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Response of Joints to Impact Loading. I. In Vitro Wear

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Response of Joints to Impact Loading
1. In Vitro Wear
Eric L. Radin and lgor L. Paul
Bovine joints were oscillated under the maximum possible static load in a device
which measured their coefficients of fraction while the joints were running.
Joint wear was evaluated by gross and histologic inspection. Joints oscillating
under loads, just below the structural capability of the joints, did not show
significant wear even after long periods of time. When periodic impact loading
was added to this regimen, cartilage wear became rapid and was easily discernible. The implications of these findings to the wearing away of articular
cartilage are discussed.
T h e etiology of idiopathic osteoarthritis
is obscure. Joint degeneration follows trauma, congenital deformity, infection and
other causes of joint incongruity or frank
cartilage destruction. It has been suggested
that subtle anatomic deformities or mild
rheuma’toid changes always precede joi,nt
destruction in the so-called idiopathic cases
(1). but the experience of most rheumatologists is that i n the majority of patients wi,th
this extremely common condhion, there is
no discernible cause. Except in a few clear-
ly syndromal forms, chemical, enzymatic
and hereditary causes have been ruled out,
although the later stages of the disease are
marked by significant metabolic changes in
the articular cartilage and synovium (2).
T h e concept of degenerative joint disease as simply a “wear and tear” phenomenon has never been successfully substantiated. I n spite of the obvious industrial and
activity-related localized arthritic changes
reported (3-5) the absence of joint degeneration in many persons who have
been “active and done heavv work’ all
From the Orthopedic Research Laboratories,
their lives seems to diminish the possibility
Massachusetts General Hospital, Harvard Medical
School, Boston, Mass; and the Department of Me- of mechanical factors being a cause (6).
chanical Engineering, Massachusetts Institute Of
Further, in spite of ,the fact that joint
Technology, Cambridge, Mass.
Supported in part by the Orthopedic Research degeneration is clearly age-related, Sokoloff
and Education Foundation.
(2)
. , has accumulated considerable evidence
ERICL. RADIN,MD: Assistant Professor of Ortho- to show that degenerative arthritis is ,not
pedic Surgery, Harvard Medical School, Boston,
a process Of agingMass; Lecturer, Department of Mechanical En@neering, Massachusetts Institute of Technology,
Bollet (7) concluded that increased stress
Cambridge, Mass; Gebbie Foundation Fellow. ICOR is probably responsible for initiating the
L. PAUL,ScD: Associate Professor of Mechanical
Engineering, Massachusetts Institute of Technology,
Cambridge, Mass.
Reprint requests should be addressed to Dr.
Radin. 300 Longwood Ave, Boston, Mass 02115.
Submitted for publication Sept 22, 1970; accepted
Jan 13, 1971.
356
enzymatic processes that
destroy
the cartilage. This conclusion led us to
begin to study how joints handle stress, and
how much of a n hcrease in stress is necessary before the joint actually begins to
Arthritis and Rheumatism, Vol. 14, No. 3 (May-June 1971)
JOINT RESPONSE TO IMPACT LOADING
wear. We will report here the results of
experiments which attempted to wear-out
bovine metacarpal-phalangeal joints by oscillating them under high, constant load,
and by subjecting them to repeated impact
loads superimposed on a constant load.
These experiments establish impact loading as a mechanism for joint wear, and
clearly demonstrate that rubbing back and
forth, even under high-load, would not
seem to account for articular cartilage destruction. T h e second paper in this series
will extend these experiments to the joints
of living animals. Subsequent papers will
establish the sequence of the bone and
cartilage changes, investigate the character
of the bone changes, and relate the enzymatic and metabolic alterations in the articular cartilage and synovium with the
changes in the mechanical characteristics of
the bone. From these data, it should be possible to draw conclusions about the relative
interaction of mechanical and chemical
changes in joint degeneration after repeated impact loading. This, taken together with studies of human osteoarthri'tic
joints (8), should establish an etiologic pathway for this disease.
METHODS AND MATERIALS
T h e hooves of adult cows, 3-4 years old, were
frozen immediately after slaughter, and thawed just
before testing. Their metacarpal-phalangeal joints
were dissected out, cut sagittally after it was
established by gross examination that they contained no arthritic changes, and then mounted in
an arthrotripsometer (9) which we had modified to
allow us to apply loads u p to 2000 pounds to the
joints (10). The arthrotripsometer is a device
which allows the measurement of instantaneous
coefficients of friction in joints which are continually oscillating in a lubricant bath under known loads
(Fig 1 ) .
