A HISTOLOGICAL STUDY OF AVASCULAR NECROSIS OF THE

A HISTOLOGICAL
STUDY
FEMORAL
HEAD
MARY
From
The
association
capital
as the
was
incidence
also
unanswered.
In the
hope
patients
under
with
by
Infirmary,
femur
with
of
all
transcervical
The
material
patients
prosthetic
falls
with
into
arthroplasty
became
redisplaced
osteitis
or
in
which
of
the
fractures
have
random
of age
are
discussed
upper
in forty-six
female
and
an average
K.P.5
or
since
January
femoral
as
a secondary
which
issue
male
on
operation
not
remain
these
and
other
necropsy
from
1958.
Journal
was
subjects
for
in
from
fracture
post-irradiation
study.
Twelve
segmental
heads
collapse
777).
examined
ranging
the
had
late
(page
necropsy
at primary
when
in this
done
at
removed
infected,
included
of the
taken
heads
procedure
were
was
femur
heads
femoral
heads
were
the
revascularisation
necropsies
sixty-four
selected
at
to eighty-six
years
of seventy-four.
Preparation
of specimens-Each
weeks.
Coronal
slices about
on Kodak
of
four
fifty
arthroplasty
in this
end
the
such
fractures,
light
examined
I)
excised
secondary
separately
the
with
groups:
Femoral
at
and
these
some
of
questions,
METHODS
2) seventy-eight
heads
death
throw
necrosis
basic
of
removed
AND
avascular
ofbone
been
THE
Glasgow
several
non-union
might
heads
preparation
comparison
in
femoral
to unite.
but
pattern
following
sixty
united
and
fractures;
histological
fracture
head
For
; 3)
or failed
inadequate
the
the
transcervical
Nevertheless
study
MATERIAL
from
the
necrosis
a histological
discussion,
displaced
Western
extent
avascular
that
of Pathology,
ago.
OF
FRACTURE
SCOTLAND
years
the
NECROSIS
GLASGOW,
fractures
many
necrosis,
played
still
Department
transcervical
role
AVASCULAR
TRANSCERVICAL
CATTO,
recognised
ofavascular
the
problems
University
of
fragment
and
the
OF
AFTER
femoral
head
was fixed in 10 per cent formal
millimetres
thick were cut on a band saw and
four
or Kodalith
film using
a Victor
Raymax
50 machine
saline
for
radiographs
at twenty-five
at least two
were taken
kilovolts
and five
amperes.
The bone slabs were subsequently
decalcified
in formic
citrate
buffer
(Meyer
1956), washed
overnight
and then processed
by a double
embedding
method
(Russell
1956).
After
embedding
in
paraffin
whole
sections
of the femoral
head, or head, neck and trochanter,
were cut on a Jung microtome
(model
K) and stained
with haemalum
and eosin.
In some cases the ligamentum
teres was also available;
it was cut into labelled
serial
blocks
and,
after
processing,
was stained
by haemalum
and eosin.
Specimens
of special
interest
were
also
stained
to demonstrate
elastica
(Weigert
and Orcein
methods),
mucopolysaccharides
(PAS),
connective
tissue
(Masson’s
trichrome),
reticulin
(Gordon
and Sweet),
amyloid
(congo
red) and
by some
of
Lendrum,
Fraser,
Slidders
and Henderson’s
stains
(1962)
for demonstrating
fibrin
(M.S.B.,
Masson
44/41 , Yellowsolve
I).
BONE
It is widely
necrosis
and
that
years
Fifty
of
age;
organs
or
empty
bone
basophilia
the
only
cause
by
lacunae;
and
be
seen
47 B, NO. 4, NOVEMBER
for
tumour.
before
as
age
and
control
a faint
life
and
and
ofpatients
taken
at random
exclusion
from
osteocytes
pink
shadow
with
from
in the
disappear
lacuna.
out
the
ages
to those
was
vascular
with
in those
In these
control
1957).
degree
of
transcervical
over
sixty-four
the
to
by the
whole
supply
and
radiotherapy
the
cortex,
Selakovich
pattern
histologically
bone
“
of the
the
and
necropsies
series
is recognised
actually
of
Sherman
to find
physiological
“
lamellae
deterioration
ofsimilar
the
some
interstitial
1951,
material
PATIENTS
onwards
in the
Majno
heads
death
ELDERLY
“
adult
bone
Bone
the
1965
NORMAL
early
advancing
“
infiltration
from
to examine
“
“
Rutishauser
normal
femoral
upper
femora
were
in
IN
subchondral
with
1934,
essential
loss
fractures.
in
increases
Ponieranz
therefore
osteocyte
that
especially
this
and
It was
VOL.
recognised
occurs,
(Jaffe
CHANGES
cell
cases
pelvic
presence
may
of
lose
the
its
degree
749
750
MARY
CATTO
1
FIG.
2
FIG.
Figure 1-The
bone trabecula
from a 74-year-old
patient
with a normal
hip shows patchy osteocyte
loss. There
are nuclei in the fat cells of the marrow.
Figure 2-There
is complete
loss of osteocytes
in this necrotic
bone
trabecula.
The marrow
is also necrotic
and there is loss of nuclear
staining.
(Haemalum
and eosin,
x 150.)
.,,
‘
.
,
.
..
4#{149}
,;#{149}
‘
(.
.#{149}l:.‘
1
. . . :.
,#{149}
‘‘4
.
,‘
-‘
it..
;
FIG.
Figure
central
dilated
3-Living
bone and
part of the trabecula
capillaries
are seen
3
FIG.
4
marrow
is in contrast
to Figure 4 in which there is evidence
of old necrosis
in the
devoid of osteocytes.
New living bone has been laid down on the surface.
Many
in the revascularised
marrow.
This femoral
head was removed
three years after
fracture.
(Haemalum
and eosin,
x 85.)
THE
JOURNAL
OF
BONE
AND
JOINT
SURGERY
A HISTOLOGICAL
of
osteocyte
and
loss
in the
was
always
subchondral
heads
some
from
None
of
found
it was
not
difficult
fracture
and
control
of
abundant.
tips
almost
or on
More
appearance
seen
Examination
that,
the
in normal
cartilage
bone
7).
