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The response of joints to impact loading — II In vivo behavior of subchondral bone
J Bwtnrc~homx.
192.
Vol. S. pp. 267-272.
Pergamm
Press.
Printed in Great Britain
THE IN VII/O Department
SHELDON R. SIMON: and ERIC L. RADINS of Orthopedic Surgery, Harvard Medical School, Children’s Hospital Center, Boston, Massachusetts 021 IS, U.S.A.
Medical
and
Massachusetts
IGOR L. PAULQ and ROBERT M. ROSE11 Institute of Technology, Cambridge. Massachusetts 02 139. U.S.A.
Abstract-The knee joints of live guinea pigs, subjected to repeated longitudinal impaction. developed obvious cartilage degeneration over a 3 week period. In vitro tests had previously shown that articular cartilage is particularly susceptible to injury from impact loading and that subchondral bone acts as a cushion to protect the overlying cartilage from damage during such loading. Associated with. and slightly preceding the earliest cartilage changes, as judged histochemicaliy, was a stiffening of the underlying subchondraf bone. The bone stiffness measurements returned to within the normal range as the cartilage degeneration progressed. INTRODUCTION
joints basically function as bearings, allowing vertebrates ease of motion with considerable flexibility and stability. Considering the stresses under which joints function. they are remarkably wear resistant. Although articular cartilage is extremely resistant to cyclic shear stress even under high loads, this tissue has been shown to be very susceptible to repetitive longitudinal loading (Radin and Paul, 1971). Subchondral bone has been experimentalLy shown to function effectively as a shock absorber (Physick as quoted by Wistar, 1827: Evans and Ring, 1961: McElhaney and Byars, 1956; Radin and Paul, 1970). It would thus be in a position to help protect its overlying articular cartilage from longitudinal impact loads. If the subchondral ‘cushion’ does fail in uivo, one might expect articular cartilage degeneration to follow close behind. This paper will report SYNOWAL
on the subchondral bone and articular cartilage changes resulting from the repetitive loading of the joints of live animals. METHODS
Young adult (12- 14 month old) male English short-haired guinea pigs were chosen as the experimental animal. An impaction table was made by mounting a piece of plywood on a metal plate which was cyclically elevated and depressed 0.4 cm by a motor-driven eccentric shaft. The guinea pigs were suspended in a rack above the impaction table in such a way that they could not sit down. The animals were held in the rack so that their fully extended hind legs almost touched the vibrating table. Each guinea pig was then fitted with long leg methacrylate splints which held the knees in maximum extension and the ankles in neutral. The right splint had an extension which was attached to the vibrating table and
*Received 6 May I97 1. torthopedic Research Fellow. *Assistant Professor. $Associate Professor of Mechanical Engineering. l/Associate Professor of Metallurgy and Materials Science. 267
268
S. R. SIMON,
E. L. RADIN,
I. L. PAUL
and R M. ROSE
conducted the impact load to the animal’s Groups of animals were sacrificed at daily heel {Fig. I). This was the experimental side. intervals from 3-7 days then weekly to 3 The let? leg was held in a splint which kept the weeks. All groups contained at least 5 animals. knee in maximal extension but the foot com- Upon sacrifice the animals’ knees were displetely off the vibrating table. The left knee of articulated, their distal femurs and synovial each animal therefore acted as the control. tissue were histologically evaluated, and stiffThe splints were applied just before the ness measurements were carried out on the impaction period and removed immediately proximal tibias. The distal femurs were immediately fixed in upon its completion. Once accustomed to the splints the animals were not bothered by the formalin, then decalcified in 4% fotiic acid, impacting procedure. They were allowed to stained with Safranin-0 and examined microrun free in their cages the remainder of the scopically. This stain geographically and time. They were initially hesitant to walk for a quantitatively demonstrates losses of mucofew hours after impaction. As the experiment polysaccharide from articular cartilage (Rosenprogressed, they protected their right hind berg, 1970). Such a loss, preferentially at the legs more and more. Any animal who devel- cartilage surface, is felt to be the first recognizoped significant pressure sores, infections, or able cartilaginous change in degenerative systemic illness was excluded from the study, joint disease (Barland et al. 1966; Bollet, All animals were examined twice a week by a 1967). The synovium was studied in 6 P veterinarian to insure their continued good sections, mounted in paraffin, and stained with hematoxylin and eosin. health. The legs below the knee were frozen to be The table was vibrated at 1500 c/m. Strain gauges affixed to representative splints at thawed just before mechanical testing. At that various positions on the table showed the time their proximal tibias were freed of all impaction force to approximate the weight of soft tissue. The tibial shaft was cut across the guinea pig (1- 1.23 kg). These strain gauge about O-6cm below the knee and the right and measurements were repeated at regular inter- left specimens mounted side by side on vals throughout the experiment and demon- adjoining plates in a cryostat, articular side strated no significant variance (& Ci-1 kg) _ up. The diapbyseal bases of these specimens The animals were run daily for I5 min. were adjusted so that both pieces had exactly
SIDE
VIEW
REAR
VIEW
Fig. I. Guinea pig in the rack wearing bilateral long-leg splints. The splint on the right has a plug which extends from the heel of the animal to the impaction table. This transmits the impulses from the table to the guinea pig’s right lower extremity. The left leg is held in a splint which makes no contact with the table.