Synovial fluid was obtained from the hocks of the
same animals and was processed as previously
reported (11). The relative viscosities of the synovi-
Fig 1M. Arthrotripsometer modified to apply both static and dynamic loads. Equipment can be made to
oscillate, to oscillate with midcycle stops, or to oscillate with dynamic force added during midcycle stops.
Arthritis and Rheumatism, Vol. 14, No. 3 (May-June 1971)
357
RADlN 81 PAUL
fluids ranged from 2.58 to 6.88. Veronate buffer,
pH 7.2, 0.155 M, was used as the standard lubricant. T h e joints were oscillated at 40 cycles/min at
ri
29°C.
Identical t a t s were run under varying static !oads
with the same joint, comparing synovial fluid and
buffer as lubricants. T h e load was increased by
200-pund increments, until the supporting bony
elements of the joint broke. T h e maximum load
under which bovine metatarsal-phalangeal joints
can be oscillated was found to be 1200-1500
pounds. Five joints were run at a value just under
this range-I000 pounds-for up to 500 hours, in
appropriate fresh lubricant which was slowly circulated through the lubricant bath. T h e joints were
grossly examined for wear each day. The friction
values of the joints were measured every 24 hours.
At the end of the test, wedges of the joints were
taken, fixed in Bouin's solution, decalcified in 5 %
formic acid, embedded in paraffin, sectioned perpendicular to the articular surface, stained with
hematoxylin and eosin, and examined for microscopic evidence of cartilaginous wear.
The arthrotripsometer was fitted with an electromagnetic clutch actuated by a cam-operated microswitch installed in the drive train (12). This was
set to interrupt the joints' oscillation in midposition
for 2 seconds, and then to resume the cycle. Three
joints were run under these conditions, 1000 pounds
of static load for up to 200 hours. Their wear was
monitored as detailed above.
The arthrotripsometer was further modified by
adding a pneumatic loading system which applied a
sudden additional load. A 500-pound static load was
applied. The oscillatory cycle was interrupted i n its
midpoint for 2 seconds. During this pause, with the
joint in the upright position, a dynamic load of 500
pounds was rapidly applied and quickly released
(Fig 1). T h e oscillation was then resumed until the
joint returned to the midposition, where it was
again stopped and impacted. This was done on
three joints, and their wear was measured as in the
earlier experiments.
RESULTS
It is estimated that the physiologic load
on 'the cow metatarsal-phalangeal joint
used in these experiments is in the order of
250 pounds (13). It was found that static
loads of between 1200 and 1500 pounds
consistently crushed the bony supporting
elements of the joint, while they oscillated.
358
In the upright position, the joint could
withstand about 1800 pounds. As a result
of these preliminary experiments, the tests
on oscillating Joints were carried out under
1000-pound load. Tests, comparing synovia1 fluid and veronate buffer at these higher
physiologic load conditions, showed that
synovial fluid had no lubricatiag advantage
Over veronate buffer above approximately
600 pounds (Table 1). For this reason, the
remainder of the high-load testing was carried out, using buffer as a lubricant.
There was a consistent increase of approximately 10% in the coefficient of friction of joiats run under static loading at
about 24 hours. The coefficients of friction
then remained level throughout the remainder of the experiments, which in
some, ran as long as 500 hours (Fig 2A). At
the end of the experiment, there were no
discernible signs of wear i,n the joint (Fig
SA).
Repeated interruptions of the oscillatory
cycle in midposition for 2 seconds transiently increased the coefficients of friction
(Table 2), but after 15 minutes of continuous oscillation, these values returned to
those expected if the joint had just been
simply oscillated (Fig 2B). Joints run for
200 hours under a static load of 1000
pounds, with regular midcycle interrup
tions of 2 seconds, showed no obvious changes. On histologic examination, it was apTable 1. Coefficient of Friction at
Increasing Load
Load (Ib)
200
400
600
800
1000
Synovial fluid
0.0062
0.0068
0.0083*
0.0092
0.0112
Buffer
0.0117
0.0105
0.0094
0.0098
0.0115
*Erratic at this load; the lowest value is reported; experimental error (& 0.0005).