Both
of
elderly
articular
patients
lacunae,
the
fracture.
of
any
OF
were
the
almost
of
those
neck
devoid
marrow
in the fracture
small
strands
seen
were
6).
of
changes
series.
by sudden
excrescences
Usually
in the
In practice
ischaemia
of
few,
marrow
Table
I shows
appeared
to follow
completely-surrounded
patterns
in the
fibre
after
bone
occasionally
spaces
deeper
(Fig.
were
they
were
5) and
were
HEADS
femora
treated
of adipose
cells so
giving a curiously
are
as a reaction
REMOVED
removed
WITHIN
important
to
because,
it.
no osteoarthritis
loss of chondrocytes
showed
from
FIFTEEN
DAYS
FRACTURE
from
patients
by internal
undergoing
fixation
who
primary
arthroplasty
died
within
fifteen
days
DAYS
AFTER
FRACTURE
of
details.
REMOVED
Numberofdaysafterfracture
borders
by bone,
layer.
TABLE
FEMORAL
normal
regarded
TRANSCERVICAL
patients
the
on femoral
heads
with
sometimes
a slight patchy
HEADS
were
the
in the
be
cartilage
there was
heads
from
OF
and
produced
cases,
(Fig.
FEMORAL
taken
NUMBER
of
in trabecular
trabecula
or even the area
I and 2). In two femoral
evidence
necrosis
the
wrongly
especially
femoral
were
cortex
surface.
of osteocytes
of trabeculae
ofthese
might
OF
ten
inferior
of osteocytes
matrix
the
showed
loss
of trabeculae
sometimes
they
STUDY
and
the
Absence
751
HEAD
in the head and sometimes
also in the neck of the femur.
In rather
less
cases
and particularly
in one there
was bizarre
bone
formation.
Here,
injury,
Forty-nine
of
FEMORAL
“
fibre
(Fig.
after
bone
bone.
on
between
bone
necrosis.
surfaces
bone
forming
on the surface
that these became
partly-and
spiky
heads
two-thirds
the
rarely,
distributed
unevenly
than
a third
of the
when
OF THE
a basophilic
bone
or accompany
physiological
“
in
at the
Haversian
showed
to distinguish
that
NECROSIS
in spongy
of live
femoral
to precede
Unexpectedly,
present
than
protrusions
these
were
in the
plate
trabeculae
small
which
AVASCULAR
patchy
and it was unusual
to find a whole
line to be completely
devoid
of cells (Figs.
subchondral
apart
OF
greater
bone
bone
was essentially
bounded
by a cement
cells
STUDY
ON
I
EACH
OF
THE
FIRST
FIFTEEN
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
6
8
8
10
8
4
3
4
2
1
I
2
I
I
0
Total
.
Numberofspecimens
.
HISTOLOGICAL
Fibrin
heads
and
haemorrhage
removed
fibroblasts
within
in the
sometimes
area.
extensive
appeared
in damaged
of oil cysts
ringed
of new
surface
of trabeculae
of
fracture
new
Changes
evidence
in areas
VOL.
47 B,
This
and
reaction
from
in the
in less
apparent.
spaces
an
days,
formation
was
quite
day
or even
in only
(Fig.
noticeable
very
and,
days
one
9) on
by the
and
cells
in some
slight
by
the
Foamy
later
(Fig.
there
8).
was
macrophages
It was
of osteoblasts
case
at four
days
the
surface
was
of trabeculae
day
of
fifth
was formation
of plumping
thirteenth
femoral
proliferation
and
in capillaries.
onwards
by giant
site
and
in all cases
was
in subsequent
increase
sometimes
site
there
the fourth
fracture
five
Bone
marrow
injury,
increased
by
about
at the
than
of
often
or
formation
CHANGES
at the fracture
hours
accompanied
marrow
bone
bone
site and
present
by macrophages
evidence
area
were
twenty-four
59
in some
rare
to see
on
one
the
minute
at
the
specimens.
in marrow
spaces-These
begin to be recognisable
from two days onwards.
The first
of ischaemia
was a peculiar
agglomeration
of the marrow,
most readily
recognisable
of haemopoiesis
where
large
spaces
appeared,
surrounded
by blood-forming
cells.
NO.
4,
NOVEMBER
1965
752
MARY
CATTO
.1
;;
.
I
5
FIG.
Irregular
strands
of fibre
FIG.
bone are seen in the marrow
and on the surface
of trabeculae
normal
elderly patients.
(Haemalum
and eosin,
x 100.)
6
in the femoral
heads
p.
I
__
I
FIG.
7
A normal
femoral
head with bone
forming
on the
surface
of a trabecula
and enclosing
within it fat cells.
(Haemalum
and eosin,
x 195.)
THE
JOURNAL
OF
BONE
AND
JOINT
SURGERY
of
A HISTOLOGICAL
These
cells,
Often,
in necrotic
seen
and
14).
14),
absence
of
nuclei,
or
fracture
site
that
it was
rarely
trabeculae
four
the
foveal
and
days
was
present
surrounded
until
by
A
changes
striking
were
alteration
of lipocyte
nuclei
(Figs.
blood
vessels
in marrow
(Fig.
15) could
be recognised
teres
eosinophilia
of the
from
the
fragmented
extent
from
the
fourth
or even
marrow
less
loss
eosinophilic.
these
of small
nuclei
necrotic
hecame
but
by
753
HEAD
fracture,
similar
necrosis
day
and
the
ligamentum
the fourteenth
apparently
12).
increased
FEMORAL
nuclei
after
accompanied
ofthe
and
to some
complete
10 to
was
OF THE
their
weeks
onwards,
end
of osteocyte
lost
many
(Figs.
marrow
or
NECROSIS
died,
removed
homogeneity
in bone-Loss
the
onwards,
manner
three
tags
OF AVASCULAR
heads
in fatty
From
capsular
Changes
days
ghostlike
occurred
13 and
(Fig.
four
femoral
in a faint
sometimes
by
from
STUDY
and
later.
was
walls.
bone
fifth
trabeculae
days,
but
Osteocyte
slower
and
crushed
it was
death
could
at
notable
in uncrushed
not
be
discerned
.#{248}#{149}_.
;
1.