RESPONSE
OF JOINTS
TO IMPACT
the same orientation in the cryostat. The articular cartilage was then removed a few microns at a time. As soon as all articular cartilage had been removed from both specimens, they were mounted on the same plate of the cryostat, articular side down. and the remnants of diaphysis and epiphyseal plate were removed from both specimens at the same time. This gave us specimens equal in thickness from each animal as measured from the subchondral plate (O-07-0.13 cm). These thin discs of subchondral bone were then subjected to an impact load (1.08 kg dropped 0.16 cm) to determine their response. The impacting technique as well as the force and deflection measurement methods have been previously described (Radin et al. 1970). The plugs were subjected to known impact loads in a reproducible manner. With this equipment the maximum initial strain rates applied were approximately 670 per centlsec for cartilage plugs and about 1 IO per cent/set for bone plugs. The force was registered on a force transducer:* the defiection, by a linear variable differential transformer:: and both values were displayed on an oscilloscope as a function of time and photographed. An ‘equivalent stiffness’ value was defined as the ratio of the measured peak force over the measured peak deflection under identical impact condirions. This value was felt to be a
LOADING-II
769
more meaningful measurement of the significant mechanical properties of the specimens than the relative energy absorbing previously used, since we are interested in the change of stiffness which determines the peak force during impact loading. Although the paired bone specimens from each animal were identical in size and shape, there was some unavoidable variation from animal to animal. To obtain a meaningful relative value for each animal, a ‘stiffness ratio’ was calculated by dividing the stiffness of the right (experimental) plug over that of the left (control). A few animals were run for 6 weeks. Because of the development of pressure sores, this group was too small to be confidently gauged histologically or mechanically. but was examined grossly. RESULTS
The ‘stiffness ratios’ for each of the groups were averaged. These values and their statistical distribution are presented in Table 1. Animals kept in their cages and not subjected to impaction maintained a l-01 (2 O-11) ‘stiffness ratio’ throughout the experiment. The first alterations in bone stiffness occurred at 3 days. The bone became less able to attenuate peak force and less deformable, i.e. stiffer, on the experimental side. However, it was not until the 5th day that the bone stiffness
Table I. Stiffness ratios
Days impacted Control 3 days 4 days 5 days 6 days 7 days 14 days 2 1days
No. 1’ 6 6 6 6 8 8 6
Equiv. StifF.rt. Range 1.45-3.80 3.10-4.92
Equiv. stiff. It. Range
1.32-3.79
Ratio Rt./Lt. Range 0.82- 1.20 0.93-I .29 0.89-I .75 I 60-I .86
1.96-3.30
2.40-3.93 I .30-4.07 I .05-l .87
1.73-3.23 1.67-3.28 0.78- 1.62 0.74- 1acl
laL1~66
1.24-2-45
1’15-3.32 0.80-l .88 0.67- 1.36
1~14-2~10 0.86-0.99 0.76-1.12
1.2.5-3.82
Mean (2) S.D.
