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Does cartilage compliance reduce skeletal impact loads. the relative force-attenuating properties of articular cartilage synovial fluid periarticular soft tissues and bone

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Does Cartilage Compliance Reduce Skeletal Impact Loads?
The Relative Force-Attenuating Properties of Articular Cartilage,
Synovial Fluid, Periarticular Soft Tissues and Bone
Eric L. Radin and lgor L. Paul
Joint wear is related t o the pressure exerted at the articular cartilage interface.
The largest loads an animal joint experiences in life will be brief and will result
from impact. Compliance in the system will decrease the peak value of such
impulsive loadings a t the expense, probably unimportant, of increasing their
duration. The ability of synovial fluid, supporting bone and periarticular soft
tissues to provide this compliance and attenuate peak forces might spare the
articular cartilage and prevent wear. Measurements were made of the relative
attenuation of longitudinally applied, external impulsive force by these major
joint elements of adult bovine interphalangeal joints. The effect of the various
elements, independently, upon the over-all compliance of the joint was measured
i n nonimpulsive experiments and found to correlate quite well with their ability
to reduce the peak load in the impulsive experiments. Only the periarticular
soft tissues (capsule, ligaments and synovial tissue) and bone have significant
force-attenuating properties. Articular cartilage and synovial fluid have little
effect. These results support the contention that the integrity of bone could well
be important in prolonging joint life.
From the Orthopedic Research Laboratories,
Harvard Medical School, Massachusetts General
Hospital, Boston, Mass.
ERIC L. RADIN,
MD: Instructor in Orthopedic
Surgery, Harvard Medical School, Massachusetts
General Hospital, Boston, Mass: Research Fellow in
Orthopedic Surgery, Massachusetts General Hospital, Boston, Mass; Special Post-Doctoral Fellow of
the National Institute of Arthritis and Metabolic
Diseases. ICORL. PAUL,DSc: Associate Professor of
Mechanical Engineering, Massachusetts Institute of
Technology, Cambridge, Mass.
Reprint requests should be addressed to Dr.
Radin, Orthopedic Research Laboratories, Massachusetts General Hospital, Boston, Mass 021 14.
Submitted for publication July 7, 1969; accepted,
Oct 11. 1969.
objectively substantiated;l however, aging,
in and of itself, has been precluded as a
causative factor.293 Although joint incongruities obviously lead to arthritic changes,
Murray’s4 contention that gross architectural irregularities are always present in
osteoarthritis implies that a significant
number of us develop poorly formed joints.
It is much more reasonable to postulate
that joints are basically well designed, but
as any bearings, are subject to wear. The
continuing ability of a joint to function
under load would, then, be inversely related to its rate of wear. The ability of
distal joints to attenuate peak compressive
stresses transmitted to the cartilage inter-
Arthritis and Rheumatism, Vol. 13, No. 2 (March-April 1970)
139
The clinical impression that osteoarthritis is a disease of older people has been
RADIN P PAUL
cartilage after fresh-freezing has been established.‘*Ja
Any hoof showing arthritic changes was discarded.
The proximal interphalangeal joints were dissected
out with capsule and ligaments intact. The joints
were mounted in holders to maintain their natural
alignment (Fig 1 ) . Their bony ends, cut flat, protruded above the holders. The proximal, interphalangeal cartilaginous surfaces, enclosed within
the periarticular soft tissues, articulated.
These mounted joints were then subjected to
rapidly applied forces in a specially designed impacting sleeve (Fig 2) which permitted reproducible
dropping of weights on the joints to achieve suddenly applied pressures between 250 and 1200 psi.
The force transmitted through the joints was registered by a force transducer,* displayed on an
oscilloscope and photographed. Great care was
taken to prevent false attenuation from rotatory
components and from friction of the holders against
the aligning sleeve. The joints were then subjected
to slow (0.02 and 0.04 inches/min) , evenly applied
forces (to 300 pounds) in an Instron Tensile Testing Machinet modified for compression (Fig 3).
The force required to produce a standard compressive strain, 0.45% of the total length of the
preparation, gave an inverse measure of the compliance of the preparation.