‘
r
...‘.
,
.
.
8
FIG.
9
FIG.
8-An
oil cyst is seen in revascularised
marrow.
It is partly surrounded
by giant cells.
(Haemalum
and eosin,
. 85.) Figure 9-Active
new bone formation
and plumping
of osteoblasts
on the trabecular
surfaces
has occurred
at the fracture
site ten days after injury.
There has been much capillary
and fibroblastic
proliferation
in the marrow.
(Haemalum
and eosin,
x 160.)
Figure
until
about
the
approximately
the
femoral
on
bone
or
immediately
In
loss
of
heads
or
surfaces
or
four
removed
the
assessing
state
and
new
adjacent
of
lipocytes
absence
were
thirteenth
three
of
cellular
thought
to
fatty
ofthe
fracture.
femoral
head,
to it.
marrow,
at the
formation
fibroblast
complete,
or
nearly
of pre-existing
proliferation,
taken
with
site
an
was
evidence
presence
fracture
In
no
were
Agglomeration
the
It
was
after
bone
ischaemia.
day.
There
soon
reaction
indicate
fourteenth
weeks.
to
necrosis
of necrotic
plumping
indicate
a blood
marrow
osteocyte
loss
occasional
case
at the
blood
at
death
in
of osteoblasts
supply
of haemopoietic
and
complete,
trabecular
in the
marrow,
vessels,
in the
uncrushed
fourth
or
fifth
area
total
complete
trabeculae
day
in which
all the above
changes
except
osteocyte
loss were present
throughout
the head, it was possible
to deduce
tentatively
that necrosis
had occurred.
In general,
however,
and especially
when
these
changes
were not uniform,
no conclusion
could
be reached
until the tenth
day or later.
VOL.
47 B,
NO.
4,
NOVEMBER
1965
754
At this
time
marrow
dead and living
but the changes
was
ample
necrosis
in affected
MARY
CATTO
areas
appeared
marrow
was more readily
were even more pronounced
material,
there
was
no
real
to be complete,
the boundary
between
defined
and osteocyte
loss was becoming
apparent;
by the sixteenth
day.
In practice,
provided
there
problem
in deciding
FIG.
the
extent
of
necrosis
in femoral
10
#{149},‘: T
FIG.
11
Figure
10-Normal
haemopoietic
marrow.
Figure
1 1-Necrotic
showing
agglomeration
and loss ofnuclei.
Figure 12-Complete
marrow
spaces in a dead head seventeen
weeks after
heads
removed
than
more
femoral
head
were
opinion
on
smaller
expected
to
be
sixteen
available
complete,
days
for
amounts
often
after
the
examination.
of
material,
three
weeks
such
or
Usually
It
foolhardy,
more
12
FIG.
haemopoietic
marrow
five days after fracture
loss ofnuclei
with the shadows
of agglomerated
injury.
(Haemalum
and eosin,
x 100.)
fracture.
as
:;
seems
bone
cores,
from
the
THE
time
JOURNAL
three
or four
however,
until
blocks
to
osteocyte
give
loss
of the
a firm
can
of fracture.
OF
BONE
AND
JOINT
SURGERY
be
A HISTOLOGICAL
STUDY
OF AVASCULAR
NECROSIS
OF THE
FEMORAL
755
HEAD
DISCUSSION
Various
interpretations
bone
lacunae
alive,
and
after
it has
have
ischaemia.
been
suggested
been
placed
Some
believe
that
if the
on
the
that
blood
\
slow
until
disappearance
the
supply
can
be
..
‘
.
ID
.
t
\‘\..
restored
\
,,
bone
fifteen
-
is
days
,r,p
\..
I
r
1
:‘
.
.-
from
the
within
/
. 1
...-‘
osteocytes
disappear
L
\
\.
of
osteocytes
p.-.’
FIG.
‘V.
13
.-
FIG.
14
Normal
fatty
marrow
with a blood
vessel is shown in Figure 13 and is in contrast
to the
of lipocyte
nuclei
in Figure
14. This was ten days after injury.
The blood vessel wall
osteocytes
remain
in the bone.
(Haemalum
and eosin,
x 160.)
FIG.
Necrotic
blood
vessels
are
seen
and
bone
death
necrosis
twelve
days,
47 B,
K
not
NO.
occur
femoral
hours.
eighteen
VOL.
will
in the
4,
(Patrick
heads
Sevitt
(1964)
might
be
NOVEMBER
the
1965
of
1960).
dogs
ligamentum
eosin,
that
result
of necrosis
the
marrow
necrosed.
devoid
Some
teres.
(Haemalum
x 85.)
temporary
suggested
necrotic
is also
15
in the
Woodhouse
after
7
late
some
(l962a
of
persistence
days
b), however,
and
occlusion
of
after
the
osteocytes,
injury.
produced
blood
supply
for
It is not,
bone
for
only
example
however,
at
756
MARY
necessary
to accept
after
the
and
Catto
bone
this
interruption
1964).
is dead
exp’anation,
of the
The
shortly
the
1948,
Bonfiglio
1960)
or at the
time
of vessels
or,
tearing
seems
1954,
to
that,
Campbell
1961),
complete
of dogs
in spite
of the
1947,
this
internal
suggested
simplify
the
(1948,
tendency
to
Potter
write
and
and
about
Driscoll
complication
conception
“
1953
there
manifestations
and
of the
1960),
when
in
fact
it
1945;
is the
to imply
that
it is in some
way
term
different
Woodhouse
death
terms
(Cleveland
Wallace
1942,
is a general
Christophe,
Howard,
recognition
from
bone:
femoral
has
been
dead
or one
which
has
“
for
its
Ifwe
“
viable
clinical
are correct
heads
are
incidence
is sometimes
whether
this is a
head
“
indicating
been
this
a false
suitable.
is more
necrosis
of
indicates
“
avascular
and Fielding
1954).
The term
Brindley
1963) without
clearly
“
by
there
necrosis
dead
quickly
would
of admonitions
clinical
“
fracture
it is caused
fractures
with definite
displacement
of the femoral
it is not surprising
that there is a continuing
high
of avascular
necrosis
used (Compere
and
never
the
the
1947,
of
1959,
others,
“
reserve
time
whether
In spite
“
to
the
that bone
descriptive
and
In particular,
the term
late segmental
involved
and
late segmental
collapse
is a tendency
which
literature.