*Significantly different from the control values at the O-01 confidence level by ‘f’ test.
*Kistler Instrument Company, Clarence, New York. +Sanbom Division, Hewlett-Packard, Waltham, Massachusetts.
I.01 to.11 1.11 -co.19 1.251-0.37 1~76-cO~14’ 1.81+0.54* I *632 0.38* 0.93 2 0.06 0*%?0.18
270
S. R. SIMON,
E. L. RADIN,
increase was statistically significant with ratios averaging 1.76. The stiffness ratios continued significantly higher than control values until 14 days when these measurements had returned to within the normal range. The first obvious mucopolysaccharide loss from the articular cartilage was visible on day 5 in most animals (Fig. 2), although a few showed some surface loss on day 4. The cartilage then continued on to more marked mucopolysaccharide loss and fibrillation by 3 weeks (Fig. 3). As the cartilage changes became more marked (2-3 weeks), the stiffness of its underlying subchondral bone returned to a normal range. The 6-week animals showed more marked joint degeneration with cartilage loss and bony lipping and spurring. Serial synovial sections displayed histological evidence of inthunation on the IO- 14 day with edema, hypertrophy, and cellular proliferation. This persisted throughout the remainder of the experiments. There was no evidence of effusion or fracture. Attempts to see joint line narrowing by X-ray were unsuccessful because of the small size of the joint itself. DISCUSSION
Intermittent loading is the normal, common mode of joint loading. Bassett ( 1968) has shown than when bone formation is caused by electrical flow potentials. they must be intermittent for bone to form. Fifteen hundred cpm is decidedly unphysiological, but seemed appropriate for the type of preliminary study we were carrying out. Mucopolysaccharide loss from the articular cartilage was used as the measure of cartilage degeneration. Although lipping and spurs were noted in the knees of guinea pigs impacted longer than 3 weeks, Silverstein (1958) has reported bone changes of this nature in this species to be associated with joint degeneration. The guinea pig in his normal stance presents a problem. He stands with his knees bent and is thus in an excellent position to absorb
I. L. PAUL
and R. M. ROSE
impact loads by further flexion. Active muscle contractions are an extremely significant factor in energy absorption around joints (Hill, 1960). Secondly, subjected to repeated impactions (vibrations from below), the guinea pig would probably sit down, absorbing most of the energy in his soft underparts which are extremely effective shock absorbers. We therefore had to fix the guinea pigs so that they could not sit down and put their legs in splints so that they could not bend them. The results show that repetitive impact loading will bring about joint degeneration in guinea pigs, with changes in both subchondral bone and in the articular cartilage. The medical experience with osteoarthritis is consistent with these findings. Repetitious impact loading, such as occurs from pneumatic drills, creates degeneration of elbows and shoulders, the joints which absorb the pounding, but not the fingers or wrists which are just vibrated. Vibration, in the absence of repetitious impact loading, is said to cause loss of bony substance and peripheral neuritis, but not joint degeneration (Hunter et al. 1945). The increase in cancellous bone stiffness, followed by a return to normal values, has also been found in osteoarthritic human autopsy material as well (Radin et al. 1970). How does one explain these changes? The simplest explanation of the demonstrated ability of cancellous bone to absorb shock (Physick as quoted by Wistar, 1827; Evans and Ring, 196 1; McElhaney and Byars, 1965; Radin and Paul, 1970) is to ascribe this property to the viscous flow of interstitial blood and marrow fat (Smith and Walmsley, 1959; Frost, 1964; MacPherson and Juhasz, 1965). However, the work of Swanson and Freeman (1966) seems to indicate that there is no viscous component to the dynamic response of femoral cancellous bone, and the remaining plausible mechanism for shock absorption is limited trabecular fracture. A reasonable rate of trabecular fracture should be physiologically tolerable since the metabolic turnover of cancellous bone is much higher than that of
Fig. 2. (a) Normal guinea pig articular cartilage stained with Safranin-0. The dye, which localizes mucopolysaccharide. is visible throughout the cartilage I x 225 ) (b) Cartilage from an impacted knee at 5 days. Loss of Safranin staining especially near the surface is evident (X 225).
