THE
PETER
SIGNIFICANCE
OF
OF ARTICULAR
NEW
BULLOUGH,
From
the
Nuffield
Department
and
It is a general
forces
rule
it transmits.
of tendon
in a fascia
we are
fibres,
at its most
fine
and
to
the
Nuffield
structure
complex
and
of
to
electron
reveal
microscope
the
pattern
to
demonstrate
of collagen
be understood
the features
visible
microscopic
the
naked
eye
with
the
tension
related
Because
which
fibre
bundles
they
transmit.
cartilage,
The
but
the
fine
Sections
of articular
cartilage
glassy
or so-called
hyaline
(Greek
to the picture.
It needs a polarising
embedded
in the
collagen
ground
substance
and
an
The
significance
of
the
fibrils.
when it is seen as part of the gross
of healthy
and degenerate
articular
structure
to the
arrangement
are visible in a radiograph
tissues
both to the gross
in articular
demonstrate.
a formless
add little
fibres
is closely
longitudinal
of bone.
trabeculae
connective
absolute
individual
fine structure
thus revealed
can only
This paper
attempts
to correlate
to
structure
and
less
ENGLAND
of Oxford,
tissue
in the
because
bone
of these
is no
the
University
of a connective
compression
OXFORD,
Centre
is exemplified
of this material
is more
difficult
to
by simple
direct
light microscopy
reveal
matrix,
and differential
staining
methods
microscope
Surgery,
in the trabecular
function
STRUCTURE
GOODFELLOW,
Orthopaedic
at its simplest,
forces
of form
JOHN
ofOrthopaedic
the
be seen with the naked eye and
accustomed
to relate
the microstructure
interdependence
L(LALLtOS)
the
rule,
and
can
anatomy
structure
viewed
that
This
U.S.A.,
YORK,
FINE
CARTILAGE
THE
of
cartilage,
of
which
structure.
cartilage
they
are
the
consequence.
CHONDROMALACIA
This
term
is used
widely
and
imprecisely
to describe
degeneration
of cartilage
of many
degrees
of severity.
change
is tangible,
The apparent
when this variation
We prefer
to restrict
its use to the literal
meaning-soft
cartilage.
Such a
not visible,
and the surface
is smooth
and intact.
stiffness
of articular
cartilage
will of course
vary with its thickness,
but even
is allowed
for it has been shown
that there are considerable
variations
in
the
of
real
stiffness
Weichselbaum
covering
other
femoral
head
the
cartilage
over
an
articular
commented
upon
the softness
of the
parts
of the femoral
head.
Recently
there
are
contours
of cartilage
surface
perifoveal
Kempson
stiffness
(Kempson
cartilage
(1967)
in a pattern
1967).
In
as compared
has shown
that
which
1877
to that
on the
is consistent
from
subject
to subject
and from
youth
to old age.
The present
authors
have described
areas
of
soft cartilage
and correlated
these changes
to the pattern
of load distribution
(Goodfellow
and
Bullough
1967, 1968).
In both the elbow and the hip those areas which do not usually
articulate
with opposed
cartilage
always
showed
some degree
of chondromalacia.
in the
Chondromalacia
is attributed
ground
substance,
and this
haematoxylin
If the
articulation
to a decreased
diminution
can
and eosin preparations,
unloaded
non-contact
with opposed
cartilage,
content
of sulphated
mucopolysaccharides
be demonstrated
by a loss of basophilia
and more
specifically
by the Alcian
blue technique.
areas
were
never
subjected
to the mechanical
stress
chondromalacia
at those sites might be oflittle
significance,
in
of
but this is not the case.
Parts of such areas do occasionally
articulate,
usually
at some extreme
of the range
of movement,
and then the softened
cartilage
proves
mechanically
inadequate
to
support
the collagen
framework,
its complex
structure
begins
to break
up and the next phase
of degeneration
is observed.
FIBRILLATION
Articular
or a motor
substance
852
cartilage
car
of the
tyre.
fibrous
is a two-phase
Fibrillation
framework
system
is the
term
structurally
applied
analogous
to the
to
exposure
reinforced
through
concrete
loss
of ground
within.