“
in the vast majority
of these
and have to be revascularised,
head
voluminous
b), Sherman
(1947),
Hodges
(1954)
late
avascular
necrosis
(Whitman
; Cave
that is late.
of the processes
Similarly
that
dead
interpretation
1949a
loss,
Phemister
(Smith
greatly
weeks
Brown
osteocyte
and
by their occlusion
from
torsion.
If it is generally
accepted
the vascular
injury,
then
a more
accurate
application
of
three
1954,
and
is at
1962a),
follows
Phemister
slow
fixation,
recently
until
(Bonfiglio
Sherman
whether
and
more
not
head
(Sherman
of manipulation
been
was
femoral
be
injury
as has
loss
to the
vascular
(Crawford
osteocyte
supply
consensus
after
Phemister
by actual
for
blood
CATTO
revascularised-an
important
distinction.
STUDY
OF
FEMORAL
HEADS
REMOVED
AFTER
VIABLE
Some
necrosis
is
known
to
1930, Hatcher
1952, Ham
femoral
heads
in which
considered
within
usual
said that at least
Femoral
fracture.
limits,
halfa
heads
in
those
which
bone
death
immediately
it was
is damaged
showed
SIXTEEN
excessive.
on either
of bone
to
half
slight
in the
depth
of dead
bone
at the
lower
edge
increase
It is not
intended
to imply
where
that
at the
the
all
the
simply
that
was found
histologically
sufficient
viable
vessels
remained
both
from
studying
the operation
that any remaining
retinacular
lower
part
of
femoral
of the
head was
retinaculum.
to
only
nourish
the
remaining
Santos
callus
the
head
and
of a live
invariably
head
edge
cortex
blood
of the
of the
vessels
to the
presumably,
the
inferior
was
not,
at the
however,
fracture
a guarantee
site
from
and
were
site.
days
In the
of bony
to ten
absence
union
THE
group.
still attached
teres alone
specifically
were made
(Charnley,
JOURNAL
OF
In
after
fixation
Blockey
BONE
AND
a
spur.
intact,
but
site.
It
heads
to the
only
one
superior
part
were sufficient
noted
this
by Schmorl
months
of good
two
a small
heads
metaphysial
evidence
of live vessels
in the
the vessels
of the ligamentum
(1948)
and Sevitt
(1964).
heads
removed
from
sixteen
present
centimetre
presented
live
(1954)
of dead bone
which
ignored.
There
were
II).
Eight
showed
a
fracture
neck
Urist
to prevent
necrosis
except
at the fracture
notes
and from
examining
the femoral
vessels
were almost
invariably
attached
whole
femoral
head in which
the surgeon
had
soft-tissue
attachment.
Similar
observations
(1930),
Phemister
In the live femoral
was
were,
there
histological
In one specimen
upper
inferior
fracture
non-comminuted
to one
to be alive.
The narrow
margin
was also regarded
as normal
and
to be alive by these criteria
(Table
increase
and
closed,
been considered
the nail track
heads judged
a
had to be made
site might
be
McLean
side ofa
confined
to
ruling
fracture
the fracture
line have
commonly
surrounded
in all eighteen
femoral
similar
DAYS
adjacent
1961), and an arbitrary
of bone death
at the
in which
ofshaft
THAN
READS
any
and Leeson
the amount
from
centimetre
FEMORAL
occur
(Phemister
to separate
MORE
FRAcTURE
injury
the
and
JOINT
to be the
(1924),
viable
presence
Purser
SURGERY
A HISTOLOGICAL
1957).
In one
four
other
were
conspicuous
unfixed
patients
STUDY
fracture
there
in whom
at the
OF
was
fracture
Thirty-six
taken
femoral
place
and
heads
NECROSIS
fibrous
immobilisation
union
was
OF THE
eighteen
inadequate
FEMORAL
weeks
dense
757
HEAD
after
the
collagen
injury
and
and
in
fibrocartilage
site.
NECROSIS
had
AVASCULAR
OF
were
at the time
THE
WHOLE
completely
FEMORAL
dead.
ofremoval,
which
In fifteen
ranged
TABLE
HEAD
of these
from
sixteen
no
days
revascularisation
to forty-two
weeks
II
MATERIAL
of all femoral
Details
Removed
sixteen
Failed
nails
Primary
.
Necropsy
Total
49
29
78
30
.
59
109
of femoral
10
heads
Foveal
3
Medium
11
8
4
6
‘
.
6
.
Total
heads
dead
fracture,
removed
weeks,
.
with
3
13
4
0
4
2
6
18
18
13
49
21
15
36
of subjects
with femoral
days
Total
Average
age
30
36
72
.
7
48
55
74
.
17
92
109
an
average
of
reaction
(Table
foveal
attached.
revascularisation,
which
fibrous
union
5).
NOVEMBER
eleven
the
weeks,
II).
In the
head
I
remained
remaining
totally
twenty-one
1965
region
In
varied
between
or at the
only
from
eight
about
a dead
inferior
margin
of the
1 5 per
and
of the
thirty-six
cent
necrotic
heads,
to three years after fracture,
with an average
had occurred,
but in thirteen
this was very
was
4,
Female
after sixteen
6
in the
early
removed
78
zone
was
heads
18
tissue
NO.
30
2
of soft
47 B,
13
0
of a tiny
VOL.
17
11
shred
(Case
25
Total
14
cellular
of
there
6
-
revascularised
4
from three weeks
some revascularisation
notable
Total
4
only
case
necrosis
4
dead
Total
vestige
Complete
R
vasculisei
3
.
Completely
any
days
spared
Large
Male
after
sixteen
I
Sex and Iige
Partly
after
168
I
Necropsy
Live
removed
triangle
Small
H
0
60
.
2
T #{220}l
60
20
Lower
head
spared
over
days
0
10
___________
Primary
replacement
Removed
sixteen
.
Alive
nails
removed
.