Fig. 3. Cartilage undergoing advanced destructive changes after 3 weeks of impaction. Fibrillation, cloning, and loss of mucopolysaccharide are evident (X 180). Wacinp p. 270)
RESPONSE
OF JOINTS
cortical bone (Bauer er al. 1929), the specific surface area of the trabeculae is quite high (Dunhill et al. 1967), and a balance between fracture and healing should be achievable under ordinary circumstances. Although the mechanical properties of individual trabeculae have not (to our knowledge) been examined, it has been established that cortical bone has, at least at some strain rates, the ability to absorb relatively large (compared to many common engineering materials) amount of mechanical energy before failure occurs (Piekarski, 1970; McElhaney et al. 1970). It is interesting to note in this connection that, compared to cortical bone, cancellous bone is grossly over-loaded. Burstein et al. (1970) have analyzed static stress distributions in simplified model condyles and found that the stress in the cancellous bone is about 40 per cent of the stress in the cortical bone, andalso note that the cancellous bone is only one tenth as strong as cortical bone. If in fact the fatigue behavior of cancellous bone is similar to that of the vast majority of engineering materials and to cortical bone (King and Evans, 1967; Swanson et al. 197 1). a peak stress four times as large considered as a fraction of the static compressive or tensile strength would drastically reduce the fatigue life, to physically useless levels, without active physiological intervention. Certainly, the concentrations of stress at irregularities in the trabecular structure (McElhaney et al. 1970) should guarantee that some microfracture under physiological shock-loads occurs continually. Microfractures were apparent in the guinea pig proximal tibias which displayed increased stiffness, but these specimens provided too few trabeculae for statistical analysis. In current similar studies on larger animals (rabbits) which are still in progress, we have found considerable trabecular microfractures which were clearly not artifactual as they did not occur in the control specimens. Although this experimental work is not yet complete, it appears as if the early stiffening is associated with the first stages of healing of these frac-
TO 1MPACT
271
LOADING-II
tures, when abundant callus is present. The return to normal stiffness values seems associated with final remodelling of the fractures. This investigation is continuing and a more detailed report will be forthcoming.
REFERENCES Barland. P.. Janis. R. and Sandson, J. (1966) Immunofluorescent studies of human articular cartilage. Anjz. rheum. Dis. 25, 156-164.
Bassett, C. A. (1968) Significance of piezoelectricity.
Cul.
Tiss. Res. 1,252-272.
Bauer, W., Aub, J. C., and Albright, F. (1929) Studies of calcium and phosphorous metabolism. J. exp. Med. 49,145-161.
Ballet, A. J. (1967) Connective tissue polysaccharide metabolism and the pathogenesis of osteoarthritis. Adc. internal
Med.
13.33-60
Burstein,
A. H., Shuffer, B. W.. and Frankel, V. H. (1970) Elastic analysis of condylarstructures. A.S.M.E. Pub]. No. 70WA/BHF-1. Dunhill, M. S., Anderson, J. A. and Whitehead, R. f 1967) Quantitative histological studies on age changes in bone. J. Path. Bacr. 94,275-29 1. Evans, F. G. and King, A. I. (1961) Regional differences in some physical properties of human spongy bone, in BiomechanicalSludies
of the Musculo-SkeletalSystem.
@iited by F. G. Evans), pp. 49-67. Thomas, Springfield, Illinois. Frost, H. H. (1964) The Laws ofEone Structure. Thomas, Springfield, Illinois. Hill, A. V. (1960) Production and absorption of work by muscles. Science, 131, 867-903. Hunter, D. M., McLaughlin. A. 1. G. and Perry, K. M. A. (1945) Clinical effects of the use of pneumatic tools. Br.J. ind. Med. 2, 10-16. McElhaney, J. H. and Byars, E. F. (1965) Dynamic response of biological materials. A.S.M.E. Pub]. No. 65 WA/HUF-9. McElhaney, J. H., Alem, N., and Roberts, V. (1970) A Porous Block Model for Cancellous Bone. A.S.M.E. Pub]. No. 70 WA/BHF-2. McPherson, A. and Juhusz, L. (1965) Aerodynamics of Bone in Biomechanics
and Related
Engineer&
Topics,
(Edited by R. M. Kenedi). Pergamon Press, London. Piekarshki, R. (1970) Fracture of bone. J. aoDl. Phvs. 41,215-223. Radin, E. L. and Paul, 1. L. (1970) Does cartilage compliance reduce skeletal imuact loads? The relative forceattenuating properties if articular cartilage. synovial fluid, periarticular soft-tissues and bone. Arthritis Rheum.