THE
JOURNAL
OF
BONE
AND
JOINT
SURGERY
THE
SIGNIFICANCE
OF
THE
FINE
STRUCTURE
OF
ARTICULAR
853
CARTILAGE
__
FIG. 3
L:
FIGS. 1 TO 3
1-” Split line
pattern of a talus. The splits are
produced
by a pin, the tip of
r
‘
iT:
Figure
-.
- .
.
IL:
“
which
is covered
Figure
moving
.I
cartilage
the
before
pin.
lines”
That
some
is repeated
joint
fibrous
simple
all over
is constant
This
in
the surface
of
He
internal
layer
only
ofthe
small
fibre
cartilage
round
collagen
microscopically
of this method
filters,
permitting
cut
our
macroscopic
Figure
was
first
demonstrated
split
of the
that
is
technique
A split
the
is readily
results,
(Fig.
demonstrable
and
I).
The
cartilage.
if the
pricking
pattern
for each
then
we can
in the general
OF
FINE
refractile
a
path
Swedish
physician,
of joint
movement.
the
infer
direction
that
on the
of the split
pricked,
instead
of the cartilage
of section
fibres are
surface
line.
offissures
is pricked
(Fig.
3).
predominantly
the
fibres
If the superficial
These
appearing
a vertical
experiments
vertical.
STRUCTURE
orientation
of
the
fibres
may
be
studied
sections
with polarised
light (Amprino
1948).
As a refinement
a first-order
red filter between
the polarising
and the analysing
between
fibres running
at right angles
to each other.
We have
orientation
to confirm
examination.
4 shows
a section
the
lines did not in fact parallel
the movement
of
route
and with the least curvature,
the edges
this occurs
in all planes
layers
of the cartilage
the
doubly
by
followed
the lines followed
the tension
trajectories
set up by
If we accept
for the moment
that the fissures
reflect
cartilage,
and
lines
is pared away and the exposed
surface
holes
result
(Fig. 2). If the cut edge
in strict
by this
is revealed
the cleavage
by the shortest
to the surface
by examining
we have used
differentiation
sections
possible
lines
the
STUDIES
Since
of split
that
proposed
cartilage.
split line is produced
and
indicate
that in the deeper
cartilage
a pin.
cartilage
believed
arrangement
parallel
articular
with
on
to subject.
articular
1898.
normal
its surface
Benninghoff
showed
that
but that they connected,
are running
within
a pattern
subject
of the articular
surface.
He
compression
of the articular
the
exists
of pricking
from
property
Hultkrantz,
In 1925
the joint
system
expedient
ink.
introducing
3-”
Split
the cut
Figure
produced
edge of
by the
in indian
2-The
result of rethe outer layer of the
which
to the
fissure
and
augment
has
been
cut
line
the
parallel
pattern
on the
surface,
three-dimensional
to a split
and
model
line.
On
the
it has
suggested
surface
been
by
there
is a highly
refractile
zone in which
the fibres
run parallel
to the surface
(blue)
and at right
angles
to the vertical
fibres
in the depths
(red).
Figure
5 shows
a section
cut across
a split
line. The surface
layer is hardly
refractile
at all because
most of the fibres have been transected
and are viewed
end on.
The vertical
fibres in the depths
appear,
of course,
unaltered.
VOL.
50 B,
NO.
4, NOVEMBER
1968
854
P.
BULLOUGH
AND
J. GOODFELLOW
If after
demonstrating
the major
orientation
of the collagen
on the microscope
stage
through
an angle
of 45 degrees,
those
However,
at this angle to the plane
of polarised
light other
fibres
equally
distributed
between
the
red
and
the
blue
end
of the
fibres
we rotate
the section
fibres
are no longer
visible.
become
apparent
which
are
spectrum
and
therefore
Photomicrograph
of a section
of articular
cut across
a split
line.
( < 20, polarised
first-order
red filter.)
running
cartilage
light with
____
Photomicrograph
cut parallel
of a section
to the split line.
with first-order
of articular
cartilage
20, polarised
light
red filter.)
(x
Photomicrograph
surface
ofarticular
with
of a horizontal
section
cartilage.
