar tendon for this study because the distribution of force and tissue quality is fairly uniform through the tissue in this tendon (Yamamoto et al., 1992~). Another reason is that the patellar tendon is easily accessible for surgical procedure, which enables to develop a reproducible model for stress deprivation. The above-described stress shielding technique can make it possible for the tendon to be free from stress yet allow normal motion of the knee joint. In addition, this technique can be extended to develop a method for quantitatively controlling the amount of stress applied to the tendon (partial stress shielding) as described later in this article. Our previous studies showed that there were no inflammatory sideeffects of the stainless steel wire on the biomechanical properties of the patellar tendon.
1 wk (n-6)
2 wks (n-6)
3 wks (n-6)
6 wks (n-6)
Fig. 3. Cross-sectional area of completely stress-shielded and non-treated, control patellar tendons in the rabbit (Yamamoto et cd., 1993). Figure 2 demonstrates the averaged stress-strain curves for the completely stress-shielded and non-treated, control patellar tendons (Yamamoto et al., 1993). The slope of the linear portion of the curve decreased progressively and remarkably in the stress-shielded tendon, and reached a minimum value of about 9% of the control value after 3 weeks. Tensile strength was also decreased very rapidly and markedly by the stress shielding: for example, it decreased to about 50% at 1 week and to less than 10% at 2 weeks compared to the control tendon, but became almost constant thereafter. No significant change was observed in the elongation at failure. In contrast to the decrease of tensile strength. the cross-sectional area of the patellar tendon was markedly increased by the stress shielding during the period of 3 weeks after the treatment (Fig. 3, Yamamoto et al., 1993). The area increased to 231% at 3 weeks compared to the control area, although it decreased to 140% at 6 weeks. Maximum failure load was decreased to 26% of the control value by 2-week stress shielding; however, owing to the considerable increase in the cross-sectional area, the decrease of the maximum load was less than that of tensile strength. These biomechanical changes occurring in response to stress shielding were also observed in the canine anterior cruciate ligament to which a special experimental technique was applied for releasing tension in the ligament (Keira et nl., 1992. in press). To know the effects of the extent of stress reduction, we have extended the above-mentioned stress-shielding method to quantitatively control the magnitude of stress in the patellar tendon (Majima et al., 1992, in press). Instead of the stainless steel wire shown in Fig. 1, a polyester-mesh made artificial ligament was hooked between the patella and the tibia1 tubercle in parallel to the patellar tendon. It was then pulled and fixed using a steel clamp when load in the patellar tendon was reduced to about 30% of the normal force. Reduction of the load was monitored with a buckle transducer (Yamamoto et al., 1992b) temporarily attached to the patellar tendon. At the time of sacrifice, percentage ratios of the load shared by the partially stress-shielded tendons were, for example, about 33, 41, and 48% at 3, 6, and 12 weeks, respectively. These changes are attributable to the creep of the artificial ligament and/or the shortening of tendon length caused by tissue remodeling. Figure 4 demonstrates temporal changes of the tensile strength and maximum failure load of the partially (70%) stress-shielded patellar tendons together with those of the completely (100%) stress-shielded tendons, control tendons, and sham-operated tendons (Majima et al.. 1992a). The data for the tendons completely stress-shielded for 12 weeks are not shown in these figures mainly because the patella was fractured inside the body by this period and the data could not be obtained. In a fashion similar to the complete stress shielding, the partial stress shielding also significantly decreased the tensile strength of the patellar tendon: however, the decrease was much less than
ISB Keynote
m
Sham (n=6) l
m
;2;
7or
Control
z
800
uf
600
x 0
400
EE, ; z
P < 0.05
(VS
PSS (fl=6)
# P’ 0.05
CSS (n=6)
(Mean:SEi
Pwks
6wks
Zwks
6wks
(VS PSS)
12wks
0 12wks
Fig. 4. Temporal changes of tensile strength and maximum failure load in partially stress-shielded (PSS), completely stress-shielded (CSS), and sham-operated patellar tendons in the rabbit (Majima et al., 1992a).
in the case of strength of the was about 60 ated tendon. stress-shielded 2 and 6 weeks,
709
less reduction of the tensile strength, there were no significant differences in the maximum failure load among the partially stress-shielded tendons, sham-operated tendons, and control tendons throughout the experimental period. Figure 5 shows plotting of the cross-sectional area against the tensile strength for all the groups, where a broken line was drawn assuming that the product of the tensile strength and the cross-sectional area is equal to that of the averaged control values. The data obtained from the partially stress-shielded tendons fit to this curve fairly well; in the case of 70% stressshielding. the tendon seems to keep the maximum failure load at the normal level by compensating for the decrease of tensile strength by increasing the cross-sectional area. On the other hand, almost all the data obtained from the completely stressshielded tendons deviate much from this curve; the decrease of tensile strength in 100% stress-shielded tendons was too much to be compensated by the increase of the cross-sectional area. Histologically, no essential change appeared at 1 week in the completely stress-shielded tendons, but great changes were observed at 2 to 6 weeks (Yamamoto et al., 1993). That is, 100% stress shielding for more than 2 weeks changed the morphology of fibroblasts from spindle to round shape, and disordered the alignment of collagen fibers. Between 1 and 2 weeks, the number of fibroblasts increased remarkably to about four times as many as that in the control tendons. Their number was almost unchanged between 2 and 6 weeks after the treatment of stress shielding. In the partially stress-shielded tendons, we observed a fairly normal crimp pattern of collagen fibers as well as spindle shape of cells. but no round shape of fibroblasts throughout the experimental period (Fujii, 1993; Majima et al., 1992a, in press). This microstructure was much different from that observed in the completely stress-shielded tendons. Table 1 shows reported data regarding the effects of immobilization on the biomechanical properties of knee joint tendons and ligaments. For example, Noyes (1977) demonstrated in the primate that knee immobilization for 8 weeks decreased the maximum failure load of the anterior cruciate ligament to 78% of that in the non-treated, control ligament. Woo et al. (1987) reported that 9-week knee immobilization decreased the maximum load of the rabbit medial collateral ligament to 3 1% of the control value. These biomechanical studies indicate that the mechanical strength of knee joint ligaments is significantly reduced by immobilization. However, if these data are compared to our results obtained from the experiments of direct stress shielding, we can see that percentages of the reduction of maximum failure load caused by
Sham)
200
Control
Lecture
complete stress shielding. For example, tensile partially stress-shielded tendon at 2 and 6 weeks and 55%, respectively, of that in the sham-operThe cross-sectional area of the partially tendon increased to about 140% and 170% at respectively. Due to this hypertrophic change and
0 Control \ \
anAY= 792.4 (Control)
30-
l
Sham
a
PSS
m
css
l a
I
20 l
10 -
o-
0
---_
10
20
30 Tensile
40 strength
50
60 on
70
o
--
80
90
(tIPa)
Fig. 5. Cross-sectional area versus tensile strength in partially stress-shielded (PSS), completely stressshielded (CSS), and sham-operated patellar tendons in the rabbit. The broken line was drawn assuming that the product of tensile strength and cross-sectional area is equal to that of the averaged control values.
710
ISB Keynote Lecture
Table 1. Change of cross-sectional area and strength of tendons and ligaments by immobilization
Noyes (1977) Klein et al. (1982) Binkley and Peat (1986) Woo et al. (1987) Larsen et al. (1987)
(% control tissue, *p
Animal
Period
Tissue
Strain rate
Area
Monkey Dog Rat Rabbit Rabbit Rat Rat
8 wk 12wk 40d 9wk
66.2% s - l 60mms-’ 5 mmmin-’ 0.5% s-l 0.5%s-’
97
80*
89 78* 79*
38*
4wk 4wk
ACL ACL MCL MCL MCL ACL PCL
2wk 3 wk 2wk 3 wk
PT PT PT PT
20mmmin-’ 20mmmin-’ 20 mmmin-’ 20mmmin-’
209* 231* 173* 170*
13* 9* 55* 56*
12wk
Fuji (1993), Majima et al. (in press) 100% stress-shielded Rabbit Rabbit 70% stress-shielded Rabbit Rabbit
< 0.05)
Tensile strength Max. load 78* 44* 31* 29* 73* 88 26* 20* 94 95
ACL = Anterior cruciate ligament, MCL = Medial collateral ligament. PCL = Posterior cruciate ligament, PT = Patellar tendon.
immobilization are in between those induced by the 100% and 70% stress shielding. These results may indicate that tension in the ligament and tendon is not completely released by immobilization treatment, although it is reduced to less than 30% of a normal value. In addition, there are large differences in the change of the cross-sectional area between our experiments and the other studies. That is, immobilization slightly decreases the cross-sectional area, while direct stress shielding remarkably increases the area. The immobilization data shown in Table 1 were all obtained from ligaments. Response to stress deprivation may be different for ligaments and tendons. Further detailed studies are required to know the reason why the direct stress shielding-induced tissue hypertrophy in the patellar tendon. Biochemically, Amiel et al. (1982, 1983, 1990) observed that 9-week immobilization of the rabbit knee enhanced the production of new (immature) collagen as well as the degradation of old collagen, resulting in a net decrease of total collagen in the anterior cruciate ligament but no change of total collagen in the medial collateral ligament and the patellar tendon. On the other hand, Vailas et al. (1988) showed in the rat that hindlimb suspension for 28 days significantly decreased collagen and proteoglycan concentrations in the patellar tendon. By means of electron microscopy, Nakagawa et al. (1989) observed in the rat achilles tendon that 5-week suspension of hindlimb significantly decreased the total cross-sectional area of collagen fibers, and increased the relative percentage of thin collagen fibers. Disuse of hindlimb might have produced thin, immature collagen fibers and, at the same time, degradated thick, old collagen fibers. Additional work on the effects of stress deprivation upon the biochemistry and microstructure of tendons and ligaments is suggested.
the devices, and some extent of stress shielding occurs in the autografts. As an experimental mode1 of autografts, we developed a technique of instantaneously freezing the patellar tendon in situ to kill fibroblasts (Ohno et al., 1991, 1993; Yasuda and Hayashi, 1994). After freezing the patellar tendons in rabbits, we applied the same treatment of stress shielding as done to non-frozen tendons. In the case of complete stress shielding, the maximum failure load decreased somewhat slower than in the non-frozen tendons. However, the decrease was again remarkable, and the maximum load at 3 and 6 weeks was fairly similar to that obtained at 2-6 weeks in the non-frozen tendons (Ohno et al., 1993). In the case of partial stress shielding, the maximum failure load decreased to about 80% of the control value at 1 week. However, there were essentially no changes thereafter (Majima et al., 1993, 1994). Tensile strength changed in a fashion similar to the maximum failure load, although the decrease of the tensile strength was larger than that of the maximum load (Majima et al., 1992a, 1992b, 1994). These results indicate that we should apply some appropriate stress, say 30% or more than 30% of the normal stress, to autogenous grafts when they are augmented with synthetic devices. Otherwise, autografts markedly lose the strength. Besides the role of tension in maintaining autograft strength, we should consider additional factors that may contribute to the initial weakening of autograft patellar tendons, including the switch from an extra-synovial to an intra-synovial environment. Histologically, regardless of the extent of stress shielding, no cells were observed in the tendons which were in situ frozen and then stress-shielded for 2 weeks (Majima et al., 1992a, 1993, 1994; Ohno et al., 1991,1993; Yasuda and Hayashi, 1994). Even in the absence of fibroblasts during this period, the tensile strength of the tendons markedly decreased and hypertrophy occurred. That is, the patellar tendon responded to mechanical stress without cell. Although this is a very interesting phenomenon, the mechanisms are not yet clarified.