13.139-144.
Radin, E. L. and Paul, 1. L. (I 97 1) The response of joints to impact loading. I. In vitro wear. Arthritis Rheum. 14,52
I-530.
Radin, E. L., Paul, I. L. and Lowy, M. (1970) A comparison of the dynamic force transmitting properties of subchondral bone and articular cartilage. J. Bone Jr. Surg. 52A, 444-456.
272
S. R. SIMON,
E. IL. RADIN,
Radin, E. L., Paul, I. L. and Tolkoff, M. J. (1970) Sub-
chondral bone chaugcs in patients with early degenerativcjoint disease. Arthritis Rheum. l3,400-405. Rosenberg, L. (1971) Chemical basis for the histological use of safmnin-0 in the study of articular cattibg~. J. Bone J. Surg. 53A. 69-82.
Silverstein. E. and Sokoloff. L. (1958) Natural history of degenerative joint disease in small animals 5. Osteo-
I. L. PAUL and R. M. ROSE arthritis in guinea pigs. Arthritis Rheum. 1, 82-86. Smith. J. W. and Wohnskv. R. (1959) Factors a&ctina the &asticity of bone. J. &at. &, SO&523. Swanson, S. A. and Freeman, M. A. R. (1966) Is bono hydraulically strcngthcnui? &-fed.biol. Engng 4,433438. Wistar. C. A. (1827) System of Anatomy. Part 1. Osteology, 4th cdn. Lea and Carey, Philadelphia.
192.
Vol. S. pp. 267-272.
Pergamm
Press.
Printed in Great Britain
THE IN VII/O Department
SHELDON R. SIMON: and ERIC L. RADINS of Orthopedic Surgery, Harvard Medical School, Children’s Hospital Center, Boston, Massachusetts 021 IS, U.S.A.
Medical
and
Massachusetts
IGOR L. PAULQ and ROBERT M. ROSE11 Institute of Technology, Cambridge. Massachusetts 02 139. U.S.A.
Abstract-The knee joints of live guinea pigs, subjected to repeated longitudinal impaction. developed obvious cartilage degeneration over a 3 week period. In vitro tests had previously shown that articular cartilage is particularly susceptible to injury from impact loading and that subchondral bone acts as a cushion to protect the overlying cartilage from damage during such loading. Associated with. and slightly preceding the earliest cartilage changes, as judged histochemicaliy, was a stiffening of the underlying subchondraf bone. The bone stiffness measurements returned to within the normal range as the cartilage degeneration progressed. INTRODUCTION
joints basically function as bearings, allowing vertebrates ease of motion with considerable flexibility and stability. Considering the stresses under which joints function. they are remarkably wear resistant. Although articular cartilage is extremely resistant to cyclic shear stress even under high loads, this tissue has been shown to be very susceptible to repetitive longitudinal loading (Radin and Paul, 1971). Subchondral bone has been experimentalLy shown to function effectively as a shock absorber (Physick as quoted by Wistar, 1827: Evans and Ring, 1961: McElhaney and Byars, 1956; Radin and Paul, 1970). It would thus be in a position to help protect its overlying articular cartilage from longitudinal impact loads. If the subchondral ‘cushion’ does fail in uivo, one might expect articular cartilage degeneration to follow close behind. This paper will report SYNOWAL
on the subchondral bone and articular cartilage changes resulting from the repetitive loading of the joints of live animals. METHODS