Details
Failed
under
days
.
replacement
heads
to almost
were
time of twenty-nine
slight and consisted
fracture
femoral
unrevascularised
without
which
line
heads
complete.
head
and
where
was
there
In one
a live
neck
a
758
MARY
PARTIAL
In fifty-five
cases)
was
of
varying
in size
roughly
classified
(less
than
femoral
heads
a wedge
from
of
a few
cent)
bone,
trabeculae
as large
10 per
NECROSIS
necrosis
living
(more
(Fig.
CATTO
than
17);
the
OF
was
THE
FEMORAL
partial.
READ
The
most
its base in the
to more than half the
33 per
cent)
numbers
(Fig.
16),
in each
common
pattern
subchondral
head.
The
with
medium
group
(10-33
are
(forty-nine
region
of the fovea,
size of this wedge
was
per
shown
cent)
and
in Table
II.
small
It was
clear that these areas
were nourished
from the ligamentum
teres.
In six cases the lower part
of the head was spared,
the upper
part being dead.
In most of these the living bone included
that around
the fovea
but in one it barely
impinged
on this zone.
In five, retinacular
tissue
containing
live blood
vessels
was recognised
some
blood
supply
came
from
the inferior
histologically
metaphysial
invariably,
In all cases
also
from
the
ligamentum
.
11’
teres.
and it is likely
that
arteries
and probably,
in which
there
16
was
in this group
though
not
partial
survival
of
l
FIG.
Figure
16-A
large vascular
wedge of living bone with its base on the foveal area
remainder
of the bone is necrotic.
Figure
17-A
small vascular
foval
wedge remains
is shown.
The
in the fernoral
head.
the femoral
head some revascularisation
of dead
any conclusion
about
the rate of revascularisation
bone had
because
occurred.
there was
It was difficult
to reach
such a wide variation
in
the amount
of initially
living bone marrow.
As might
be expected,
in general,
those
femoral
heads
with a large,
living foveal
wedge
became
revascularised
more
rapidly,
the process
being
virtually
complete
sometimes
as early as four to eight weeks
after the fracture,
whereas
those
with a small,
living foveal
wedge
sometimes
showed
only small areas of revascularisation
forty-two
weeks.
There
was no histological
evidence
in either
the complete
or partly
necrotic
femoral
that necrosis
fracture
site.
had
occurred
in more
HISTOLOGICAL
of the
Revascularisation
ofcapillaries
with
groups
marrow
offoamy
than
one
FEATURES
episode
OF
from
slight
local
damage
heads
at the
REVASCULARISATION
was recognised
macrophages
apart
after
by proliferation
(Figs.
18 and
THE
19).
JOURNAL
of fibroblasts
This
OF
was
BONE
and
usually
AND
JOINT
leashes
followed
SURGERY
A HISTOLOGICAL
STUDY
OF AVASCULAR
NECROSIS
OF THE
FEMORAL
759
HEAD
j/
;:
p
Figure
18-Foamy,
fat-laden
I 20.) Figure
19-The
the
right.
Numerous
thin
marrow
walled
is
capillaries
are
and
\
present
eosin,
but
no
osteoblast
activity
seen.
f_
It
.
:-
.
‘!
:
..
,
(:
.:
A
#{149}
I,
.
1’
-
.
,
.;.
\‘
.‘
.
._.‘c
-
‘#{149}#{149}
.
#{149}‘
\
..-
‘\‘:‘:
.
(Haemalum
/,
p--.
and
on
x 55.)
.
-.
(Hacmalum
remaining
I
,,,t,
;#;;.r.
:‘T’
.L’
r
,-;
.
-
macrophages
are seen at the edge of an area ofrevascularisation.
edge of an area of revascularisation
is seen, still necrotic
,-
,
-
.
eosin,
{\;
T
!
rT
V
‘
.
F
;4
.j.
-,.
I,.
.I.;e.:\:J.
,pr
‘+...
,
1
P,
j
..,.:
.
..
.1
A
V,
#{149}.
.
.-,..
..
:±iThI
FIG.
Figure
20-Both
revascularised.
here.
VOL.
osteoclasts
(Haemalum
The marrow
47 B,
NO.
4.
20
and osteoblasts
are seen on the surface
and eosin,
x 125.) Figure 21-No
cellular
is mostly
NOVEMBER
fibrous
1965
and only small capillaries
21
bone.
The marrow
has been
is seen in relation
to dead bone
FIG.
of dead
reaction
are present.
(Haemalum
and cosin,
x 60.)
760
MARY
by osteoclasis
of dead
(Fig.
20),
of poorly
slight,
bone
and
though
sometimes
vascularised
fibrous
laying
CATTO
down
of new
the striking
feature
being
the
In the early months
after fracture
laying
down
the marrow
of new
changes
to distinguish
at a glance
living
bone
surrounded
and dead
bone
with a few surface
excrescences
proliferative
marrow.
Later
the marrow
cellularity
dead
bone
within
trabeculae
revascularisation
was
between
bone which,
that which
had been
persisted
far
bone
on
all cellular
reaction
appeared
tissue
in the marrow
spaces
advanced,
.
:
,.
.
of
bone
were
bone
tion
r.’
,‘
.
#{149}.
..-.
.
‘--
.
. 1’
,
#{149}1
.
ii’
..a..,
#{149}<‘.
.
.
usually
a shallow
maining
necrotic
(Figs.
a blood
the
a blood
supply.
subchondral
26 and
In most
heads
of
they
were
a feature
adults
with
caisson
region,
The
was
upper
almost
were
a wedge-shaped
area
This had its base on the
and
advanced
into
the
triangle
in the
the
by
were
to supply
the
still
part
not
usually
sizeable
enough
in the
of
area
of
the
to become
at
site
the
the
but
their
own
any
spurs
neck
were
head,
and
and
femoral
a
was
on
area
cortex
part
re-
of the
Sometimes
attachments
the fracture
any
last
bone
23).
was
to revascularisation
inferior
the
(Fig.
there
of necrosis
head.
vascular
margin
of
weight-bearing
of
inferior
area
of
contribution
these
invariably
to
a larger
part
made
inferior
of
especially
and
small
.
regain
in living
femoral
of revascularisation
confined
superior
22
Twelve
weeks after fracture
much new bone containing
osteocytes
has formed
on the surface
of the dead bone
which has empty lacunae.