AUGMENTATION FOR THE RECONSTRUCTION OF KNEE JOINT LIGAMENTS RECOVERY
Stress shielding is one of the most important problems in the reconstruction of knee joint ligaments using augmentation techniques. A failed anterior cruciate ligament is often reconstructed using a portion of the patellar tendon as an autogenous graft (Pattee and Friedman, 1988). Immediately after transplantation, cellular necrosis occurs in the autograft, resulting in a tremendous decrease of the graft strength. As a method to solve this problem, augmentation devices made of synthetic materials are implanted in parallel with the grafts (Andrish and Woods, 1984; Kennedy et al., 1980; Yoshiya et al., 1986). In this case, tension applied to the grafts is partially shared or completely reduced by
FROM
STRESS
DEPRIVATION
Let me turn now the subject to recovery from stress deprivation. This issue has been mostly studied through remobilization after immoblization. Evaluation of the effect of joint remobilization on the functional properties of ligaments is of prime importance for the rehabilitation of previously immobilized joints. For this subject, we used a method of applying stress again to previously stress-shielded patellar tendons, i.e. restressing (Fujii, 1993; Yamamoto et al., in press). The stainless steel wire or the artificial ligament installed in parallel to the rabbit patellar
ISB Keynote Lecture
.&‘;a,,
711 Restressed (PSS*R) .-.--..---- __________ ---------.
-.-- *-- ---------o--- --o-----------o 70% stress-shielded
(PSS) Restressed (CSS+R)
60
‘OH’-
0
2
100% stress-shielded
4
6 Per lod
T
8 (week)
(CSS)
10
12
14
Fig. 6. Temporal percent changes of maximum failure load of the patellar tendons during stress shielding as well as during recovery from stress shielding (Fujii, 1993; Yamamoto et al., in press).
tendon for stress shielding (Fig. 1) was cut and removed after 2-week partial (70%) or complete (100%) stress-shielding, and normal stress was applied again to the tendon for the following 3 to 12 weeks. Tensile strength of the patellar tendon was progressively increased by restressing; the recovery of tensile strength was greater and faster in completely stress-shielded tendons than in partially stress-shielded tendons (Fujii, 1993). However, the tensile strength was significantly lower than the control value even if normal stress was applied to the tendons for 12 weeks. In contrast to the increase of tensile strength, the cross-sectional area of the tendons progressively decreased with time. The maximum failure load of the 70% stress-shielded tendons was remained at a control level throughout the period of restressing. In the completely stress-shielded tendons, the recovery of tensile strength was very fast and large, and the maximum failure load
finally returned to the control level after stressing for 12 weeks (Fig. 6). We should note that it takes much time for the tendons to recover the mechanical strength if it is once exposed to non-stress condition even for a short period of time. Table 2 demonstrates reported data on the percentage changes of the mechanical strength of ligaments induced by remobilization following immobilization. Woo et al. (1987) showed that the strength of the rabbit media1 collateral ligament immobilized for 9 weeks was increased markedly by the following 9-week remobilization, but it returned to only 79% of the original strength. Noyes (1977) immobilized rhesus monkeys in total body plaster casts for 8 weeks and, then, reconditioned by placing the animals in room size gang cages for 35 weeks or 72 weeks. By 8 weeks of immobilization, the maximum failure load of the anterior cruciate ligament was decreased by 39% in comparison
Table 2. Change of cross-sectional area and strength of tendons and ligaments by remobilization (% control tissues, ( ) % immobilized tissue)
Noyes (1977)
Larsen et al. (1987)
Woo et a/. (1987)
Animal
Immobil.
Monkey
8wk
Monkey
Tissue
Strain rate
35wk
ACL
66.2% s-’
8wk
12 wk
ACL
66.2%s-’
Rat
4wk
ACL
Rat
4wk
Rabbit
9wk
6wk (Swim) 6wk (Swim) 9wk
Rabbit
12wk
Remobil.
9wk
Area
PCL MCL MCL
0.5%s-’ 0.5%s-’
103
(121) (1::)
Fujii (1993), Yamamoto et al. (in press) 100% stress-shielded Rabbit 2wk 70% stress-shielded Rabbit
2wk
12wk
PT
20 mmmin-’
12wk
PT
20mmmin-’
143 (69) 123
(68) = Anterior cruciate ligament, MCL = Medial collateral ligament. PCL = Posterior cruciate ligament, PT = Patellar tendon.
ACL
Tens. strenth
Max. load
712
ISB Keynote Lecture l
**
0’0.001
(VS
Control)
## ~‘0.01 (vs Imnobilized) ### o
q
After
m
At sacrifice
removal
Mean:SD) L
800 2 tl? D z 5 E ';; P
600 Cont. (n=l6)
400 -
3 wks
6 wks
(n=5)
(n=6)
12 wks (n=6)
(Mean+S.E.)
200 -
Control
lmrobillzed
Remobilized
8 wks 35 wks 72 wks Fig. 7. Effects of reconditioning on maximum failure load of the anterior cruciate ligaments in the rhesus monkeys immobilized for 8 weeks in total body plaster casts (Noyes, 1977). 2
to the control group (Fig. 7). The maximum load in the specimens obtained from the 35-week reconditioned animals still showed 21% reduction in comparison to the control group, which indicates that a partial but incomplete recovery process had occurred. By reconditioning for 72 weeks, the maximum load returned to within 9% reduction from that in the control group; the difference between the control and the 72-week remobilized animals was not statistically significant. These results are similar to our results obtained from the restressed rabbit patellar tendons. From these results, we can say that prolonged recovery time is required for recovery from relatively brief period of stress deprivation. RESPONSE
TO STRESS
ENHANCEMENT
As stated above, return to normal stress levels greatly improve the biomechanical properties of previously stress-shielded or immobilized tendons and ligaments, although prolonged recovery time is necessary. How about the effectsof increased tension on normal tendons and ligaments? Connective tissues have been neglected by sports medicine and sports science researchers because their interests have been primarily directed on the cardiovascular and musculoskeletal systems(Tipton et nl., 1986). Recently, however, several animal studies have been done on the effects of exercise and training on tendon and ligament properties. Like the immobilization regimen, we cannot say the exact amount of tension increased by exercise and training. From an experimental perspective, it would be of interest if studies could be designed so that the forces acting directly on connective tissues are quantitatively increased (Tipton et al., 1986). As a direct and quantitative method, we have been using a technique of elevating stress level in tendons and ligaments by partial removal of the tissues (Hayashi et al., 1991; Yamamoto et al., 1992a). For example, we cut off both edges of the rabbit patellar tendon, and reduced the cross-sectional area of the remained tendon to about 75% or 50% of the original area. By this surgical treatment, 33% or 100% higher stress than the normal stress is applied to the remained tendon. Figure 8 demonstrates the results obtained from the patellar tendons stress-elevated to 133% of the normal stress. Although the tensile strength was slightly lower than the control value at 3 weeks, there were no significant differences in the stress-strain
Before removal
3 wks
6 wks
12 wks
(n=S)
(n=6)
(n-6)
(n=l?)
(Mean+S.E.l
Before
3 wks
6 wks
12 wks
removal
(n=5)
(n=6)
(n=6)
(n-17) (Mean+S.E.)
Fig. 8. Tensile strength, cross-sectional area, and maximum failure load of the rabbit patellar tendons stresselevated to 133% of normal stress.
relation and tensile strength among the control tendons and the tendons overstressed for 3 to 12 weeks. However, the crosssectional area was significantly increased by the overstressing if compared to each initial area. Eventually, the maximum failure load increased with increase in the cross-sectional area, and at 6 and 12 weeks there were no significant differences in the maximum load between the overstressed tendons and the control whole tendons. Figure 9 demonstrates the stress-strain curves obtained from the tendons overstressed to 2-fold of the normal stress. Depending on the mechanical characteristics, these tendons were divided into two groups, namely groups N and D. In group N, there was no change in the stress-strain behavior for 12 weeks, while the slope of the curve and tensile strength progressively decreased with time in group D. There was no histological difference between the group N and control tendons. In group D, on the other hand, there were a great number of fibroblasts, and breakage of collagen bundles was observed occasionally. In group N, there was almost no change in the tensile strength. The cross-sectional area was increased by the stress elevation, which increased the maximum failure load. The
ISB Keynote Lecture Stress-elevated
70 r l
Control
-r
! $’
6.
A
3wks(n=4)
n
6wksin=4)
4
result, the maximum load was maintained at the level obtained immediately after the tissue removal, i.e. 50% of the maximum load in the normal tendons. Separately from the above-mentioned experiments, we overstressed the anterior cruciate ligaments in rabbits for 3 to 6 weeks after reducing their cross-sectional areas by cutting off the medial or lateral l/2 bundles along the longitudinal axis (Yamamoto et al., 1992a). In vitro anterior-posterior drawer tests performed on the knees harvested from the other control rabbits indicated that tension applied to the remaining medial portion was increased to 13&150% of the normal level by the removal of the medial l/2 bundle, and that tension in the lateral portion was increased to 40&800% by the removal of the lateral l/2 bundle. This 3&50% overstressing induced no significant changes in the mechanical properties and dimensions of the medial portion of the anterior cruciate ligament. On the otherhand, the mechanical properties of the lateral bundle were significantly changed by the 300-700% overstressing: the tangent modulus and stiffness decreased to 60 and 46% of the control values, respectively, after 6 weeks of overstressing. These results indicate that knee joint ligaments and tendons seem to have an ability to adapt to overstressing within a certain range, i.e. if stressis less than 200% of the normal level; however, they cannot adapt if stress exceeds this limit. Gomez (1988) inserted a 1.6 mm diameter stainless steel pin underneath the rabbit medial collateral ligament to increase load and stress in the ligament from 2- to 3.5fold compared to the control ligament. This stress elevation increased the maximum load by 26% at 6 weeks, although this difference disappered at 12 weeks. Ultrastructurally, Biagini er al. (1991) observed the presence of areas having a high number of small diameter collagen fibrils in the clinically expanded extensor tendon. Table 3 shows reported data for the effects of exercise and training upon the strength of tendons and ligaments. Although the kind and extent of exercise and training are quite different among those studies, we can see that exercise and training induce minimal effectson the strength of tendons and ligaments. Cabaud et al., (1980) showed that higher-frequency and shorter-
to 200%
(n-18)
Group
N
12wksCn=4)
(MeantSE)
50
I
-0UD il
0
0
4
2 Strain
12wksln=S)
6 E
713
8
(%)
Fig. 9. Stress-strain curves of the rabbit patellar tendons overstressed to 200% of normal stress. These tendons are divided into two groups: group N and group D.
maximum load at 12 weeks increased by 40% in comparison to that obtained immediately after the partial removal of tissue. However, it was still about 70% of that of the whole tendon in the control knee. In group D, on the other hand, the tensile strength progressively decreased with time. Contrary to this, the cross-sectional area of the tendon increased markedly. As the
Table 3. Change of strength of tendons and ligaments by exercise (% control tissue, *p < 0.05, ( ) = normalized by body weight) Animal
Exercise
Period
Tissue
Viidik (1968)
Rabbit
3 times d-l, 5 dwk-’ total 100 km
40wk
ACL
Woo et al. (1979)
Swine
5.76kmh-‘, 1 hd-’ 7.92 kmh-‘, 30 min cod- ’ 5 dwk-’ 3.24.0 kmh-’ 15-20% grade 6&75 mind- ’
52
wk
MCL
Tipton (1979)
Monkey
Cabaud et al. (1980)
Rat
Wang et al. (1989)
Dog
1.8 km h-i, 8% grade 30mind-‘,6dwk-’ 1.8 km h-l, 8% grade 60mind-‘,6dwk-’ 3 kmh-i, 75 mind-’ 11 kg backpack Sdwk-’
Strain
rate
Tens.
strength
Max. load 116*
l%s-’
123
106 (138)*
20
wk
MCL LCL PT Achilles
91 82 141* 89
8wk
ACL
95%s-'
117*
8wk
ACL
95%s-'
109
42&557
wk MCL
ACL = Anterior cruciate ligament, MCL = Medial collateral ligament. LCL = Lateral cruciate ligament, PT = Patellar tendon.