( x 20, polarised
first-order
red filter.)
of
the
light
-;
#{149}:
-‘
.
.
,
-.
FIG.
As
at
Figure
right
4 but
angles
fibre orientation
to the principal
all
6
with
the section
45 degrees.
to
each
other
FIG.
rotated
(Fig.
there is a bracing
orientation.
Figure
7 shows
the visible
fibres
a horizontal
are running
As Figure
through
6).
Thus
we
can
deduce
running
8
7 but with the section
45 degrees.
that
system
of fibres
generally
section
parallel
of the surface
to include
to the split line.
This
THE
JOURNAL
in addition
at an
rotated
through
to
principal
angle
a split line.
is the principal
OF BONE
AND
the
of 45 degrees
In this plane
orientation
JOINT
SURGERY
THE SIGNIFICANCE
and
the
the
explanation
for
microscope
fibres
stage
running
the
has
generally
OF THE
direction
been
FINE
of
rotated
angle
at an
STRUCTURE
the
split.
through
of45
In
an
degrees
OF ARTICULAR
Figure
angle
to the
8 the
of 45
principal
same
FIG.
horizontal
1 I-Electron
with the
in cross-section.
cut
from
the
Only
same
the
orientation
fibrils.
VOL.
They
50 B,
NO.
is again
but
system
of
revealed.
section
surface.
the split
of
cartilage
cut parallel
to the split
( . 6,000.)
Figure
10-Electron
photomicrograph
line.
In this plane
of section
most
of the fibres
in cross-section.
articular
(
line.
of
are
6,OCO.)
11
FIG.
12
section
of articular
cartilage
cut immediately
beneath
and
orientation
of the fibres
is parallel
and that no fibres
are seen,
photomicrograph
of ultra-thin
section
of articular
cartilage
illustrated
in Figure
1 1 , but at a deeper
level.
The vertical
are now seen
in cross-section.
( 6,000.)
general
collagen
alignment
it is not
can,
4,
is shown
bracing
photomicrograph
of ultra-thin
surface.
Note
that the general
( 6,000.)
Figure
1 2-Electron
block
and parallel
to the section
fibres
of the articular
cartilage
and
observations,
A
..3.I0
photomicrograph
of ulLra-thin
fibrils
running
parallel
with the
of articular
cartilage
cut across
seen
Figure
section
degrees.
FIG.9
Figure
9-Ehctron
Note
the collagen
ultra-thin
section
855
CARTILAGE
possible
however,
NOVEMBER
be
1968
of
by
the
optical
demonstrated
fibres
microscopy
with
the
can
be
to visualise
electron
deduced
from
the
individual
microscope.
The
the
above
collagen
technical
856
P.
BULLOUGH
AND
J. GOODFELLOW
FIGS.
Figure
radial
head
.
13
13-Enlarged
ofan
hment
18-year-old
of the superficial
(
x 7.)
Figure
of the
C membrane
,
detached.
of the r
to the s it line
15
of part
of the
man
showing
layer
of the
14-The
cartilage
thin
arti-
A split line is seen in the
_t corner.
view of part of the periphery
of a patella showing
detachment
strands.
The relationship
of the detached
strands
TO
view
1 layer
Figure
of cartilage
pattern
15-Enlarged
in the form
of
is demonstrated.
I
j#{149}
.
. .
:.‘
FIG.
16
Figure
16-The
fibrillated
cartilage
been gently rubbed
with indian ink.
FIG.
around
Figure
intact
the fovea of a femoral
head
17-Enlarged
view of Figure
and
fibrillated
17
is demonstrated
after the surface
16 showing
the junction
between
has
the
cartilage.
THE
JOURNAL
OF
BONE
AND
JOINT
SURGERY
THE
problem
SIGNIFICANCE
is to orientate
if one
knows
the
shows
membrane.
away
it
membrane
area
ink.
The
on the
with
17 show
ink
blocks
section
ARTICULAR
from
to the
857
CARTILAGE
which
split
illustrated
has
of
split
the sections
line
(Figs.
pattern
are cut.
can
one
9 to 12) should
Only
interpret
be compared
this
lines
failure.