While still mounted in its holder, each joint was
completely retested under 3 further conditions:
(I) capsule, synovium, and ligaments cut, but
synovial fluid left undisturbed within the joint;
(2) synovial fluid wiped, washed away and replaced
with isotonic buffer (pH 7.2) : (9) articular cartilage totally removed surgically, leaving denuded
subchondral bone which was lubricated with fresh
buffer.
The joints were measured before testing, and
their weight-bearing areas measured by a carbon
black transfer technic” under a static load of 300
pounds.
These experiments measured relative rather than
absolute force transmissibility of specimens. What
has been reported is peak output force values for
identical input conditions. The transmitted peak
force was used as an indicator of the dynamic,
force-attenuating qualities of the joint. Due to the
viscoelastic nature of cartilage and bone, their
peak deflections do not exactly coincide with their
peak forces. To date, simultaneous measurements
MATERIALS AND METHODS
of transmitted force and deformation have been
carried out on bone and cartilage plugs and are
The hooves Of
to
freshly currently in progress on half joints. It is further
slaughtered cows were frozen immediately for storage and thawed just before testing. The maintefKistler Instrument co., Clarence, ~ y .
nance of the mechanical properties of bone and
tInstron Corp., Canton, Mass.
face in impulsive loading might, to a great
extent, determine how well the proximal
joints can function before they begin to
wear.
Of course, static loading also stresses the
cartilage, and there is no way to mitigate
this effect. A static load, or a load that
varies slowly, stresses various joints to a
degree determined by the arrangement of
the skeletal system and the loads, themselves, be they external or the result of
gravity acting on the body’s own mass. Impulsive loads can be higher, for instancethe load resultant in stepping straightlegged off an unperceived step. Any compliance (“springiness”) in the system reduces the peak load by spreading the impulse over a longer time. If it is these peak
loads which damage cartilage, then skeletal
compliance may be an important factor in
preventing osteoarthritis.
Since the resilience of articular cartilage
has been recognized,5 it has been assumed
that most of the compliance in the skeletal
system is provided by the cartilage. However, the later establishment of the viscoelasticity of synovial fluids has led to the
supposition that it, too, acts as a “shock
absorber.”7-9 Recent work with bone and
cartilage plugsll has suggested that subchondral bone might well play an even
more significant role in force attenuation
than does cartilage or synovia. This paper
presents the results of force transmission
studies on whole-joint preparations made to
determine the relative capabilities of articular cartilage, synovial fluid, periarticular
soft tissues, and bone, to attenuate peak
stress produced by impulsive loading.
’-
140
Arthritis and Rheumatism, Vol. 13, No. 2 (March-April 1970)
CARTllAPE COMPLIANCE
I
/
c
-----Knurl
Proximal phalanx
-
,/
Aligning
serous
.-capsule a
Ligrnents
Mounting
holders
--Aligning
sleeve
-----Weight
Middle phalanx
Fig 1. Whole proximal interphalangeal joint mounted
in test holders and held by screws. Bone protrudes beyond
the ends of the holders.
recognized that the stress-strain relations of biological materials are time-dependent. A more
quantitative description of the mechanical properties of the various joint components will be presented in a future publication.
-----Joint
RESULTS
Although the absolute values of the measured parameters varied considerably among
the different joints tested, the relative effects of the joint components were consistent for each joint. The average weightbearing area in the proximal interphalangeal joints was approximately one-half
square inch.
Peak forces experienced by joints under
impulsive loading in various experimental
conditions are shown in Table 1, using
1 0 0 ~ oas the value initially obtained with
the whole joint. Cutting the periarticular
soft tissues significantly increased the peak
force experienced by joints when subjected
to identical impact. The presence or absence of synovial fluid had no significant
effect. Surgical removal of the articular cartilage either made little difference or decreased the maximum transmitted force.
This decrease in force was felt to be artifactual and will be discussed later.
Arthritis and Rheumatism, Vol. 13, No. 2 (March-April 1970)
Force
transducer-----=
-
~
Fig 2 The impacting sleeve allows reproducible dropping of weight on joints.
Table 2 lists the results of the slow compression (Instron) tests. This data is reported as a percentage increase in the
amount of force requised to achieve a given
amount of strain (tleflection/initial length)
using 100% as the vaiue initially obtained
with the whole joint. At slow rates of compression, the compliahce introduced by the
soft tissue was clearly apparent, although
less than would be interred from the impact
experiments. The rehoval of articular cartilage made little difference. Experimental
errors, which are listed with the data in the
Tables, were determined by repeating each
measurement 3 times.