0.7%s-'
97
110
714
ISB Keynote 60 l
0<0.05 (vs Control (llean+SE)
) 1-•
50
2 -
Lecture
T
40
u? g 0
30
5 ;
20
10
i
0
Control
30minld 3davslw 1
6Qnin/d 3daWw I
Exercise Fig. 10. Effects of duration
30min/d 6dayslw
(1,8km/h,
Normal
load of the rat anterior
Restressed
Period
cruciate
T (wk)
0
u0 8 2
\ -80
-
.Lz
----
100% stress-shielded
6
," I?
8%grade)
and frequency of exercise on maximum failure ligament (Cabaud et al., 1980).
70% stress-shielded
60min/d 6daWw I
-100
Fig. 11. Summary shielding,
L
of the experimental and stress increase
results on the effects of stress shielding, restressing after upon the structural properties of rabbit patellar tendons.
duration exercise regimen yielded the largest change of the maximum failure load in the rat anterior cruciate ligament (Fig. lo), although the effect was not so much. In addition, it is very interesting to see the results obtained by Wang et al. (1989),
the tendon dry weight and collagen concentration. They suggested that the biosynthesis and/or molecular assembly of proteoglycans might be affected by variations in mechanical stimuli exerted on the tendon.
which showed that a lifelong exercise training, say 42C557 weeks training, had little or no effect on the biomechanical properties of the canine medial collateral ligament. Vailas et al. (1985) showed in the male rat that voluntary exercise for 9 months significantly increased glycosaminoglycan concentration in the patellar tendon, but induced no changes
SUMMARY
The
in
stress
results
obtained
from
our
three
experiments
done
on
the rabbit patellar tendons are summarized in Fig. 11. Stress
ISB Keynote deprivation of 70% induced minimal and insignificant decrease of the structural strength (maximum load) of the patellar tendon, which indicates that the tendon can maintain the original strength even if stress is reduced to 30% ofthe normal stress. On the other hand, 100% stress shielding, namely non-stress condition, decreased the strength of the tendon very quickly and markedly. Even if the tendon strength was so much decreased by 100% stress shielding, it recovered to the control level if normal stress was applied again to the tendon for a long period of time. In the patellar tendon whose cross-sectional area was reduced to 75%, i.e. in 33% overstressed tendon, the structural strength was increased to the normal level of the whole intact tendon by the overstressing due to tissue hypertrophy. In the case of 100% overstressing induced by reducing the cross-sectional area to 50%, the structural strength increased in some tendons, but decreased in others. However, even if the strength increased, it remained much less than that of the normal whole tendon. These biomechanical changes occurred in response to stress alterations were also observed in the rabbit and canine anterior cruciate ligaments. In addition, these results were essentially similar to those obtained by other investigators. In conclusion, tendons and ligaments have the ability to adapt to stress alteration by changing the material properties and/or tissue dimensions if the extent of the stress alteration is within allowable ranges. Acknowledgement-This paper was presented as a keynote lecture under the title of ‘Remodeling of tendons and ligaments’ for the 14th Congress of the International Society of Biomechanics which was held in Paris on 48 July 1993. The author expresses his sincere thanks to Professors Simon Bouisset and Stephane Metral, and members of the Organizing Committee for inviting him to the Congress and giving an opportunity to present the lecture. Our experimental work was done at Hokkaido University. The author appreciates his collaborates, Drs Kiyoshi Kaneda, Kazunori Y&da, Noritaka Yamamoto, Kazunori Ohno, Harukazu Tohyama, Motoharu Keira, Tokifumi Majima, Takamasa Tsuchida, Hirohide Ishida, and Mr. Takahide Ishizaka, as well as his former students, Hiroyuki Kuriyama, Fumihiro Hayashi, and Takashi Fujii. This research work was supported financially in part by the Joint Research Project of the International Scientific Research Program (K. Hayashi et al., no. 01044009), the Grant-in-Aids for Scientific Research-Category B (K. Hayashi et al., no. 02452096), the Grant-in-Aids for Scientific Research on Priority Areas (K. Hayashi et al., nos. 04237102,04237103 and 04237104 for Biomechanics) and the Grant-in-Aids for Encouragement of Young Scientists (N. Yamamoto, nos. 03855013 and 04855014) from the Ministry of Education, Science and Culture of Japan.
REFERENCES
Akeson, W. H., Amiel, D. and Woo, S. L.-Y. (1980) Immobility effects on synovial joints-the pathomechanics of joint contracture. Biorheology 17, 95-l 10. Amiel, D., Akeson, W. H., Harwood, F. L. and Frank, C. B. (1983) Stress deprivation effect on metabolic turnover of the medial collateral ligament collagen-a comparison between nine- and 12-week immobilization Clin. Orthop. Rel. Res. 172, 265-270. Amiel, D., Schroeder, H. von and Akeson, W. H. (1990) The response of ligaments to stress deprivation and stress enhancement-biochemical studies. In Knee Ligaments: Structure. Function. Iniurv. and Reoair (Edited bv Daniel. D., Akeson, W. H.‘andtiConner, J.J., pp. 329-338. Raven Press, New York. Amiel, D., Woo, S. L.-Y., Harwood, F. L. and Akeson, W. H. (1982) The effect of immobilization on collagen turnover in connective tissue: a biochemical-biomechanical correlation. Acta Orthop. Stand. 53, 325-332.
Lecture Andrish, J. T. and Woods, L. D. (1984) Dacron anterior cruciate ligament reconstruction
715 augmentation in in dogs. Clin.
Orthop. 183,298-302. Biagini, G., Pugnaloni, A., Carboni, V., Riccio, M., Soragni, 0. and Bertani, M. (1991) Clinical-morphological analyses on tendons submitted to mechanical stress by tissue expander. Clin. Mat. 7, 233-239. Binkley, J. M. and Peat, M. (1986) The effects of immobilization on the ultrastructure and mechanical properties of the medial collateral ligament of rats. Clin. Orthop. Rel. Res. 203, 301-308. Cabaud, H. E., Chatty, A., Gildengorin, V. and Feltman, R. J. (1980) Exercise effects on the strength of the rat anterior cruciate ligament. Am. J. Sports Med. 8, 79-86. Cowin, S. C. (1993) Nature’s structural engineering of bone on a daily basis. In Theoretical and Applied Mechanics, 1992 (Edited by Bodner, S. R., Singer, J., Solan, A. and Hashin, Z.), pp. 145-160. Elsevier, Amsterdam. Fujii, T. (1993) Effects of mechanical environment on the biomechanical properties of patellar tendons. MS thesis, Hokkaido University Graduate School of Engineering, Sapporo. Fung, Y. C. (1990) Biomechanics-Motion. Flow, Stress, and Growth, pp. 499-546. Springer, New York. Gomez, M. A. (1988) The effect of tension on normal and healing medial collateral ligaments. PhD. thesis. University of California, San Diego. Hayashi, K. (1992) Residual stress in living material. In Residual Stresses 111 (Edited by Fujiwara, H., Abe, T. and Tanaka, K.), pp. 121-127. Elsevier Appl. Sci., London. Hayashi, K., Majima, T., Fujii, T., Yamamoto, N., Yasuda, K. and Kaneda, K. (1992) Effects of complete and partial stress shielding on the mechanical properties of rabbit patellar tendon. In Proc. 8th Meeting of the European Society of Biomechanics, p. 17, Rome. Havashi. K. and Matsumoto. T. (1994) Biomechanical response of aortic wall to hypertension in the rat. In Clinical Biomechanics and Related Research (Edited by Hirasawa, Y., Sledge, C. B. and Woo, S. L.-Y.), pp. 231-240, Springer, Tokyo. Hayashi, K. and Nakamura, T. (1985) Material test system for the evaluation of mechanical properties of biomaterials. J. Biomed. Mat. Res. 19, 133-144. Hayashi, K., Yamamoto, N., Ohno, K., Yasuda, K. and Kaneda, K. (1991) Mechanical properties of rabbit patellar tendon exposed to various stress condition. In Proc. 3rd U.S.A.China-Japan Conf. on Biomechanics, pp. 29930, Atlanta. Keira M., Yasuda, K., Hayashi, K., Yamamoto, N. and Kaneda, K. (1992) Mechanical properties of the canine anterior cruciate ligament chronically relaxed by elevation of the tibia1 insertion. Trans. Orthop. Res. Sot. 17, 661. Keira, M., Yasuda, K., Kaneda, K., Yamamoto, N. and Hayashi, K. Mechanical properties of the anterior cruciate ligament chronically relaxed by elevation of the tibia1 insertion. J. Orchop.-Res. (in press). Kennedy, J. C., Roth, J. H., Mendenhall. H. V. and Sanford, J. B. (1980) Intraarticular replacement in the anterior cruciate ligament-deficient knee. Am. J. Sports Med. 8, l-8. Klein, L., Player, J. S., Heiple, K. G., Bahniuk, E. and Goldberg, V. M. (1982) Isotopic evidence for resorption of soft tissues and bone in immobilized dogs. J. Bone Jt Surg. &IA, 2255230. Larsen, N. P., Forwood, M. R. and Parker, A. W. (1987) Immobilization and retraining of cruciate ligaments in the rat. Acta Orthop. Stand. 58,266264. Majima, T., Fujii, T., Yamamoto, N., Yasuda, K.. Kaneda, K. and Havashi. K. (1992a) Effects of complete and partial stress shielding on the mechanical properties of rabbit patellar tendon-role of fibroblasts. In Proc. 7th Int. Conf: on Biomedical Engineering, pp. 1133115, Singapore. Majima, T., Yasuda. K., Yamamoto, N., Hayashi, K. and Kaneda, K. (1992b) Effects of stress shielding on the mechanical properties of in situ frozen patellar tendon augmented with polyester artificial ligament. Trans. Orthop. Res. Sot. 17, 614.