(Haemalum
and eosin,
< 70.)
to
in the
in a narrower
spearhead
it reached
the fracture
line
head
-
FIG.
slow
been indefined
entombed
seen
the fovea.
surface
marrow
When
#.
.
-
3), and
living
in the completely
and partly
dead
heads.
In most cases revascularisa-
was
around
articular
; I;
necrosis
not
patterns
same
femoral
.
by
disease.
The
.:
(Fig.
covered
than
it had
that clearly
to
areas
the
.
was
elderly
controls
but
in bones
of young
‘,
possible
even when
the borc.er
throughout
be smaller
It is emphasised
appear
:
.
it was
by normal
fatty or haemopoietic
marrow
of new bone
surrounded
by very cellular,
decreased
but central
cores of unresorbed
bone
(Fig. 4).
If resorption
had been unusually
active
the area of dead bone could
..
..
trabeculae
for several
years.
This made
it possible,
deduce
with
a fair degree
of certainty
to
#{149}
of dead
bone (Fig. 22).
were so clear cut that
itially.
.
surface
having
never
been dead,
contained
osteocytes
dead
and now,
after
marrow
revascularisation,
S4
‘i.)
the
to be inhibited
by the formation
(Fig. 21).
Often
osteoclasis
was
revascularised
31).
of these
capital
fragments
it was
clear
that
no contribution
to the
restoration
of
group
supply
had been made
from the neck across
the fracture
site because
there was still a
of dead
trabeculae
and fibrin
at the fracture
site (Fig. 24).
In the primary
arthroplasty
and two of the necropsy
cases this can be explained
by the absence
of fixation.
In the
group
head
in which
may have
mass
pinning
destroyed
failed,
inadequate
immobilisation
attempts
by granulation
tissue
or continuing
to bridge
the
impaction
ofthe
dead
fracture
line.
In seven
of the redisplaced
fractures
there were fragments
of dead callus
(Fig. 25) lying at the fracture
site indicating
attempted
union
and revascularisation.
In the forty cases in which
pieces
of
the neck
were available
for study,
although
the depth
of bone
necrosis
varied
from
a few
THE
JOURNAL
OF
BONE
AND
JOINT
SURGERY
A HISTOLOGICAL
millimetres
to more
was
always
and
much
surface
dead
partly
pletely
or
was
NECROSIS
OF THE FEMORAL
761
HEAD
there
revascularisation
of new
trabeculae.
necrotic
evidence
OF AVASCULAR
a centimetre
active
formation
of
there
than
very
STUDY
of
bone
on
the
In five cornfemoral
heads
a vascular
contri-
bution
from the neck with attempted
and these are described
below.
union
DISCUSSION
The
femoral
normal
head
vascular
and
neck
been
widely
investigated
Wolcott
1943;
Tucker
Harrison
1953;
Dunoyer
adopted
blood
The
by
vessels
Judet,
and
the
has
1925;
and
Lagrange
the
and
nomenclature
Trueta
and
Harrison
for the
has been used in this paper.
femoral
cervical
spaces
(Kolodny
1949; Trueta
Judet,
1955)
pattern
of
in adults
is supplied
head
with
blood
Revascularisation
epiphysial
which
run
all superior
artery
arising
from
along the neck beneath
metaphysial
branches
of dead bone is occurring
The extent
of the base of the
wedge
is marked
by arrows.
the fovea.
vessels
which
cross
the marrow
from below,
by the ligarnenturn
teres
(medial
23
FIG.
by
the obturator
artery)and
chiefly
by the retinacular
the synovium.
The superior
retinacular
and then a larger lateral epiphysial
artery
S_.#{149}#{149}
from
around
revascularised
group
which
arteries
gives offfirst
of
within the head
S.
\\
;:i;
I’
‘i-’
;‘_
‘:
.
,
‘-
.
..
1’
.,-
, .
S
.
\4$4
.
.;,.,.
‘
%..
.
S.
.
.
‘ .
,. S
-%
#{149}‘_).
. S
#{149}
.S
&5.,5‘ ,
:
.
:
.
S
I,
,
.
#{149}
,,
,
.
‘I’
.
.
..
#{182}
.... . .
.
..
.
.
‘
t’:L.
..‘
.
.S’\
.
S
#{149}
iS.
‘‘3-r
-.5
4,,
S..
4P
S
24
of the femoral
head has clearly
not
side fibrin and shattered
dead trabeculae.
FIG.
Figure
shows
24-Revascularisation
on the proximal
A frustrated
attempt
at union
has
occurred
here:
dead
eosin,
VOL.
47 B,
NO.
4,
NOVEMBER
1965
callus
\/ 80.)
can
FIG.
25
occurred
across
the fracture
line which still
(Haemalum
and eosin,
x 70.) Figure 25-be seen
at the
fracture
line.
(Haemalum
and
762
MARY
forms
an
arcade
cartilage
of
plate.
vessels
These
which
vessels
run
supply
CATTO
parallel
the
to
medial
but
and
above
upper
the
parts
line
of
of the
the
head
old
epiphysial
while
the
lowest
third
of the head
is supplied
by the inferior
metaphysial
arteries
running
in the inferior
retinaculurn.
When
a fracture
occurs
the cervical
vessels
are ruptured
and the femoral
head
then depends
for its nutrition
on any surviving
retinacular
blood
vessels-though
Badgley
(1960)
believes
that all are ruptured
in displaced
fractures-and
on those
of the ligamentum
teres.
As described
much
after
the
upper
Hulth
of the
always
the
on
retinacular
medial
(Trueta
and
demonstrated
was
frequently
the
sufficient
half
femoral
the
there
were
1953,
alone,
weight-bearing
the
whole
alone
from
any
or aided
by the
It is seen
that
area.
This
1954,
et
a!.
head.
The
amount
from
a few
area
teres
histological
revascularisation
contribution
from
amount.