141
W I N 6 PAUL
sistent behavior, more marked than would
be expected from the compliance measureT h e maximum intra-articular pressure ments, is probably due to irregularities in
experienced by a joint subjected to impul- the denuded joint surface. T h e subchonsive loading depends upon the attenuating dral bone-cartilage interface is irregular.15
properties of the joint components. T h e These irregularities, normally unimportant
major contribution to peak force attenua- from the point of view of joint fit because
tion in the experiment comes from capsule they are covered by a relatively flexible
and bone rather than cartilage and syn- cartilaginous surface, become obvious when
ovial fluid. I n fact, surgical removal of the cartilage is removed. Irregularities
cartilage appears to result i n little deterio- would act to increase the compliance of the
ration of force attenuation and in actual joints and thus, attenuate any suddenly
improvement in some cases. This incon- applied forces. At slow rates of compres-
DISCUSSION
To recorder
Fig 3. The lnstron apparatus modified for compression allows slow, controlled reproducible joint
compression.
142
Arthritis and Rheumatism, Vol. 13,
No. 2 (March-April 1970)
CARTILAGE COMPLIANCE
Table 1. Peak Force Transmission Through
lnterphalangeal Joints on Impact of
3.25 Pound Weight*
Experiment
No.
1
Peak Force (X)
___
Distance
weight Capsule Capsule
dropped cut-S. F. cut-S. F. Cartilage
(in.)
present absent removed
-
w
147
159
123
M
126
169
M
166
152
%i 147
M
2
3
4
w
w
w
* Experimental
147
159
123
124
170
171
152
145
141
155
106
118
138
143
150
143
error 2%
Table 2. Slow Compressive Force Necessary
to Produce Strain of 0.45% in Joints*
Compressive Force (96)
CompresExperision
Capsule Capsule
rnent
speed cut& F. cut-S. F. Cartilage
No.
(in./rnin) present absent removed
5
6
7
8
.02
.04
.02
.a4 .
.02
.04
.02
.04
102
108
105
108
102
101
103
106
103
107
106
105
107
105
105
105
116
108
107
104
108
101
108
104
* Experimental error 3%
sion, these irregularities tend to become
flattened, and for this reason, paradoxical
behavior is less obvious in the Instron tests.
Trapped air was not felt to contribute
significantly to force attenuation because of
the presence of a lubricant between the
articulating surfaces.
T h e surprising lack of significant force
attenuation by both articular cartilage and
synovial fluid, compared to bone, supports
Mhritir and Rheumatism, Vol. 13, No. 2 (March-April 1970)
earlier compression test results on cartilage
plugs, coated and uncoated with synovial
fluid, and those on subchondral bone.1l
These results suggested that cancellous bone
with its associated marrow, although approximately 10 times stiffer than articular
cartilage per unit thickness, is considerably
thicker and is capable of contributing as
much or more to dynamic force attenuation. Cortical bone, about 10 times stiffer
than cancellous bone, also exists in large
amounts and is likewise capable of considerable force attenuation. Were the entire bone shafts still intact, the compliance
of the bone should be higher still compared
to that of the cartilage. The attenuation of
force requires deflection; to allow deflection to reduce peak force a sufficiently thick
layer must exist. T o use an analogy, sponge
rubber is worthless as a shock absorber if
it is only a fraction of an inch thick.
Cartilage is viscoelastic,l”ls which means
its compression under load is time-dependent. Rapidly applied loads compress cartilage less than slowly applied loads of
the same magnitude. Thus, at very low
load rates, cartilage is more compliant, but
at such rates loading is not impulsive and
the force-attenuating effect will not occur.
T h e same relationship between deflection
and loading rate holds true for the thin
film of synovial fluid of the joint surface.
At the high loading rates which occur in
impulsive loading, synovial fluid adds no
demonstrable force-attenuating capacity to
whole joints or cartilage p1ugs;”J at low
rates it introduces a little compliance.