This
layer
if the
produced
by revealed
fibres
which
in an area
been
mucopolysaccharides.
The degenerative
process
described
cartilage
and ends with disruption
of the
in the
collagen
foregoing
framework.
Figure
gently
pattern
area
pages
To
to
surface
pulled
15 shows
fibres
cartilage.
are
seen
Figures
rubbed
of fibrillation
are seen to accord
with the split line
show
loss of staining
in the fibrillated
thin
and
superficial
adjacent
has
subject
a
cartilage
malacic.
exposed
on the
head
of
normal
is already
The
of cartilage
detachment
from
cartilage
of a patella.
artificially
is an area
and
detached
of a femoral
trapped
hidden
in healthy
cartilage,
is revealed
of the radial
head of an eighteen-year-old
surface
artificially
surface
surface
been
the
be
to do
articular
the
and they
sections
of cartilage
can
the articular
perifoveal)
Histological
sign
blistering
(Fig.
14).
it is easier
to be parallel
small
photomicrographs
visible
shows
This
as a sheet
Significantly,
a fibrillated
and
earliest
and
very
of the
OF
photographs.
of the collagen
fibres,
though
degenerates.
Figure
13, the rim
the
softening,
electron
STRUCTURE
light
the
man,
FINE
the
relationship
The
polarised
The orientation
when the cartilage
with
THE
accurately
exact
the observations.
OF
with
(which
16
indian
is typically
in the intact
cartilage.
from
its deficiency
in
begins
in areas
recognise
that
of softened
the cartilage
covering
a joint facet is organised
as a whole is to accept
that a lesion in any part may prejudice
the integrity
of it all. An interruption
in the transmission
of tension
forces
by a defect,
even
in an unloaded
area,
must lead to the setting
up of abnormal
stress
patterns
and predispose
the
adjacent
loaded
areas
to mechanical
breakdown.
SUMMARY
The
to resist
as
collagen
tension
framework
forces
by
demonstrated
gross
anatomy
and
within
of articular
cartilage
the material.
In this
polarised
light
to the naked
eye
is disposed,
paper
as in other
the fine structure
microscopy
and electron
changes
of chondromalacia
connective
tissues,
ofarticular
cartilage,
microscopy,
is related
and fibrillation.
to
the
REFERENCES
AMPRINO,
BENNINGHOFF,
R. (1948):
Recherches
et considerations
sur Ia structure
A. (1925a):
Form
und Bau der Gelenkknorpel
Mitteilung
Zeitschr,ft
A. (1925b):
BENNINGHOFF,
Zeitschrift
Form
f#{252}r
Zellforschung
GOODFELLOW,
J.
Elbow
W.,
Joint.
and
of Bone
and
HULTKRANTZ,
Joint
W.
Gesellschaft,
Bau der Gelenkknorpel
und
mikroskopische
P.
and
BULLOUGH,
50-B,
: Ueber
die
Surgery,
P. G. (1968):
222.
The
49-B,
Studies
VOL.
50 B,
Spaltrichtungen
der
G. (I 967) : Personal
communication.
A. (1877): Die senilen Veranderungen
NO.
Anatomica,
zur
5, 123.
Funktion.
Erste
76,
in ihren
2, 783.
Pattern
of Ageing
zur Funktion.
Zweiter
Teil:
of the Articular
Cartilage
of the
175.
on Age
Changes
Gelenkknorpel.
in the Human
Verhandlungen
Hip
Joint.
der
Journal
Anatomischen
Kiel, p. 248.
der Gelenke
WEICHSELBAUM,
deformans.
Acta
Anatomie,
G. (1967):
Joint
hyalin.
Beziehungen
43.
Beziehungen
Entwicklungsgeschichte,
und
ofBone
Surgery,
(1 898)
und
BULLOUGH,
Journal
J. W., and
GOODFELLOW,
KEMPSON,
f#{252}rAnatomie
du cartilage
in ihren
Sitzungsbericht
4, NOVEMBER
der
1968
kaiserlichen
Akademie
der
und
deren
Wissenschaften,
Zusammenhang
lxxv, 193.
mit der Arthritis