Arthritis and Rheumatism, Vol. 14, No. 3 (May-June 1971)
JOINT RESPONSE TO IMPACT LOADING
:x-
A
' =
-
-
300
400
-11
B
o*008'E-
0.0016
-
'
1
0.0028
0.0026
0.0020
0.00 18
0.0016
td
I
0
I
24
I
48
I
I
1 1 -
72
96
120"
200
500
HOURS
Fig 2. Representative coefficients of friction of joints taken every 24 hours after 30 minutes of continuous oscillation under following conditions: (a) continuous oscillation under a static load of 1000 pounds;
there is little increase in coefficient of friction; (b) oscillation under a static load of 1000 pounds with
2-second midcycle pauses; there is little change in steadystate coefficient of friction; (c) oscillation under
a static load of 500 pounds with 2-second midcycle pauses during which 500 pounds of dynamic load was
added. Coefficient of friction almost doubled in 192 hours. The experimental error in all these tests was
25%.
parent that, a t best, only the surface layers
of the cartilage had been worn away. It was
very difficult to detect any signs of cartilage
wear, on either gross or microscopic examination.
The addition of impact dynamic loading
to the oscillatory cycle caused fairly rapid
and obvious gross cartilage wear, visible as
early as 12 hours after the onset of the experiment. The coefficient of friction of these
same joints, measured by running the joint
without interruption for 30 minutes, increased almost 50y0 within the first day
(Fig 2C). Within 24 hours, small fissures
appeared peripherally in the joint cartilage, but these did ,not serve as initiating
points for the worn area, which was in a
totally and much more centrally located
part of the cartilage. After 48 hours, the
cartilage began to roughen, and after 72
Arthritis and Rheumatism, Vol. 14, No. 3 (May-lune 1971)
hours, the second layer of cartilage became
exposed. At 192 hours, the bone was visible
(Fig 4). T h e microscopic appearance of
the articular cartilage of these joints is
shown in Fig 3B.
DISCUSSION
Even under the extremely high loads
used ,in the experiments, the coefficient of
friction of cartilage on cartilage was extremely low-in the neighborhood of 0.010.
Under these test conditions, even an approximate 10% rise in the coefficient of
friction will not produce particularly high
shear at the cartilage surfaces. It is difficult
to conceive of articular cartilage wearing
under such low stresses. The significance of
the findings-that
synovial fluid loses its
lubricating advantage at high loads, and
that joint friction decreases with increasing
359
RADIN & PAUL
Fig 3. Photomicrographs of bovine articular cartilage from head of metacarpal (H and E, x 120).
A (top). After 500 hours oscillating under 1000 pounds, slight loss of surface layers of cartilage is visible.
B (bottom). After 192 hours oscillating under 500 pounds with 2-second midcycle pauses during which
500 pounds of dynamic load was added, extreme cartilage wear is evident.
360
Arthritis and Rheumatism, Vol. 14, No. 3 (May-June 1971)
JOINT RESPONSE TO IMPACT LOADING
acteristically appears in certain athletes
(15-17). If the very high forces that joints
sustain are not of short duration, the bone
underlying the joint will break. Thus, imCoefficient of friction
pact loading represents the only mechaStatic load nism compatible with preservation of the
500-lb
joint structure by which the joint cartilage
Static load 2-sec
can be subjected to extremely high loads.
1000-lb
inter2-sec
ruption
There are two possible explanations for
inter- plus 500-lb
the dramatic wear of the articular cartilage
Oscillation time
ruption impaction
after repeated impact loading. One possi0.0089
Steady oscillation (baseline) 0.0089
bility is that the high compressive loads,
Time after test
with the joint in a fixed position, squeeze
0.0515
0.0370
2 sec
out considerable cartilaginous interstitial
0.0357
0.0323
5 sec
fluid and causes a temporary high shear
0.0276
0.0298,
10 sec
0.0264
(friction) after motion was resumed. Fric0.0268
15 sec
0.0217
0.0205
60 sec
tional forces of this magnitude imply sig0.0109
0.0163
5 min
nificant cartilage surface contact which
0.0116
0.0093
10 min
could well induce wear. T h e other possibil0.0089
0.0089
15 min
ity is that large compressive stress damages
the structure and integrity of the cartilage,
load-to the joint lubrication theory have making it more vulnerable to shear stress.
been discussed in previous publications (9,- Impact loading during the interruption
almost doubles the friction to which the
13).
T h e forces to which joints are subjected cartilage is subjected, immediately after
motion is resumed, compared to what it is
in compression can be quite high-many
times body weight (14). Arthritic change under static loading. It might be that
has been reported after repetitive impact sufficiently long runs, with longer interruploading (3-5), and joint degeneration char- tions, would accomplish the same things
Table 2. Effect of Interruption and Impaction on
the Coefficient of Friction (Lubricant: Buffer,
40 cycles/min)
Fig 4. Photograph of a
joint subjected to oscillation
with additional impact loading.