This
detail
elsewhere
head remained
may
the foveal
occur
(medial
which
at the
to
arteries
to keep
alive
vulnerable
is supported
was
fovea
was
the
lower
to necrosis
by many
other
is
studies
and autoradiography
1963), tetracycline
maps
necropsy
radio-opaque
varying
degrees
callus
ofinitial
formation
the fracture,
was
quicker,
the
front
of the
necrotic
very
necrotic
the
bone
fractures
avascular
where
fracture
vessels
line
but
when
there
it is extremely
slow
is no significant
and
often
upper
were
1 and
common
in a recent
and
submitted
head
slow
fibrous
of small
important
this
part
(Bonfiglio
head
1954,
Boyd
with
follow-up
study
histology
and
known.
redisplacement
Phemister
a necrotic
(Brown
because
capital
and
of
(1949a)
Abrami
of redisplacement
fragment
1964)
were,
THE
Sevitt’s
the
findings
in 1964.
was
1957).
pockets
Small
with
bony
initially,
OF
with
femoral
four
one;
excised
or
JOINT
an
times
a live
heads
AND
their
with
be
completely
BONE
of
of
fractures
in those
almost
union
to
the
of the
revascularised
all of the
JOURNAL
dead
at
revascularisation
non-union
than
the
seen
It is, however,
transcervical
found
variable,
then
the
surrounding
tissue.
with
to become
across
sometimes
in the
is in agreement
of the femoral
reossification
arteries,
though
was
not,
and
were
of soft
much
because,
in spite of
revascularisation
tissue
revascularisation
an
and
and
the
medial
epiphysial
occasionally
it
reattachment
play
region
non-union
is well
in fractures
to
been
heads
area
with
present
(Figs.
26 and 31) in two patients
2) and in one with fibrous
union
(Case 4).
of
femoral
to
which
last
revascularisation
non-osteoblastic
had
subchondral
association
and
the
still
marrow
from the
although
there
femoral
that
of the distal femoral
neck fragment
fractures,
there
was invariably,
In comparison
of dense
teres
necrotic
(Cases
The
active
contributions
ligamentum
striking
invariably
consisted
head
partly
or
It was
very
et a!. 1955).
additional
of the
arteries
the
by necrosis
redisplaced
rate of revascularisation
and
often
continuing,
Small
periphery
about
from
necrosis,
(Judet
revascularisation
trabeculae.
across
epiphysial)
was seen in the twelve
examples
of late segmental
collapse
discussed
in greater
in this issue.
In eleven
of these
patients
with united
fractures
much
of the
dead several
years after injury.
It was unlikely
that the delay and incompleteness
of revascularisation
was brought
in the neck
samples
examined
more
head
metaphysial
most
was
as remained
patterns.
Some
and
supply
of the
such
as venography
(Hulth
1958a
and
b), phosphorus32
injection
(Boyd,
Zilversmit
and Calandruccio
1955; Boyd
and Calandruccio
(Woodhouse
l962b)
and most
recently
by Sevitt’s
(1964)
elegant
injection
1957,
extent
on the
in injection
trabeculae
vessels,
head
finding
Boyd
or
in
anastomosis
blood
inferior
of the
1956,
1955)
such
varied
remaining
fractures,
the inferior
metaphysial
head depends
to a great
and to a lesser
that, although
in practice
ligamentum
the
Cormier
teres
apparent
Judet
displaced
at the time of fracture
often
in the lower than
(1960)
believes
of the femoral
of vessels,
arteries
in these
whether
were more
d’Aubign#{233} and
Cheynel
groups
contribution
head.
Merle
usually,
arteries
in the ligamentum
inferior
ones.
It was
epiphysial
The
sometimes
upper
1953,
to nourish
medial
head.
of the
that
although
Claffey
the blood
supply
various
insufficient
by the
entire
(Harty
Harrison
between
supplied
the
head
epiphysial
especially
vessels,
studies
concluded
b, Mathon
1959)
torn.
In general,
and
are
extent
it was
and damage
of retinacular
attachments
but that when vessels
survived
they
part
1958a
arteries
the
above
destruction
manipulation
partly
SURGERY
A HISTOLOGICAL
necrotic.
It
The
has
been
STUDY
interpretation
of
suggested
immobilisation
are
OF AVASCULAR
this
(Compere
factors
NECROSIS
association
between
OF
FEMORAL
non-union
and
Wallace
1942) that
to death
of the head and
leading
THE
and
inadequate
that fibrous
763
HEAD
necrosis
is difficult.
reduction
and
poor
union
may result
in
FIGS.
26 TO 28
I-The
gross specimen
(Fig.
26), slab radiograph
(Fig. 27) and
histological
section
(Fig.
28) all
show
bony
union
which
has
Case
occurred
in
an
initially
almost
completely
necrotic head.
Only a
very small subchondral
zone of
bone (marked
with an arrow
in
Figure
26) remains
dead in the
upper
head, and it is surrounded
by
thickened
trabeculae.
FIG.
extension
of
however,
is unconvincing
more
VOL.
than
necrosis
one
47 B, NO. 4,
episode
NOVEMBER
in a partly
and
necrotic
there
of ischaemia.
1965
were
head
(Coleman
no
histological
It is more
likely
and
28
Compere
features
that
necrosis
1961).
in this
The
material
of the
capital
evidence,
to suggest
fragment
764
MARY
Case
CATTO
2-Slab
radiograph
shows
early
bony
union
thirteen
weeks
after
in a femoral
head more than half of which had initially
been dead.
Revascularisation
was almost
complete.
fracture
I-_.
Figure
Fibrous
a few
30-Case
3. Callus
union
has occurred
tiny
upper
subchondral
is seen bridging
and
the fracture
the head
which
pockets
marked
probably,
was
with
at least
line.
at the
arrows.
(Haemalum
beginning
This
initially,
and
half
is the
eosin,
necrotic
has
only
fracture
30.)
Figure
31-Case
revascularised
in the series
except
which
4.
for
was
undisplaced.
THE
JOURNAL
OF
BONE
AND
JOINT
SURGERY
A HISTOLOGICAL
contributes
STUDY
to non-union
not
the sole cause
with
a completely
by failure
in some
live
partly
or totally
but
in many
and
most
in the
the
HEALING
showed
head
specimens
weeks
IN NECROTIC
been
towards
necropsy
fracture
or
Primary
.