Young adult (12- 14 month old) male English short-haired guinea pigs were chosen as the experimental animal. An impaction table was made by mounting a piece of plywood on a metal plate which was cyclically elevated and depressed 0.4 cm by a motor-driven eccentric shaft. The guinea pigs were suspended in a rack above the impaction table in such a way that they could not sit down. The animals were held in the rack so that their fully extended hind legs almost touched the vibrating table. Each guinea pig was then fitted with long leg methacrylate splints which held the knees in maximum extension and the ankles in neutral. The right splint had an extension which was attached to the vibrating table and
*Received 6 May I97 1. torthopedic Research Fellow. *Assistant Professor. $Associate Professor of Mechanical Engineering. l/Associate Professor of Metallurgy and Materials Science. 267
268
S. R. SIMON,
E. L. RADIN,
I. L. PAUL
and R M. ROSE
conducted the impact load to the animal’s Groups of animals were sacrificed at daily heel {Fig. I). This was the experimental side. intervals from 3-7 days then weekly to 3 The let? leg was held in a splint which kept the weeks. All groups contained at least 5 animals. knee in maximal extension but the foot com- Upon sacrifice the animals’ knees were displetely off the vibrating table. The left knee of articulated, their distal femurs and synovial each animal therefore acted as the control. tissue were histologically evaluated, and stiffThe splints were applied just before the ness measurements were carried out on the impaction period and removed immediately proximal tibias. The distal femurs were immediately fixed in upon its completion. Once accustomed to the splints the animals were not bothered by the formalin, then decalcified in 4% fotiic acid, impacting procedure. They were allowed to stained with Safranin-0 and examined microrun free in their cages the remainder of the scopically. This stain geographically and time. They were initially hesitant to walk for a quantitatively demonstrates losses of mucofew hours after impaction. As the experiment polysaccharide from articular cartilage (Rosenprogressed, they protected their right hind berg, 1970). Such a loss, preferentially at the legs more and more. Any animal who devel- cartilage surface, is felt to be the first recognizoped significant pressure sores, infections, or able cartilaginous change in degenerative systemic illness was excluded from the study, joint disease (Barland et al. 1966; Bollet, All animals were examined twice a week by a 1967). The synovium was studied in 6 P veterinarian to insure their continued good sections, mounted in paraffin, and stained with hematoxylin and eosin. health. The legs below the knee were frozen to be The table was vibrated at 1500 c/m. Strain gauges affixed to representative splints at thawed just before mechanical testing. At that various positions on the table showed the time their proximal tibias were freed of all impaction force to approximate the weight of soft tissue. The tibial shaft was cut across the guinea pig (1- 1.23 kg). These strain gauge about O-6cm below the knee and the right and measurements were repeated at regular inter- left specimens mounted side by side on vals throughout the experiment and demon- adjoining plates in a cryostat, articular side strated no significant variance (& Ci-1 kg) _ up. The diapbyseal bases of these specimens The animals were run daily for I5 min. were adjusted so that both pieces had exactly
SIDE
VIEW
REAR
VIEW
Fig. I. Guinea pig in the rack wearing bilateral long-leg splints. The splint on the right has a plug which extends from the heel of the animal to the impaction table. This transmits the impulses from the table to the guinea pig’s right lower extremity. The left leg is held in a splint which makes no contact with the table.