There is obvious loss of cartilage centrally with bone showing through.
Arthritis and Rheumatism, Vol. 14, No. 3 (May-June 1971)
361
RADIN & PAUL
that impact does.' From a physiologic
point of view, excessive loading of the
magnitude dup1,icated i,n these experiments
is usually of brief duration, increasing 'the
probability that impact loading is a primary contributor to cartilage wear in vivo.
The contribution of cartilage autolysis to
joint wear, in ,these experiments, would
certainly be less in the shorter (192 hour)
than in the longer (500 hour) oscillation
experiments. Since it would not seem to be
significant we have disregarded these effects. The ability of articular cartilage to
maintain its mechanical functions in the
absence of living cells for such long periods
of time is, in itself, remarkable. Killing the
chondrocytes by simply freezing the articular cartilage of joints in living animals does
not produce degenerative changes. (18).
The pathophysiologic implications of experimental findi,ng reported here must be
verified in vivo, before they can be considered meaningful in the pathophysiology of
degenerative joint disease. This will be the
subject of the second report in this series.
ACKNOWLEDGMENTS
Dennis C. Pollock, Paul A. Weisser, Sheldon R.
Simon, MD and John D. MacDougall contributed
valuable technical assistance.
REFERENCES
1. Murray RO: T h e aetiology of primary
osteoarthritis of the hip. Brit J Radio1 38:
810-824, 1965
*We have found that 15-second interruptions of
the oscillatory cycle increase the immediate coefficient of friction to values even higher than do 2second interruptions with 500 pounds of added
dynamic load. The steady state coefficient of friction
does not show the same gradual increase as that
which occurred in dynamically loaded joints, but at
200 hours, the cartilage appears about half worn,
on both gross and microscopic examination. Because
the long pause under very high loads is relatively
unphysiologic, the wear capabilities of this mechanism have not been stressed in this discussion.
362
2. Sokoloff L: T h e biology of degenerative
joint disease. Chicago, University of Chicago Press, 1969
3. Hunter D, McLaughlin AIG, Perry KMA:
Clinical effects of the use of pneumatic
tools. Brit J Indust Med 2:lO-16, 1945
4. Engel A, Burch TA: Osteoarthritis in adults
by selected demographic characteristics.
United States 1960-62. Washington, DC.
US Public Health Service, 1966
5. Louyot I>, Savin R: La coxarthrose chez
l'agriculteur. Rev Rheum 33:625-632, 1966
6. Lawrence JS, Bremner JM, Bier F: Osteoarthrosis prevalence i n the population and
relationship between symptoms and x-ray
changes. Amer Rheum Dis 25:l-24, 1966
7. Bollet AJ: Current comment: an essay on
the biology of osteoarthritis. Arth Rheum
12~152-163, 1969
8. Radin EL, Paul IL, Tolkoff MJ: Subchondral bone changes in patients with early
degenerative joint disease. Arthritis Rheum
13:400-405, 1970
9. Linn FC: Lubrication of animal joints. I.
T h e arthrotripsometer. J Bone Joint Surg
49A: 1079-1098, 1967
10. Pollock DC: Friction and wear behavior in
animal joints. MS thesis, M.I.T., 1970
11. Linn FC, Radin EL: Lubrication of animal
joints. 111. T h e effects of certain chemical
alterations of the cartilage and lubricant.
Arthritis Rheum 11:674-682, 1968
12. MacDougall JD: Fatigue of bovine joints.
MS thesis, M.I.T., 1970
13. Kadin EL, Paul IL, Pollock DC: Animal
joint behavior under expressive loading.
Nature 226:554-555, 1970
14. Kydell NW: Forces acting on the femoral
head prosthesis. A study on strain gauge
supplied prostheses in living persons. Acta
Ortliop Scand:Suppl88: 1-32, 1966
15. Brodelius A: Osteoarthritis of the talar
joints in footballers and ballet dancers.
Acta Orthop Scand 30:309-314, 1961
16. Solonen KA: T h e joints of the lower extremities of football players. Ann Chir
Gynaec Fenn 55:176-180, 1966
17. Nicholas JA: Personal communication
18. Simon WH, Green WT: Unpublished data
Arthritis and Rheumatism, Vol. 14, No. 3 (May-June 1971)
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