716
ISB Keynote
Majima, T., Fujii, T.. Yasuda, K and Yamamoto, N. (1993) Effects of controlled stress shielding on the mechanical properties of the rabbit patellar tendon-role of fibroblasts. Trans. orthop. Res. Sot. 18, 365. Majima, T., Yasuda. K., Fujii, T., Yamamoto, N., Hayashi, K. and Kaneda, K. Biomechanical effects of stress-shielding of the rabbit patellar tendon depend upon the degree of stress reduction. J. Orthop. Res. (in press). Majima, T., Yasuda, K., Yamamoto, N., Kaneda, K. and Hayashi, K. (1994) Deterioration of mechanical properties of the autograft in controlled stress-shielded augmentation procedures: an experimental study with rabbit patellar tendon. Am. J. Sports Med. 22, 821-829. Matsumoto, T. and Hayashi, K. (1991) Mechanical response of rat aorta to hypertension. In 1991 Advances in Bioengineering (Edited by Vanderby, R. Jr.), pp. 631-634. ASME, New York. Matsumoto. T. and Hayashi, K. (1994) Mechanical and dimensional adaptation of rat aorta to hypertension. Trans. ASME, 3. Biomech. Engng 116, 278-283. Matsumoto, T. and Hayashi, K. Analysis of stress and strain distributions in hypertensive and normotensive rat aorta considering resdual strain. Trans. ASME, J. Biomech. Engng (in press). Meade, J. B. (1989) The adaptation of bone to mechanical stress: experimentation and current concepts. In Bone Mechanics (Edited by Cowin, S. C.), pp. 211-251. CRC Press, Boca Raton, FL. Nakagawa. Y., Totsuka, M., Sato, T., Fukuda, Y. and Hirota, K. (1989) Effect of disuse on the ultrastructure of the achilles tendon in rats. Eur. J. Appl. Physiol. 59, 239-242. Noyes, F. R. (1977) Functional properties of knee ligaments and alterations induced by immobilization. Clin. Orthop. Rel Res. 123,21&242. Noyes, F. R., Torvik, P. J., Hyde, W. B. and DeLucas, J. L. (1974) Biomechanics of ligament failure II. An analysis of immobilization, exercise, and reconditioning effects in primates. .I. Bone Jr Surg. 56A, 1406-1418. Ohno, K., Yasuda, K., Yamamoto, N. and Hayashi, K. (1991) Effects of stress shielding on the mechanical properties of normal and in situ frozen patellar tendon. Trans. orthop. Res. Sot. 16, 134. Ohno, K., K. Yasuda, K., Yamamoto, N., Kaneda, K. and Hayashi, K. (1993) Effects of complete stress-shielding on the mechanical properties and histology of in situ frozen patellar tendon. J. orthop. Res. 11, 592-602. Pattee, G. A. and Friedman, M. J. (1988) A review of autogenous intra-articular reconstruction of the anterior cruciate ligament. In Prosthetic Ligament Reconstruction of the Knee (Edited by Friedman, M. J. and Ferkel, R. D.), pp. 22-28. W. B. Saunders, Philadelphia. Tipton, C. M., Matthes, R. D., Vailas, A. C. and Schnoebelen, C. L. (1979) The response of the galago senegalensis to physical training. Comp. Biochem. Physiol. 63A, 29-36. Tipton, C. M., Vailas, A. C. and Matthes, R. D. (1986) Experimental studies on the influences of physical activity on ligaments, tendons and joints: a brief review. Acta Med. Stand. Suppl. 711, 157-168. Tohyama, H., Ohno, K., Yamamoto, N., Hayashi, K., Yasuda, K. and Kaneda, K. (1992) Stress-strain characteristics of in situ frozen and stress-shielded rabbit patellar tendon. Clin. Biomech. 7, 226-230. Vailas, A. C.. Pedrini, V. A., Pedrini-Mille, A. and Holloszy, J. 0. (1985) Patellar tendon matrix changes associated with aging and voluntary exercise. J. Appl. Physiol. 58, 1572-1576.
Lecture Viidik, A. (1968) Elasticity and tensile strength of the anterior cruciate ligament in rabbits as influenced by training. Acta Physiol. Stand. 74, 372-380. Wang, C. W., Weiss, J. A., Albright, J. P., Buckwalter, J. A. and Woo, S. L.-Y. (1989) The effects of long term exercise on the structural and mechanical properties of the canine medial collateral ligament. In 1989 Biomechanics Symp. (Edited by Torzilli, P. A. and Friedman, M. H.), pp. 69-72. ASME, New York. Woo, S. L.-Y., Gomez, M. A., Sites, T. J., Newton. P. O., Orlando, C. A. and Akeson, W. H. (1987) The biomechanical and biomophological changes in the medial collateral ligament of the rabbit after immobilization and remobilization. J. Bone Jt Surg. 69A, 120&1211. Woo, S. L.-Y., Harwood, F. L. and Akeson, W. H. (1982) The effect of immobilization on collagen turnover in connective tissue: a biochemical&biomechanical correlation. Acta orthop. Stand. 53, 325-332. Woo, S. L.-Y., Kuei, S. C., Gomez, M. A., Winters, J. M., Amiel, D. and Akeson, W. H. (1979) The effects of immobilization and exercise on the strength characteristics of bone-medial collateral ligament-bone complex. In 1979 Biomechanics Symp. (Edited by Buskirk, W. C. van), pp. 67-70. ASME, New York. Woo, S. L.-.Y., Wang, C. W., Newton, P. 0. and Lyon, R. M. (1990) The response of ligaments to stress deprivation and stress enhancement-biomechanical studies. In Knee Ligaments: Structure, Function, Injury, and Repair (Edited by Daniel, D., Akeson, W. H. and O’Conner, J.J.), pp. 337-350. Raven Press, New York. Yamamoto, N., Ohno, K., Kuriyama, H., Yasuda, K., Hayashi, K. and Kaneda, K. (1989) Effects of stress shielding on the mechanical properties of patellar tendon. In Tissue Engineering-1989 (Edited by Woo, S. L.-Y. and Seguchi, Y.), pp. 103-106. ASME, New York. Yamamoto, N., Hayashi, F. and Hayashi, K. (1992a) Mechanical response of rabbit anterior cruciate ligament to overloading. In Proc. 7th Inr. Conf on Biomedical Engineering, pp. 1 l&l 12, Singapore. Yamamoto, N., Hayashi, K. and Hayashi, F. (1992b) In viuo measurement of tension in the rabbit patellar tendon. Trans. Jap. Sot. Mech. Engng, Ser. A, 58, 1142-l 147. Yamamoto, N., Hayashi, K., Kuriyama, H., Ohno, K., Yasuda, K. and Kaneda, K. (1992~) Mechanical properties of the rabbit patellar tendon. Trans. ASME J. Biomech. Engng 114, 332-337. Yamamoto, N., Ohno, K., Hayashi, K., Kuriyama, H., Yasuda, K. and Kaneda, K. (1993) Effects of stress shielding on the mechanical properties of rabbit patellar tendon. Trans. ASME J. Biomech. Engng 115,23-28. Yamamoto, N., Hayashi, K., Kuriyama, H., Ohno, K., Yasuda, K. and Kaneda, K. Effects of restressing on the mechanical properties of stress-shielded patellar tendons in rabbits. Trans. ASME J. Biomech. Engng (in press). Yasuda, K. and Hayashi, K. (1994) Effects of stress shielding on autografts in augmentation procedures: experimental studies using the in situ frozen patellar tendon. In Clinical Biomechanics and Related Research (Edited by Hirasawa, Y., Sledge, C. B. and Woo, S. L.-Y.), pp. 3633379. Springer, Tokyo. Yoshiya, S., Andrish, J. T., Manley, M. T. and Kurosaka, M. (1986) Augmentation of anterior cruciate ligament reconstruction in dogs with prostheses of different stiffnesses. J. Orthop. Res. 4, 475485.
OOZl-9290(95)00163-8
ISB KEYNOTE
BIOMECHANICAL
J. Biomchanics, Vol. 29, No. 6, pp. 707-716, 1996 c 1996 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0021-9290/96 $15.00 + .oO
LECTURE
STUDIES OF THE REMODELING TENDONS AND LIGAMENTS
OF KNEE
JOINT
Kozaburo Hayashi Biomechanics Laboratory, Department of Mechanical Engineering, Faculty of Engineering Science, Osaka University, Toyonaka, Osaka 560, Japan Abstract-Living tissues and organs are dynamic and change their mechanical properties and structure in response to stressalteration as a phenomenon of functional adaptation and optimal operation. This phenomenon is called ‘Tissue Remodeling’, and Wolff s law on bone remodeling is widely known. Several recent studies have shown that fibrous connective tissues such as tendons and ligaments also have the ability of remodeling. However, relatively little is known about the stress and motion effects on tissue homeostasis in biological soft tissues. This article primarily deals with changes of the biomechanical properties of knee joint tendons and ligaments through a wide variety of treatment modalities, including stress deprivation, recovery after stress deprivation, and stress enhancement. The experimental results indicate that tendons and ligaments have an ability to adapt in response to the change of stress if the extent of stress alteration is within allowable ranges. Copyright 0 1996 Els&er Science Ltd.Keywords: Tendon; Ligament; Remodeling; Stress deprivation; Stress shielding; Stress enhancement: Immobilization; Remobilization; Exercise.