RESPONSE
OF JOINTS
TO IMPACT
the same orientation in the cryostat. The articular cartilage was then removed a few microns at a time. As soon as all articular cartilage had been removed from both specimens, they were mounted on the same plate of the cryostat, articular side down. and the remnants of diaphysis and epiphyseal plate were removed from both specimens at the same time. This gave us specimens equal in thickness from each animal as measured from the subchondral plate (O-07-0.13 cm). These thin discs of subchondral bone were then subjected to an impact load (1.08 kg dropped 0.16 cm) to determine their response. The impacting technique as well as the force and deflection measurement methods have been previously described (Radin et al. 1970). The plugs were subjected to known impact loads in a reproducible manner. With this equipment the maximum initial strain rates applied were approximately 670 per centlsec for cartilage plugs and about 1 IO per cent/set for bone plugs. The force was registered on a force transducer:* the defiection, by a linear variable differential transformer:: and both values were displayed on an oscilloscope as a function of time and photographed. An ‘equivalent stiffness’ value was defined as the ratio of the measured peak force over the measured peak deflection under identical impact condirions. This value was felt to be a
LOADING-II
769
more meaningful measurement of the significant mechanical properties of the specimens than the relative energy absorbing previously used, since we are interested in the change of stiffness which determines the peak force during impact loading. Although the paired bone specimens from each animal were identical in size and shape, there was some unavoidable variation from animal to animal. To obtain a meaningful relative value for each animal, a ‘stiffness ratio’ was calculated by dividing the stiffness of the right (experimental) plug over that of the left (control). A few animals were run for 6 weeks. Because of the development of pressure sores, this group was too small to be confidently gauged histologically or mechanically. but was examined grossly. RESULTS
The ‘stiffness ratios’ for each of the groups were averaged. These values and their statistical distribution are presented in Table 1. Animals kept in their cages and not subjected to impaction maintained a l-01 (2 O-11) ‘stiffness ratio’ throughout the experiment. The first alterations in bone stiffness occurred at 3 days. The bone became less able to attenuate peak force and less deformable, i.e. stiffer, on the experimental side. However, it was not until the 5th day that the bone stiffness
Table I. Stiffness ratios
Days impacted Control 3 days 4 days 5 days 6 days 7 days 14 days 2 1days
No. 1’ 6 6 6 6 8 8 6
Equiv. StifF.rt. Range 1.45-3.80 3.10-4.92
Equiv. stiff. It. Range
1.32-3.79
Ratio Rt./Lt. Range 0.82- 1.20 0.93-I .29 0.89-I .75 I 60-I .86
1.96-3.30
2.40-3.93 I .30-4.07 I .05-l .87
1.73-3.23 1.67-3.28 0.78- 1.62 0.74- 1acl
laL1~66
1.24-2-45
1’15-3.32 0.80-l .88 0.67- 1.36
1~14-2~10 0.86-0.99 0.76-1.12
1.2.5-3.82
Mean (2) S.D.
*Significantly different from the control values at the O-01 confidence level by ‘f’ test.
*Kistler Instrument Company, Clarence, New York. +Sanbom Division, Hewlett-Packard, Waltham, Massachusetts.
I.01 to.11 1.11 -co.19 1.251-0.37 1~76-cO~14’ 1.81+0.54* I *632 0.38* 0.93 2 0.06 0*%?0.18
270
S. R. SIMON,
E. L. RADIN,
increase was statistically significant with ratios averaging 1.76. The stiffness ratios continued significantly higher than control values until 14 days when these measurements had returned to within the normal range. The first obvious mucopolysaccharide loss from the articular cartilage was visible on day 5 in most animals (Fig. 2), although a few showed some surface loss on day 4. The cartilage then continued on to more marked mucopolysaccharide loss and fibrillation by 3 weeks (Fig. 3). As the cartilage changes became more marked (2-3 weeks), the stiffness of its underlying subchondral bone returned to a normal range. The 6-week animals showed more marked joint degeneration with cartilage loss and bony lipping and spurring. Serial synovial sections displayed histological evidence of inthunation on the IO- 14 day with edema, hypertrophy, and cellular proliferation. This persisted throughout the remainder of the experiments. There was no evidence of effusion or fracture. Attempts to see joint line narrowing by X-ray were unsuccessful because of the small size of the joint itself. DISCUSSION
Intermittent loading is the normal, common mode of joint loading. Bassett ( 1968) has shown than when bone formation is caused by electrical flow potentials. they must be intermittent for bone to form. Fifteen hundred cpm is decidedly unphysiological, but seemed appropriate for the type of preliminary study we were carrying out. Mucopolysaccharide loss from the articular cartilage was used as the measure of cartilage degeneration. Although lipping and spurs were noted in the knees of guinea pigs impacted longer than 3 weeks, Silverstein (1958) has reported bone changes of this nature in this species to be associated with joint degeneration. The guinea pig in his normal stance presents a problem. He stands with his knees bent and is thus in an excellent position to absorb