The important role played by periarticular soft tissues in force attenuation is probably due to their own elastic nature, resulting from tissue water content. Experiments reported here do not preclude the
possibility that the force-attenuating properties of soft tissues may be related to the
presence of intra-articular fluid or articular
143
RADlN 81 PAUL
effect of aging on protein synthesis in articular
cartilage of rabbits. Lab Invest 14:658, 1965.
4. MURRAY,
R. 0. The etiology of primary
osteoarthritis of the hip. Brit J Radio1 38:810,
1965.
5. RAUBER,
A. 1876. Quoted by Edwards, J.
Physical characteristics of articular cartilage.
Symposium on Lubrication and Wear, Institution of Mechanical Engineering, London, 1967,
p 24.
6. OCSTON,
A. G., STANIER,
J. E., TOMS,
B. A.,
and STRAWBRIDGE,
D. J. Elastic properties of ox
synovial fluid. Nature (London) 165:571, 1950.
A. G., and STANIER,
J. E. On the
7. OGSTON,
state of hyaluronic acid in synovial fluid. Biochem J 46.964, 1950.
8. WHITE,R. K. The rheology of synovial
fluid. J Bone Joint Surg 45A:1084, 1963.
9. MET~AM,A. R. Comments in Symposium
on Biomechanics, Institution of Mechanical
Engineering, London, 1959, p 44.
10. RADIN,E. L., and PAUL,I. L. Failure of
synovial fluid to cushion. Nature (London)
222:999, 1969.
11. RADIN,E. L., PAUL,I. L., and LOWY,
M. A. Comparison of the peak force transmitting
properties of subchondral bone and articular
cartilage. J Bone Jqint Surg In press.
12. ELMORE,
S. M., SOKOLOFF,L., NORRIS,
G..
and CARMELI,
P. Nature of “Imperfect” elaslying bone.
ticity of articular cartilage. J Appl Physiol 18:
393, 1963.
13. SEDLIN,F. O., and HIRSCH,C. Factors
ACKNOWLEDGMENTS
affecting the determination of the physical prop
We thank Drs. Charles McCutchen and Leon erties of femoral cortical bone. Acta Orfhop
Sokoloff who reviewed the manuscript and Scand 37:29, 1960.
offered helpful suggestions, and Lee Siler, who
14. SAHA,A. K. Theory of shoulder mechaprovided valuable technical assistance.
nism: Descriptive and applied. Thomas, Springfield, Ill, 1961.
15. JOHNSON,
L. C. Kinetics of Osteoarthritis.
REFERENCES
Lab Invest 8:1223, 1956.
16. HIRSCH,C. A contribution to the patho1. LAWRENCE,
J. S., BREMNER,
J. S., and BIER,
F. Osteoarthrosis: Prevalence in the population genesis of chondrqmalacia of athe patella. Acta
and relationship between symptoms and x-ray Chir S p n d 90 (Suppl. 83):9, 1944.
17. MCCUTCHEN,
C. W. The frictional prop
changes. Ann Rheum Dis 25:1, 1966.
2. SOKOLOFF,
L. Elastici.ty of aging cartilage. erties of animal joints. Wear 5:1, 1962.
18. SOKOLOFF,
L. Elasticity of articular cartiFed Proc 25:1089, 1966.
3. MANKIN.H. J., and BARON,P. A. The lage. Science 242:1055. 1963.
cartilage. Further experiments to clarify
this point are in progress.
T h e major functions of joints are “motion” and “support.” Both functions are
related to the amount of weight borne by
the joint; “motion,” because the frictional
forces generated are directly proportional
to load; “support,” for obvious reasons.
The ability to withstand loading (compressive force) must, to a great extent,
determine the life of a joint. T h e effect of
loading o n the joint is obviously a function
of many factors: amplitude, frequency, duration, and rate of application. Although
the total picture has yet to be drawn, the
results presented here do suggest that the
integrity of bone could be of great importance in prolonging joint life; cartilage
and synovial fluid, critical i n reducing the
frictional forces during motion, have relatively little effect in attenuating peak impulsive loads borne by joints. If bone became unable to attenuate sudden loads (ie,
by being much stiffer), articular cartilage
would obviously suffer. Therefore, cartilage
degeneration could be caused by alterations
i n the mechanical properties of the under-
144
Arthritis and Rheumatism, Vol. 13, No. 2 (March-April 1970)
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