INTRODUCTION
Living tissues and organs are dynamic and adapt mechanically and structurally to alteration in function. They grow or resorb in response to change in mechanical environment as a phenomenon of functional adaptation and optimal operation (Fung, 1990; Hayashi, 1992). That is, living tissues and organs have an ability to homeostatically respond to mechanical demands. In normal life, almost all biological tissues and organs are always exposed to some forces after birth, and never experience with non-load condition. This phenomenon is essential to living tissues and organs, and does not exist in non-living materials. This kind of biomechanical phenomenon is called ‘Tissue Remodeling’, and Wolffs law on bone remodeling is well known (Fung, 1990). Tissue remodeling occurs during disuse and exercise. In addition, repair of injury and healing of autografts are also associated with tissue remodeling. Although the adaptation of bone to mechanical stress and bone remodeling have been studied extensively (Cowin, 1993; Meade, 1989), relatively little is known about the stress and motion effects on tissue homeostasis in biological soft tissues like tendons and ligaments. However, several recent studies have shown that these soft fibrous connective tissues also have the ability of remodeling. We have been doing a series of studies on the biomechanical, morphometrical, and histological responses of knee joint tendons and ligaments (Fujii, 1993; Hayashi et al., 1991, 1992; Keira et al., 1992, in press; Majima et al., 1992a,b, 1993, 1994, in press; Ohno et al., 1991, 1993; Tohyama et al., 1992; Yamamoto et al., 1989,1992a, 1993, in press; Yasuda and Hayashi, 1994) as well as arterial walls (Hayashi, 1992; Hayashi and Matsumoto, 1994; Matsumoto and Hayashi, 1991, 1994, in press) to stress alter-
Received in jinal form 23 September 1995. Address correspondence to: Kozaburo Hayashi, Ph.D. Department of Mechanical Engineering, Faculty of Engineering Science, Osaka University, Toyonaka, Osaka 560, Japan. 707
tion. This review paper primarily deals with the experimental findings obtained by us and others regarding changes in the biomechanical properties of knee joint tendons and ligaments through a wide variety of treatment modalities, including: (1) stress deprivation by immobilization, disuse, and stress-shielding, (2) reconditioning by remobilization and restressing,and (3) stress enhancement by increased tension and exercise training. Tipton et al. (1986) published a brief review regarding the experimental studies on the effectsof physical activity upon ligaments and tendons. Besides, Woo et al. (1990) wrote a review article on the similar subject, mainly focusing on their own studies. RESPONSE
TO STRESS
DEPRIVATION
Effects of stress deprivation on the biomechnanics of knee joint tendons and ligaments have so far been studied by the experiments of immobilizing or disusing animal knees (Akeson et al., 1980; Binkley and Peat, 1986; Klein et al., 1982; Larsen et al., 1987; Noyes, 1977; Noyes et al., 1974; Woo et al., 1979, 1982, 1987). Although immobilization and disuse decrease both stress and motion, we do not know the exact amount of the reduction of stress. Actually, stress applied to tendons and ligaments during immobilization or disuse is not always zero. As a more direct method for stress deprivation, we developed a novel method of stress shielding by which tension in the patellar tendon can be released completely under the condition of normal knee motion (Ohno et al., 1991; Yamamoto et .al.. __..__.- _. .... 1989). We have been applying this technique to the rabbit patellar tendon. After exposing the patellar tendon in each right knee, a stainless steel pin and a stainless steel screw were transversely inserted into the patella and in the tibia1 tubercle. respectively. Then, the patellar tendon was slackened b; drawing the patella toward the tibia1 tubercle, and this position was maintained with use of a flexible stainless steel wire installed between the pin and the screw (Fig. 1). Postoperatively, no immobilization treatment was applied, and all animals were allowed daily activities in cages. One to 6 weeks after surgery,
708
ISB Keynote
Lecture (Mean+S.E.)
40
T
,^
Control (n-16) Fig. 1. Method for complete stress shielding by which tension in the patellar tendon is released under condition of regular knee motion (Yamamoto et al., 1993).
/"
(MeapSE)
0
2 Strain
Fig. 2. Stress-strain non-treated, control
Control
6
4 E
8
(%)
curves of completely stress-shielded and patellar tendons in the rabbit (Yamamoto et al., 1993).
a patella-patellar tendon-tibia complex was excised from each knee. Tensile testing was carried out on the complex at a cross-head speed of 20mmmin-’ after measuring the cross-sectional area of the patellar tendon with an area micrometer (Yamamoto et al., 1992~). Strain in the tendon was determined using a video dimension analyzer (Hayashi and Nakamura, 1985). We chose the patellar tendon for this study because the distribution of force and tissue quality is fairly uniform through the tissue in this tendon (Yamamoto et al., 1992~). Another reason is that the patellar tendon is easily accessible for surgical procedure, which enables to develop a reproducible model for stress deprivation. The above-described stress shielding technique can make it possible for the tendon to be free from stress yet allow normal motion of the knee joint. In addition, this technique can be extended to develop a method for quantitatively controlling the amount of stress applied to the tendon (partial stress shielding) as described later in this article. Our previous studies showed that there were no inflammatory sideeffects of the stainless steel wire on the biomechanical properties of the patellar tendon.
1 wk (n-6)
2 wks (n-6)
3 wks (n-6)
6 wks (n-6)
Fig. 3. Cross-sectional area of completely stress-shielded and non-treated, control patellar tendons in the rabbit (Yamamoto et cd., 1993). Figure 2 demonstrates the averaged stress-strain curves for the completely stress-shielded and non-treated, control patellar tendons (Yamamoto et al., 1993). The slope of the linear portion of the curve decreased progressively and remarkably in the stress-shielded tendon, and reached a minimum value of about 9% of the control value after 3 weeks. Tensile strength was also decreased very rapidly and markedly by the stress shielding: for example, it decreased to about 50% at 1 week and to less than 10% at 2 weeks compared to the control tendon, but became almost constant thereafter. No significant change was observed in the elongation at failure. In contrast to the decrease of tensile strength. the cross-sectional area of the patellar tendon was markedly increased by the stress shielding during the period of 3 weeks after the treatment (Fig. 3, Yamamoto et al., 1993). The area increased to 231% at 3 weeks compared to the control area, although it decreased to 140% at 6 weeks. Maximum failure load was decreased to 26% of the control value by 2-week stress shielding; however, owing to the considerable increase in the cross-sectional area, the decrease of the maximum load was less than that of tensile strength. These biomechanical changes occurring in response to stress shielding were also observed in the canine anterior cruciate ligament to which a special experimental technique was applied for releasing tension in the ligament (Keira et nl., 1992. in press). To know the effects of the extent of stress reduction, we have extended the above-mentioned stress-shielding method to quantitatively control the magnitude of stress in the patellar tendon (Majima et al., 1992, in press). Instead of the stainless steel wire shown in Fig. 1, a polyester-mesh made artificial ligament was hooked between the patella and the tibia1 tubercle in parallel to the patellar tendon. It was then pulled and fixed using a steel clamp when load in the patellar tendon was reduced to about 30% of the normal force. Reduction of the load was monitored with a buckle transducer (Yamamoto et al., 1992b) temporarily attached to the patellar tendon. At the time of sacrifice, percentage ratios of the load shared by the partially stress-shielded tendons were, for example, about 33, 41, and 48% at 3, 6, and 12 weeks, respectively. These changes are attributable to the creep of the artificial ligament and/or the shortening of tendon length caused by tissue remodeling. Figure 4 demonstrates temporal changes of the tensile strength and maximum failure load of the partially (70%) stress-shielded patellar tendons together with those of the completely (100%) stress-shielded tendons, control tendons, and sham-operated tendons (Majima et al.. 1992a). The data for the tendons completely stress-shielded for 12 weeks are not shown in these figures mainly because the patella was fractured inside the body by this period and the data could not be obtained. In a fashion similar to the complete stress shielding, the partial stress shielding also significantly decreased the tensile strength of the patellar tendon: however, the decrease was much less than
ISB Keynote
m
Sham (n=6) l
m
;2;
7or
Control
z
800
uf
600
x 0
400
EE, ; z
P < 0.05
(VS
PSS (fl=6)
# P’ 0.05
CSS (n=6)
(Mean:SEi
Pwks
6wks
Zwks
6wks
(VS PSS)
12wks
0 12wks
Fig. 4. Temporal changes of tensile strength and maximum failure load in partially stress-shielded (PSS), completely stress-shielded (CSS), and sham-operated patellar tendons in the rabbit (Majima et al., 1992a).
in the case of strength of the was about 60 ated tendon. stress-shielded 2 and 6 weeks,
709
less reduction of the tensile strength, there were no significant differences in the maximum failure load among the partially stress-shielded tendons, sham-operated tendons, and control tendons throughout the experimental period. Figure 5 shows plotting of the cross-sectional area against the tensile strength for all the groups, where a broken line was drawn assuming that the product of the tensile strength and the cross-sectional area is equal to that of the averaged control values. The data obtained from the partially stress-shielded tendons fit to this curve fairly well; in the case of 70% stressshielding. the tendon seems to keep the maximum failure load at the normal level by compensating for the decrease of tensile strength by increasing the cross-sectional area. On the other hand, almost all the data obtained from the completely stressshielded tendons deviate much from this curve; the decrease of tensile strength in 100% stress-shielded tendons was too much to be compensated by the increase of the cross-sectional area. Histologically, no essential change appeared at 1 week in the completely stress-shielded tendons, but great changes were observed at 2 to 6 weeks (Yamamoto et al., 1993). That is, 100% stress shielding for more than 2 weeks changed the morphology of fibroblasts from spindle to round shape, and disordered the alignment of collagen fibers. Between 1 and 2 weeks, the number of fibroblasts increased remarkably to about four times as many as that in the control tendons. Their number was almost unchanged between 2 and 6 weeks after the treatment of stress shielding. In the partially stress-shielded tendons, we observed a fairly normal crimp pattern of collagen fibers as well as spindle shape of cells. but no round shape of fibroblasts throughout the experimental period (Fujii, 1993; Majima et al., 1992a, in press). This microstructure was much different from that observed in the completely stress-shielded tendons. Table 1 shows reported data regarding the effects of immobilization on the biomechanical properties of knee joint tendons and ligaments. For example, Noyes (1977) demonstrated in the primate that knee immobilization for 8 weeks decreased the maximum failure load of the anterior cruciate ligament to 78% of that in the non-treated, control ligament. Woo et al. (1987) reported that 9-week knee immobilization decreased the maximum load of the rabbit medial collateral ligament to 3 1% of the control value. These biomechanical studies indicate that the mechanical strength of knee joint ligaments is significantly reduced by immobilization. However, if these data are compared to our results obtained from the experiments of direct stress shielding, we can see that percentages of the reduction of maximum failure load caused by
Sham)
200
Control
Lecture
complete stress shielding. For example, tensile partially stress-shielded tendon at 2 and 6 weeks and 55%, respectively, of that in the sham-operThe cross-sectional area of the partially tendon increased to about 140% and 170% at respectively. Due to this hypertrophic change and
0 Control \ \
anAY= 792.4 (Control)
30-
l
Sham
a
PSS
m
css
l a
I
20 l
10 -
o-
0
---_
10
20
30 Tensile
40 strength
50
60 on
70
o
--
80
90
(tIPa)
Fig. 5. Cross-sectional area versus tensile strength in partially stress-shielded (PSS), completely stressshielded (CSS), and sham-operated patellar tendons in the rabbit. The broken line was drawn assuming that the product of tensile strength and cross-sectional area is equal to that of the averaged control values.