I. L. PAUL
and R. M. ROSE
impact loads by further flexion. Active muscle contractions are an extremely significant factor in energy absorption around joints (Hill, 1960). Secondly, subjected to repeated impactions (vibrations from below), the guinea pig would probably sit down, absorbing most of the energy in his soft underparts which are extremely effective shock absorbers. We therefore had to fix the guinea pigs so that they could not sit down and put their legs in splints so that they could not bend them. The results show that repetitive impact loading will bring about joint degeneration in guinea pigs, with changes in both subchondral bone and in the articular cartilage. The medical experience with osteoarthritis is consistent with these findings. Repetitious impact loading, such as occurs from pneumatic drills, creates degeneration of elbows and shoulders, the joints which absorb the pounding, but not the fingers or wrists which are just vibrated. Vibration, in the absence of repetitious impact loading, is said to cause loss of bony substance and peripheral neuritis, but not joint degeneration (Hunter et al. 1945). The increase in cancellous bone stiffness, followed by a return to normal values, has also been found in osteoarthritic human autopsy material as well (Radin et al. 1970). How does one explain these changes? The simplest explanation of the demonstrated ability of cancellous bone to absorb shock (Physick as quoted by Wistar, 1827; Evans and Ring, 196 1; McElhaney and Byars, 1965; Radin and Paul, 1970) is to ascribe this property to the viscous flow of interstitial blood and marrow fat (Smith and Walmsley, 1959; Frost, 1964; MacPherson and Juhasz, 1965). However, the work of Swanson and Freeman (1966) seems to indicate that there is no viscous component to the dynamic response of femoral cancellous bone, and the remaining plausible mechanism for shock absorption is limited trabecular fracture. A reasonable rate of trabecular fracture should be physiologically tolerable since the metabolic turnover of cancellous bone is much higher than that of
Fig. 2. (a) Normal guinea pig articular cartilage stained with Safranin-0. The dye, which localizes mucopolysaccharide. is visible throughout the cartilage I x 225 ) (b) Cartilage from an impacted knee at 5 days. Loss of Safranin staining especially near the surface is evident (X 225).
Fig. 3. Cartilage undergoing advanced destructive changes after 3 weeks of impaction. Fibrillation, cloning, and loss of mucopolysaccharide are evident (X 180). Wacinp p. 270)
RESPONSE
OF JOINTS
cortical bone (Bauer er al. 1929), the specific surface area of the trabeculae is quite high (Dunhill et al. 1967), and a balance between fracture and healing should be achievable under ordinary circumstances. Although the mechanical properties of individual trabeculae have not (to our knowledge) been examined, it has been established that cortical bone has, at least at some strain rates, the ability to absorb relatively large (compared to many common engineering materials) amount of mechanical energy before failure occurs (Piekarski, 1970; McElhaney et al. 1970). It is interesting to note in this connection that, compared to cortical bone, cancellous bone is grossly over-loaded. Burstein et al. (1970) have analyzed static stress distributions in simplified model condyles and found that the stress in the cancellous bone is about 40 per cent of the stress in the cortical bone, andalso note that the cancellous bone is only one tenth as strong as cortical bone. If in fact the fatigue behavior of cancellous bone is similar to that of the vast majority of engineering materials and to cortical bone (King and Evans, 1967; Swanson et al. 197 1). a peak stress four times as large considered as a fraction of the static compressive or tensile strength would drastically reduce the fatigue life, to physically useless levels, without active physiological intervention. Certainly, the concentrations of stress at irregularities in the trabecular structure (McElhaney et al. 1970) should guarantee that some microfracture under physiological shock-loads occurs continually. Microfractures were apparent in the guinea pig proximal tibias which displayed increased stiffness, but these specimens provided too few trabeculae for statistical analysis. In current similar studies on larger animals (rabbits) which are still in progress, we have found considerable trabecular microfractures which were clearly not artifactual as they did not occur in the control specimens. Although this experimental work is not yet complete, it appears as if the early stiffening is associated with the first stages of healing of these frac-
TO 1MPACT
271
LOADING-II
tures, when abundant callus is present. The return to normal stiffness values seems associated with final remodelling of the fractures. This investigation is continuing and a more detailed report will be forthcoming.
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