710
ISB Keynote Lecture
Table 1. Change of cross-sectional area and strength of tendons and ligaments by immobilization
Noyes (1977) Klein et al. (1982) Binkley and Peat (1986) Woo et al. (1987) Larsen et al. (1987)
(% control tissue, *p
Animal
Period
Tissue
Strain rate
Area
Monkey Dog Rat Rabbit Rabbit Rat Rat
8 wk 12wk 40d 9wk
66.2% s - l 60mms-’ 5 mmmin-’ 0.5% s-l 0.5%s-’
97
80*
89 78* 79*
38*
4wk 4wk
ACL ACL MCL MCL MCL ACL PCL
2wk 3 wk 2wk 3 wk
PT PT PT PT
20mmmin-’ 20mmmin-’ 20 mmmin-’ 20mmmin-’
209* 231* 173* 170*
13* 9* 55* 56*
12wk
Fuji (1993), Majima et al. (in press) 100% stress-shielded Rabbit Rabbit 70% stress-shielded Rabbit Rabbit
< 0.05)
Tensile strength Max. load 78* 44* 31* 29* 73* 88 26* 20* 94 95
ACL = Anterior cruciate ligament, MCL = Medial collateral ligament. PCL = Posterior cruciate ligament, PT = Patellar tendon.
immobilization are in between those induced by the 100% and 70% stress shielding. These results may indicate that tension in the ligament and tendon is not completely released by immobilization treatment, although it is reduced to less than 30% of a normal value. In addition, there are large differences in the change of the cross-sectional area between our experiments and the other studies. That is, immobilization slightly decreases the cross-sectional area, while direct stress shielding remarkably increases the area. The immobilization data shown in Table 1 were all obtained from ligaments. Response to stress deprivation may be different for ligaments and tendons. Further detailed studies are required to know the reason why the direct stress shielding-induced tissue hypertrophy in the patellar tendon. Biochemically, Amiel et al. (1982, 1983, 1990) observed that 9-week immobilization of the rabbit knee enhanced the production of new (immature) collagen as well as the degradation of old collagen, resulting in a net decrease of total collagen in the anterior cruciate ligament but no change of total collagen in the medial collateral ligament and the patellar tendon. On the other hand, Vailas et al. (1988) showed in the rat that hindlimb suspension for 28 days significantly decreased collagen and proteoglycan concentrations in the patellar tendon. By means of electron microscopy, Nakagawa et al. (1989) observed in the rat achilles tendon that 5-week suspension of hindlimb significantly decreased the total cross-sectional area of collagen fibers, and increased the relative percentage of thin collagen fibers. Disuse of hindlimb might have produced thin, immature collagen fibers and, at the same time, degradated thick, old collagen fibers. Additional work on the effects of stress deprivation upon the biochemistry and microstructure of tendons and ligaments is suggested.
the devices, and some extent of stress shielding occurs in the autografts. As an experimental mode1 of autografts, we developed a technique of instantaneously freezing the patellar tendon in situ to kill fibroblasts (Ohno et al., 1991, 1993; Yasuda and Hayashi, 1994). After freezing the patellar tendons in rabbits, we applied the same treatment of stress shielding as done to non-frozen tendons. In the case of complete stress shielding, the maximum failure load decreased somewhat slower than in the non-frozen tendons. However, the decrease was again remarkable, and the maximum load at 3 and 6 weeks was fairly similar to that obtained at 2-6 weeks in the non-frozen tendons (Ohno et al., 1993). In the case of partial stress shielding, the maximum failure load decreased to about 80% of the control value at 1 week. However, there were essentially no changes thereafter (Majima et al., 1993, 1994). Tensile strength changed in a fashion similar to the maximum failure load, although the decrease of the tensile strength was larger than that of the maximum load (Majima et al., 1992a, 1992b, 1994). These results indicate that we should apply some appropriate stress, say 30% or more than 30% of the normal stress, to autogenous grafts when they are augmented with synthetic devices. Otherwise, autografts markedly lose the strength. Besides the role of tension in maintaining autograft strength, we should consider additional factors that may contribute to the initial weakening of autograft patellar tendons, including the switch from an extra-synovial to an intra-synovial environment. Histologically, regardless of the extent of stress shielding, no cells were observed in the tendons which were in situ frozen and then stress-shielded for 2 weeks (Majima et al., 1992a, 1993, 1994; Ohno et al., 1991,1993; Yasuda and Hayashi, 1994). Even in the absence of fibroblasts during this period, the tensile strength of the tendons markedly decreased and hypertrophy occurred. That is, the patellar tendon responded to mechanical stress without cell. Although this is a very interesting phenomenon, the mechanisms are not yet clarified.
AUGMENTATION FOR THE RECONSTRUCTION OF KNEE JOINT LIGAMENTS RECOVERY
Stress shielding is one of the most important problems in the reconstruction of knee joint ligaments using augmentation techniques. A failed anterior cruciate ligament is often reconstructed using a portion of the patellar tendon as an autogenous graft (Pattee and Friedman, 1988). Immediately after transplantation, cellular necrosis occurs in the autograft, resulting in a tremendous decrease of the graft strength. As a method to solve this problem, augmentation devices made of synthetic materials are implanted in parallel with the grafts (Andrish and Woods, 1984; Kennedy et al., 1980; Yoshiya et al., 1986). In this case, tension applied to the grafts is partially shared or completely reduced by
FROM
STRESS
DEPRIVATION
Let me turn now the subject to recovery from stress deprivation. This issue has been mostly studied through remobilization after immoblization. Evaluation of the effect of joint remobilization on the functional properties of ligaments is of prime importance for the rehabilitation of previously immobilized joints. For this subject, we used a method of applying stress again to previously stress-shielded patellar tendons, i.e. restressing (Fujii, 1993; Yamamoto et al., in press). The stainless steel wire or the artificial ligament installed in parallel to the rabbit patellar
ISB Keynote Lecture
.&‘;a,,
711 Restressed (PSS*R) .-.--..---- __________ ---------.
-.-- *-- ---------o--- --o-----------o 70% stress-shielded
(PSS) Restressed (CSS+R)
60
‘OH’-
0
2
100% stress-shielded
4
6 Per lod
T
8 (week)
(CSS)
10
12
14
Fig. 6. Temporal percent changes of maximum failure load of the patellar tendons during stress shielding as well as during recovery from stress shielding (Fujii, 1993; Yamamoto et al., in press).
tendon for stress shielding (Fig. 1) was cut and removed after 2-week partial (70%) or complete (100%) stress-shielding, and normal stress was applied again to the tendon for the following 3 to 12 weeks. Tensile strength of the patellar tendon was progressively increased by restressing; the recovery of tensile strength was greater and faster in completely stress-shielded tendons than in partially stress-shielded tendons (Fujii, 1993). However, the tensile strength was significantly lower than the control value even if normal stress was applied to the tendons for 12 weeks. In contrast to the increase of tensile strength, the cross-sectional area of the tendons progressively decreased with time. The maximum failure load of the 70% stress-shielded tendons was remained at a control level throughout the period of restressing. In the completely stress-shielded tendons, the recovery of tensile strength was very fast and large, and the maximum failure load
finally returned to the control level after stressing for 12 weeks (Fig. 6). We should note that it takes much time for the tendons to recover the mechanical strength if it is once exposed to non-stress condition even for a short period of time. Table 2 demonstrates reported data on the percentage changes of the mechanical strength of ligaments induced by remobilization following immobilization. Woo et al. (1987) showed that the strength of the rabbit media1 collateral ligament immobilized for 9 weeks was increased markedly by the following 9-week remobilization, but it returned to only 79% of the original strength. Noyes (1977) immobilized rhesus monkeys in total body plaster casts for 8 weeks and, then, reconditioned by placing the animals in room size gang cages for 35 weeks or 72 weeks. By 8 weeks of immobilization, the maximum failure load of the anterior cruciate ligament was decreased by 39% in comparison
Table 2. Change of cross-sectional area and strength of tendons and ligaments by remobilization (% control tissues, ( ) % immobilized tissue)
Noyes (1977)
Larsen et al. (1987)
Woo et a/. (1987)
Animal
Immobil.
Monkey
8wk
Monkey
Tissue
Strain rate
35wk
ACL
66.2% s-’
8wk
12 wk
ACL
66.2%s-’
Rat
4wk
ACL
Rat
4wk
Rabbit
9wk
6wk (Swim) 6wk (Swim) 9wk
Rabbit
12wk
Remobil.
9wk
Area
PCL MCL MCL
0.5%s-’ 0.5%s-’
103
(121) (1::)
Fujii (1993), Yamamoto et al. (in press) 100% stress-shielded Rabbit 2wk 70% stress-shielded Rabbit
2wk
12wk
PT
20 mmmin-’
12wk
PT
20mmmin-’
143 (69) 123
(68) = Anterior cruciate ligament, MCL = Medial collateral ligament. PCL = Posterior cruciate ligament, PT = Patellar tendon.
ACL
Tens. strenth
Max. load
712
ISB Keynote Lecture l
**
0’0.001
(VS
Control)
## ~‘0.01 (vs Imnobilized) ### o
q
After
m
At sacrifice
removal
Mean:SD) L
800 2 tl? D z 5 E ';; P
600 Cont. (n=l6)
400 -
3 wks
6 wks
(n=5)
(n=6)
12 wks (n=6)
(Mean+S.E.)
200 -
Control
lmrobillzed
Remobilized
8 wks 35 wks 72 wks Fig. 7. Effects of reconditioning on maximum failure load of the anterior cruciate ligaments in the rhesus monkeys immobilized for 8 weeks in total body plaster casts (Noyes, 1977). 2
to the control group (Fig. 7). The maximum load in the specimens obtained from the 35-week reconditioned animals still showed 21% reduction in comparison to the control group, which indicates that a partial but incomplete recovery process had occurred. By reconditioning for 72 weeks, the maximum load returned to within 9% reduction from that in the control group; the difference between the control and the 72-week remobilized animals was not statistically significant. These results are similar to our results obtained from the restressed rabbit patellar tendons. From these results, we can say that prolonged recovery time is required for recovery from relatively brief period of stress deprivation. RESPONSE
TO STRESS
ENHANCEMENT
As stated above, return to normal stress levels greatly improve the biomechanical properties of previously stress-shielded or immobilized tendons and ligaments, although prolonged recovery time is necessary. How about the effectsof increased tension on normal tendons and ligaments? Connective tissues have been neglected by sports medicine and sports science researchers because their interests have been primarily directed on the cardiovascular and musculoskeletal systems(Tipton et nl., 1986). Recently, however, several animal studies have been done on the effects of exercise and training on tendon and ligament properties. Like the immobilization regimen, we cannot say the exact amount of tension increased by exercise and training. From an experimental perspective, it would be of interest if studies could be designed so that the forces acting directly on connective tissues are quantitatively increased (Tipton et al., 1986). As a direct and quantitative method, we have been using a technique of elevating stress level in tendons and ligaments by partial removal of the tissues (Hayashi et al., 1991; Yamamoto et al., 1992a). For example, we cut off both edges of the rabbit patellar tendon, and reduced the cross-sectional area of the remained tendon to about 75% or 50% of the original area. By this surgical treatment, 33% or 100% higher stress than the normal stress is applied to the remained tendon. Figure 8 demonstrates the results obtained from the patellar tendons stress-elevated to 133% of the normal stress. Although the tensile strength was slightly lower than the control value at 3 weeks, there were no significant differences in the stress-strain
Before removal
3 wks
6 wks
12 wks
(n=S)
(n=6)
(n-6)
(n=l?)
(Mean+S.E.l
Before
3 wks
6 wks
12 wks
removal
(n=5)
(n=6)
(n=6)
(n-17) (Mean+S.E.)
Fig. 8. Tensile strength, cross-sectional area, and maximum failure load of the rabbit patellar tendons stresselevated to 133% of normal stress.
relation and tensile strength among the control tendons and the tendons overstressed for 3 to 12 weeks. However, the crosssectional area was significantly increased by the overstressing if compared to each initial area. Eventually, the maximum failure load increased with increase in the cross-sectional area, and at 6 and 12 weeks there were no significant differences in the maximum load between the overstressed tendons and the control whole tendons. Figure 9 demonstrates the stress-strain curves obtained from the tendons overstressed to 2-fold of the normal stress. Depending on the mechanical characteristics, these tendons were divided into two groups, namely groups N and D. In group N, there was no change in the stress-strain behavior for 12 weeks, while the slope of the curve and tensile strength progressively decreased with time in group D. There was no histological difference between the group N and control tendons. In group D, on the other hand, there were a great number of fibroblasts, and breakage of collagen bundles was observed occasionally. In group N, there was almost no change in the tensile strength. The cross-sectional area was increased by the stress elevation, which increased the maximum failure load. The
ISB Keynote Lecture Stress-elevated
70 r l
Control
-r
! $’
6.
A
3wks(n=4)
n
6wksin=4)
4
result, the maximum load was maintained at the level obtained immediately after the tissue removal, i.e. 50% of the maximum load in the normal tendons. Separately from the above-mentioned experiments, we overstressed the anterior cruciate ligaments in rabbits for 3 to 6 weeks after reducing their cross-sectional areas by cutting off the medial or lateral l/2 bundles along the longitudinal axis (Yamamoto et al., 1992a). In vitro anterior-posterior drawer tests performed on the knees harvested from the other control rabbits indicated that tension applied to the remaining medial portion was increased to 13&150% of the normal level by the removal of the medial l/2 bundle, and that tension in the lateral portion was increased to 40&800% by the removal of the lateral l/2 bundle. This 3&50% overstressing induced no significant changes in the mechanical properties and dimensions of the medial portion of the anterior cruciate ligament. On the otherhand, the mechanical properties of the lateral bundle were significantly changed by the 300-700% overstressing: the tangent modulus and stiffness decreased to 60 and 46% of the control values, respectively, after 6 weeks of overstressing. These results indicate that knee joint ligaments and tendons seem to have an ability to adapt to overstressing within a certain range, i.e. if stressis less than 200% of the normal level; however, they cannot adapt if stress exceeds this limit. Gomez (1988) inserted a 1.6 mm diameter stainless steel pin underneath the rabbit medial collateral ligament to increase load and stress in the ligament from 2- to 3.5fold compared to the control ligament. This stress elevation increased the maximum load by 26% at 6 weeks, although this difference disappered at 12 weeks. Ultrastructurally, Biagini er al. (1991) observed the presence of areas having a high number of small diameter collagen fibrils in the clinically expanded extensor tendon. Table 3 shows reported data for the effects of exercise and training upon the strength of tendons and ligaments. Although the kind and extent of exercise and training are quite different among those studies, we can see that exercise and training induce minimal effectson the strength of tendons and ligaments. Cabaud et al., (1980) showed that higher-frequency and shorter-
to 200%
(n-18)
Group
N
12wksCn=4)
(MeantSE)
50
I
-0UD il
0
0
4
2 Strain
12wksln=S)
6 E
713
8
(%)
Fig. 9. Stress-strain curves of the rabbit patellar tendons overstressed to 200% of normal stress. These tendons are divided into two groups: group N and group D.
maximum load at 12 weeks increased by 40% in comparison to that obtained immediately after the partial removal of tissue. However, it was still about 70% of that of the whole tendon in the control knee. In group D, on the other hand, the tensile strength progressively decreased with time. Contrary to this, the cross-sectional area of the tendon increased markedly. As the
Table 3. Change of strength of tendons and ligaments by exercise (% control tissue, *p < 0.05, ( ) = normalized by body weight) Animal
Exercise
Period
Tissue
Viidik (1968)
Rabbit
3 times d-l, 5 dwk-’ total 100 km
40wk
ACL
Woo et al. (1979)
Swine
5.76kmh-‘, 1 hd-’ 7.92 kmh-‘, 30 min cod- ’ 5 dwk-’ 3.24.0 kmh-’ 15-20% grade 6&75 mind- ’
52
wk
MCL
Tipton (1979)
Monkey
Cabaud et al. (1980)
Rat
Wang et al. (1989)
Dog
1.8 km h-i, 8% grade 30mind-‘,6dwk-’ 1.8 km h-l, 8% grade 60mind-‘,6dwk-’ 3 kmh-i, 75 mind-’ 11 kg backpack Sdwk-’
Strain
rate
Tens.
strength
Max. load 116*
l%s-’
123
106 (138)*
20
wk
MCL LCL PT Achilles
91 82 141* 89
8wk
ACL
95%s-'
117*
8wk
ACL
95%s-'
109
42&557
wk MCL
ACL = Anterior cruciate ligament, MCL = Medial collateral ligament. LCL = Lateral cruciate ligament, PT = Patellar tendon.
0.7%s-'
97
110
714
ISB Keynote 60 l
0<0.05 (vs Control (llean+SE)
) 1-•
50
2 -
Lecture
T
40
u? g 0
30
5 ;
20
10
i
0
Control
30minld 3davslw 1
6Qnin/d 3daWw I
Exercise Fig. 10. Effects of duration
30min/d 6dayslw
(1,8km/h,
Normal
load of the rat anterior
Restressed
Period
cruciate
T (wk)
0
u0 8 2
\ -80
-
.Lz
----
100% stress-shielded
6
," I?
8%grade)
and frequency of exercise on maximum failure ligament (Cabaud et al., 1980).
70% stress-shielded
60min/d 6daWw I
-100
Fig. 11. Summary shielding,
L
of the experimental and stress increase
results on the effects of stress shielding, restressing after upon the structural properties of rabbit patellar tendons.
duration exercise regimen yielded the largest change of the maximum failure load in the rat anterior cruciate ligament (Fig. lo), although the effect was not so much. In addition, it is very interesting to see the results obtained by Wang et al. (1989),
the tendon dry weight and collagen concentration. They suggested that the biosynthesis and/or molecular assembly of proteoglycans might be affected by variations in mechanical stimuli exerted on the tendon.
which showed that a lifelong exercise training, say 42C557 weeks training, had little or no effect on the biomechanical properties of the canine medial collateral ligament. Vailas et al. (1985) showed in the male rat that voluntary exercise for 9 months significantly increased glycosaminoglycan concentration in the patellar tendon, but induced no changes
SUMMARY
The
in
stress
results
obtained
from
our
three
experiments
done
on
the rabbit patellar tendons are summarized in Fig. 11. Stress
ISB Keynote deprivation of 70% induced minimal and insignificant decrease of the structural strength (maximum load) of the patellar tendon, which indicates that the tendon can maintain the original strength even if stress is reduced to 30% ofthe normal stress. On the other hand, 100% stress shielding, namely non-stress condition, decreased the strength of the tendon very quickly and markedly. Even if the tendon strength was so much decreased by 100% stress shielding, it recovered to the control level if normal stress was applied again to the tendon for a long period of time. In the patellar tendon whose cross-sectional area was reduced to 75%, i.e. in 33% overstressed tendon, the structural strength was increased to the normal level of the whole intact tendon by the overstressing due to tissue hypertrophy. In the case of 100% overstressing induced by reducing the cross-sectional area to 50%, the structural strength increased in some tendons, but decreased in others. However, even if the strength increased, it remained much less than that of the normal whole tendon. These biomechanical changes occurred in response to stress alterations were also observed in the rabbit and canine anterior cruciate ligaments. In addition, these results were essentially similar to those obtained by other investigators. In conclusion, tendons and ligaments have the ability to adapt to stress alteration by changing the material properties and/or tissue dimensions if the extent of the stress alteration is within allowable ranges. Acknowledgement-This paper was presented as a keynote lecture under the title of ‘Remodeling of tendons and ligaments’ for the 14th Congress of the International Society of Biomechanics which was held in Paris on 48 July 1993. The author expresses his sincere thanks to Professors Simon Bouisset and Stephane Metral, and members of the Organizing Committee for inviting him to the Congress and giving an opportunity to present the lecture. Our experimental work was done at Hokkaido University. The author appreciates his collaborates, Drs Kiyoshi Kaneda, Kazunori Y&da, Noritaka Yamamoto, Kazunori Ohno, Harukazu Tohyama, Motoharu Keira, Tokifumi Majima, Takamasa Tsuchida, Hirohide Ishida, and Mr. Takahide Ishizaka, as well as his former students, Hiroyuki Kuriyama, Fumihiro Hayashi, and Takashi Fujii. This research work was supported financially in part by the Joint Research Project of the International Scientific Research Program (K. Hayashi et al., no. 01044009), the Grant-in-Aids for Scientific Research-Category B (K. Hayashi et al., no. 02452096), the Grant-in-Aids for Scientific Research on Priority Areas (K. Hayashi et al., nos. 04237102,04237103 and 04237104 for Biomechanics) and the Grant-in-Aids for Encouragement of Young Scientists (N. Yamamoto, nos. 03855013 and 04855014) from the Ministry of Education, Science and Culture of Japan.
REFERENCES
Akeson, W. H., Amiel, D. and Woo, S. L.-Y. (1980) Immobility effects on synovial joints-the pathomechanics of joint contracture. Biorheology 17, 95-l 10. Amiel, D., Akeson, W. H., Harwood, F. L. and Frank, C. B. (1983) Stress deprivation effect on metabolic turnover of the medial collateral ligament collagen-a comparison between nine- and 12-week immobilization Clin. Orthop. Rel. Res. 172, 265-270. Amiel, D., Schroeder, H. von and Akeson, W. H. (1990) The response of ligaments to stress deprivation and stress enhancement-biochemical studies. In Knee Ligaments: Structure. Function. Iniurv. and Reoair (Edited bv Daniel. D., Akeson, W. H.‘andtiConner, J.J., pp. 329-338. Raven Press, New York. Amiel, D., Woo, S. L.-Y., Harwood, F. L. and Akeson, W. H. (1982) The effect of immobilization on collagen turnover in connective tissue: a biochemical-biomechanical correlation. Acta Orthop. Stand. 53, 325-332.
Lecture Andrish, J. T. and Woods, L. D. (1984) Dacron anterior cruciate ligament reconstruction
715 augmentation in in dogs. Clin.
Orthop. 183,298-302. Biagini, G., Pugnaloni, A., Carboni, V., Riccio, M., Soragni, 0. and Bertani, M. (1991) Clinical-morphological analyses on tendons submitted to mechanical stress by tissue expander. Clin. Mat. 7, 233-239. Binkley, J. M. and Peat, M. (1986) The effects of immobilization on the ultrastructure and mechanical properties of the medial collateral ligament of rats. Clin. Orthop. Rel. Res. 203, 301-308. Cabaud, H. E., Chatty, A., Gildengorin, V. and Feltman, R. J. (1980) Exercise effects on the strength of the rat anterior cruciate ligament. Am. J. Sports Med. 8, 79-86. Cowin, S. C. (1993) Nature’s structural engineering of bone on a daily basis. In Theoretical and Applied Mechanics, 1992 (Edited by Bodner, S. R., Singer, J., Solan, A. and Hashin, Z.), pp. 145-160. Elsevier, Amsterdam. Fujii, T. (1993) Effects of mechanical environment on the biomechanical properties of patellar tendons. MS thesis, Hokkaido University Graduate School of Engineering, Sapporo. Fung, Y. C. (1990) Biomechanics-Motion. Flow, Stress, and Growth, pp. 499-546. Springer, New York. Gomez, M. A. (1988) The effect of tension on normal and healing medial collateral ligaments. PhD. thesis. University of California, San Diego. Hayashi, K. (1992) Residual stress in living material. In Residual Stresses 111 (Edited by Fujiwara, H., Abe, T. and Tanaka, K.), pp. 121-127. Elsevier Appl. Sci., London. Hayashi, K., Majima, T., Fujii, T., Yamamoto, N., Yasuda, K. and Kaneda, K. (1992) Effects of complete and partial stress shielding on the mechanical properties of rabbit patellar tendon. In Proc. 8th Meeting of the European Society of Biomechanics, p. 17, Rome. Havashi. K. and Matsumoto. T. (1994) Biomechanical response of aortic wall to hypertension in the rat. In Clinical Biomechanics and Related Research (Edited by Hirasawa, Y., Sledge, C. B. and Woo, S. L.-Y.), pp. 231-240, Springer, Tokyo. Hayashi, K. and Nakamura, T. (1985) Material test system for the evaluation of mechanical properties of biomaterials. J. Biomed. Mat. Res. 19, 133-144. Hayashi, K., Yamamoto, N., Ohno, K., Yasuda, K. and Kaneda, K. (1991) Mechanical properties of rabbit patellar tendon exposed to various stress condition. In Proc. 3rd U.S.A.China-Japan Conf. on Biomechanics, pp. 29930, Atlanta. Keira M., Yasuda, K., Hayashi, K., Yamamoto, N. and Kaneda, K. (1992) Mechanical properties of the canine anterior cruciate ligament chronically relaxed by elevation of the tibia1 insertion. Trans. Orthop. Res. Sot. 17, 661. Keira, M., Yasuda, K., Kaneda, K., Yamamoto, N. and Hayashi, K. Mechanical properties of the anterior cruciate ligament chronically relaxed by elevation of the tibia1 insertion. J. Orchop.-Res. (in press). Kennedy, J. C., Roth, J. H., Mendenhall. H. V. and Sanford, J. B. (1980) Intraarticular replacement in the anterior cruciate ligament-deficient knee. Am. J. Sports Med. 8, l-8. Klein, L., Player, J. S., Heiple, K. G., Bahniuk, E. and Goldberg, V. M. (1982) Isotopic evidence for resorption of soft tissues and bone in immobilized dogs. J. Bone Jt Surg. &IA, 2255230. Larsen, N. P., Forwood, M. R. and Parker, A. W. (1987) Immobilization and retraining of cruciate ligaments in the rat. Acta Orthop. Stand. 58,266264. Majima, T., Fujii, T., Yamamoto, N., Yasuda, K.. Kaneda, K. and Havashi. K. (1992a) Effects of complete and partial stress shielding on the mechanical properties of rabbit patellar tendon-role of fibroblasts. In Proc. 7th Int. Conf: on Biomedical Engineering, pp. 1133115, Singapore. Majima, T., Yasuda. K., Yamamoto, N., Hayashi, K. and Kaneda, K. (1992b) Effects of stress shielding on the mechanical properties of in situ frozen patellar tendon augmented with polyester artificial ligament. Trans. Orthop. Res. Sot. 17, 614.
716
ISB Keynote
Majima, T., Fujii, T.. Yasuda, K and Yamamoto, N. (1993) Effects of controlled stress shielding on the mechanical properties of the rabbit patellar tendon-role of fibroblasts. Trans. orthop. Res. Sot. 18, 365. Majima, T., Yasuda. K., Fujii, T., Yamamoto, N., Hayashi, K. and Kaneda, K. Biomechanical effects of stress-shielding of the rabbit patellar tendon depend upon the degree of stress reduction. J. Orthop. Res. (in press). Majima, T., Yasuda, K., Yamamoto, N., Kaneda, K. and Hayashi, K. (1994) Deterioration of mechanical properties of the autograft in controlled stress-shielded augmentation procedures: an experimental study with rabbit patellar tendon. Am. J. Sports Med. 22, 821-829. Matsumoto, T. and Hayashi, K. (1991) Mechanical response of rat aorta to hypertension. In 1991 Advances in Bioengineering (Edited by Vanderby, R. Jr.), pp. 631-634. ASME, New York. Matsumoto. T. and Hayashi, K. (1994) Mechanical and dimensional adaptation of rat aorta to hypertension. Trans. ASME, 3. Biomech. Engng 116, 278-283. Matsumoto, T. and Hayashi, K. Analysis of stress and strain distributions in hypertensive and normotensive rat aorta considering resdual strain. Trans. ASME, J. Biomech. Engng (in press). Meade, J. B. (1989) The adaptation of bone to mechanical stress: experimentation and current concepts. In Bone Mechanics (Edited by Cowin, S. C.), pp. 211-251. CRC Press, Boca Raton, FL. Nakagawa. Y., Totsuka, M., Sato, T., Fukuda, Y. and Hirota, K. (1989) Effect of disuse on the ultrastructure of the achilles tendon in rats. Eur. J. Appl. Physiol. 59, 239-242. Noyes, F. R. (1977) Functional properties of knee ligaments and alterations induced by immobilization. Clin. Orthop. Rel Res. 123,21&242. Noyes, F. R., Torvik, P. J., Hyde, W. B. and DeLucas, J. L. (1974) Biomechanics of ligament failure II. An analysis of immobilization, exercise, and reconditioning effects in primates. .I. Bone Jr Surg. 56A, 1406-1418. Ohno, K., Yasuda, K., Yamamoto, N. and Hayashi, K. (1991) Effects of stress shielding on the mechanical properties of normal and in situ frozen patellar tendon. Trans. orthop. Res. Sot. 16, 134. Ohno, K., K. Yasuda, K., Yamamoto, N., Kaneda, K. and Hayashi, K. (1993) Effects of complete stress-shielding on the mechanical properties and histology of in situ frozen patellar tendon. J. orthop. Res. 11, 592-602. Pattee, G. A. and Friedman, M. J. (1988) A review of autogenous intra-articular reconstruction of the anterior cruciate ligament. In Prosthetic Ligament Reconstruction of the Knee (Edited by Friedman, M. J. and Ferkel, R. D.), pp. 22-28. W. B. Saunders, Philadelphia. Tipton, C. M., Matthes, R. D., Vailas, A. C. and Schnoebelen, C. L. (1979) The response of the galago senegalensis to physical training. Comp. Biochem. Physiol. 63A, 29-36. Tipton, C. M., Vailas, A. C. and Matthes, R. D. (1986) Experimental studies on the influences of physical activity on ligaments, tendons and joints: a brief review. Acta Med. Stand. Suppl. 711, 157-168. Tohyama, H., Ohno, K., Yamamoto, N., Hayashi, K., Yasuda, K. and Kaneda, K. (1992) Stress-strain characteristics of in situ frozen and stress-shielded rabbit patellar tendon. Clin. Biomech. 7, 226-230. Vailas, A. C.. Pedrini, V. A., Pedrini-Mille, A. and Holloszy, J. 0. (1985) Patellar tendon matrix changes associated with aging and voluntary exercise. J. Appl. Physiol. 58, 1572-1576.
Lecture Viidik, A. (1968) Elasticity and tensile strength of the anterior cruciate ligament in rabbits as influenced by training. Acta Physiol. Stand. 74, 372-380. Wang, C. W., Weiss, J. A., Albright, J. P., Buckwalter, J. A. and Woo, S. L.-Y. (1989) The effects of long term exercise on the structural and mechanical properties of the canine medial collateral ligament. In 1989 Biomechanics Symp. (Edited by Torzilli, P. A. and Friedman, M. H.), pp. 69-72. ASME, New York. Woo, S. L.-Y., Gomez, M. A., Sites, T. J., Newton. P. O., Orlando, C. A. and Akeson, W. H. (1987) The biomechanical and biomophological changes in the medial collateral ligament of the rabbit after immobilization and remobilization. J. Bone Jt Surg. 69A, 120&1211. Woo, S. L.-Y., Harwood, F. L. and Akeson, W. H. (1982) The effect of immobilization on collagen turnover in connective tissue: a biochemical&biomechanical correlation. Acta orthop. Stand. 53, 325-332. Woo, S. L.-Y., Kuei, S. C., Gomez, M. A., Winters, J. M., Amiel, D. and Akeson, W. H. (1979) The effects of immobilization and exercise on the strength characteristics of bone-medial collateral ligament-bone complex. In 1979 Biomechanics Symp. (Edited by Buskirk, W. C. van), pp. 67-70. ASME, New York. Woo, S. L.-.Y., Wang, C. W., Newton, P. 0. and Lyon, R. M. (1990) The response of ligaments to stress deprivation and stress enhancement-biomechanical studies. In Knee Ligaments: Structure, Function, Injury, and Repair (Edited by Daniel, D., Akeson, W. H. and O’Conner, J.J.), pp. 337-350. Raven Press, New York. Yamamoto, N., Ohno, K., Kuriyama, H., Yasuda, K., Hayashi, K. and Kaneda, K. (1989) Effects of stress shielding on the mechanical properties of patellar tendon. In Tissue Engineering-1989 (Edited by Woo, S. L.-Y. and Seguchi, Y.), pp. 103-106. ASME, New York. Yamamoto, N., Hayashi, F. and Hayashi, K. (1992a) Mechanical response of rabbit anterior cruciate ligament to overloading. In Proc. 7th Inr. Conf on Biomedical Engineering, pp. 1 l&l 12, Singapore. Yamamoto, N., Hayashi, K. and Hayashi, F. (1992b) In viuo measurement of tension in the rabbit patellar tendon. Trans. Jap. Sot. Mech. Engng, Ser. A, 58, 1142-l 147. Yamamoto, N., Hayashi, K., Kuriyama, H., Ohno, K., Yasuda, K. and Kaneda, K. (1992~) Mechanical properties of the rabbit patellar tendon. Trans. ASME J. Biomech. Engng 114, 332-337. Yamamoto, N., Ohno, K., Hayashi, K., Kuriyama, H., Yasuda, K. and Kaneda, K. (1993) Effects of stress shielding on the mechanical properties of rabbit patellar tendon. Trans. ASME J. Biomech. Engng 115,23-28. Yamamoto, N., Hayashi, K., Kuriyama, H., Ohno, K., Yasuda, K. and Kaneda, K. Effects of restressing on the mechanical properties of stress-shielded patellar tendons in rabbits. Trans. ASME J. Biomech. Engng (in press). Yasuda, K. and Hayashi, K. (1994) Effects of stress shielding on autografts in augmentation procedures: experimental studies using the in situ frozen patellar tendon. In Clinical Biomechanics and Related Research (Edited by Hirasawa, Y., Sledge, C. B. and Woo, S. L.-Y.), pp. 3633379. Springer, Tokyo. Yoshiya, S., Andrish, J. T., Manley, M. T. and Kurosaka, M. (1986) Augmentation of anterior cruciate ligament reconstruction in dogs with prostheses of different stiffnesses. J. Orthop. Res. 4, 475485.