Necropsy
Total
and
of
three
head
the
right
almost
from
a small
by broad
10
7
12
9
14
5
I2
12
-
4
-
I
-
later
On
superior
following
subcapital
removed
1
14
15
area
19-24
months
I More than
24 months
I
2
-
-
6
-
1
1
2
3
of
her
two
the
left
plate.
four
arthroplasty
for
before.
There
years
examination
subchondral
1
prosthetic
a small
only
were
a transcervical
fracture
of the neck
She died of bronchopneumonia
nail
fracture
histological
(Figs.
suffered
a sliding
the
foveal
area
which
was
head,
which
being
spared,
demarcated
late
collapse
of
sound
bony
was
in the
had
beginning
union
had
been
revascularised,
by fibrous
tissue
apart
and
edged
26 to 28).
eighty-three-year-old
displaced
12
woman
avascular,
trabeculae
2-An
Case
12-18
with
number
fracture
HEAD
months
a transcervical
femur.
completely
FEMORAL
weeks
fixed
months
after
OF
27-52
22
years
REMOVAL
13-26
35
was
small
of the
III
AND
weeks
.
which
a very
arthroplasty
9-12
.
seventy-six-year-old
prosthetic
adjacent
and fibrin
which,
heads
which
had
seems
weeks
3
I-A
This
5-8
13
femur
fractures
formation
of redisplacement
weeks
.
right
femoral
FRACTURE
.
Case
callus
broken
trabeculae
In five cases femoral
2-4
replacement
it is certainly
below,
HEADS
weeks
.
though
As is shown
early
union.
primary
side
765
HEAD
III).
(Table
BETWEEN
head
was
because
TABLE
nails
there
removed
FEMORAL
1963).
unite.
FEMORAL
heads
progress
had
from
after
TIME
Failed
OF THE
on the
of these there
still remained
the head from the neck.
necrotic
femoral
of the
early
formation
or revascularised
to the fracture
site, in most
not yet organised,
separated
been
of callus
NECROSIS
of non-union
(Barnes
l962b,
1964 ; Nicoll
or partly
necrotic
capital
fragment
may
FRACTURE
Although
OF AVASCULAR
fracture
of
woman
with
right
femur,
her
osteoporosis
which
and
was
fixed
senile
by
dementia
a sliding
sustained
nail
a
She
plate.
died
of bronchopneumonia
thirteen
weeks later.
On microscopy
it was seen that a large foveal
ofbone
(33 to 50 per cent ofthe
head) had remained
alive.
Revascularisation
was almost
complete
but some tiny pockets
ofdead
bone remained
in the subchondral
region
in the upper
wedge
segment
of the
fracture
and
femoral
early
3-This
Case
sparing
ofa
although
union
medium-sized
a shallow
remained
necrotic.
fovea
and
revascularised
itself
was
bony
that
already
union
bridged
should
foveal
47
B,
NO.
wedge
saucer
In places
from
by
not
Case
4-A
seventy-three-year-old
months
before
his death.
This
VOL.
4, NOVEMBER
woman
fell
was attributed
death
subchondral
cortex
time,
There
was abundant
had occurred
(Fig.
head.
seventy-seven-year-old
weeks
later her
eight
necropsy
bony
1965
there
the
vascular
have
and
of bone
was
neck
callus
vascular
29).
and
a spread
on both
a gap
across
30)
sides
fractured
the neck
to bronchopneumonia.
ofrevascularisation
in the
(Fig.
callus
upper
of
bridging
the
her femur.
There
had
At
been
to much
segment
and
a spur
between
the area revascularised
the fracture
line, but the
and
there
seemed
no
head
ofthe
of the
inferior
from
fracture
the
line
reason
why,
given
femur
initially
twenty-two
impacted,
occurred.
man
fracture,
fell and fractured
unlike
the others,
the neck of his
was presumably
766
but
MARY
later
became
fibrous
union
ununited.
of
patient’s
might
Case
5-This
was
more
been
half
treated
by
and,
the
bone
of
which
necrosis
had
internal
seventy-six-year-old
that
of
were
initially
fixation
it
been
seems
still
present
necrotic
(Fig.
possible
that
there was
remaining
in
the
3 1 ).
more
upper
Had
this
satisfactory
occurred.
fixed
although
marrow
at the fovea
fracture
line
by
there
neck
were
head
had
been
had
been
32 and
P-w
33) and
a displaced
Smith-Petersen
no redisplacement
removed
when
necrotic
replaced
:
S
.
.
sustained
a
was
of the
entire
(Figs.
woman
and
trimming
showed
areas
than
manipulated
extruded
attached
subchondral
head
have
displaced.
No treatment
had been given and at necropsy
in its inferior
part, the upper
part of the fracture
line
fracture
small
the
fracture
which
was
the
Two
segment
union
partially
of
CATTO
and
lower
part
of the
.
of the
fracture,
the
was
about
,
head
neck
the
and
depth
of dead
revascularisation
occurred
nail
a small
Microscopy
millimetre
Some
had
femoral
later
inserted.
one
tissue.
head
S
r.:’
-
from
of the
the
neck
and
in
5
..:
.
S
her
months
only
fibrous
of
Eleven
a prosthesis
that
by dense
fracture
nail.
..
y
I
‘
,
‘
.5
‘S
1
-:
. ?
41’
.
.
,%
__.;-.
_.‘_‘J,
‘
:;,-
S
.5
.
#{149}
:“‘-
5%
S
.....r1’.’.
5’
-
.
. .
-.-
k
from the fovea.
marrow
adjacent
Early revascu.arisation
to the fracture
line
(Haemalum
places
and
new
here
bone
and
and
had
there
probably
indicating
might
eventually
revascularised
eosin,
x 70.)
formed.
along
ot dead
is seen.
Some
revascularised
fracture
line
a barely
sufficient
unite
it appeared
blood
unlikely
without
aid
the
from
the
fovea;
marrow
nodules
of
spaces
hyaline
or
contained
fibrocartilage
dense
collagen
were
present,
supply.
While
it seemed
possible
that the fracture
that any substantial
part of the head
would
be
later
the
necrotic
bone
might
have
collapsed.
DISCUSSION
and
While
it has
been
a live
neck
(Axhausen
generally
accepted
1922,
Santos
that
1930,
union
may
Palmer
occur
between
a dead
1934,
Phemister
1934,
THE
JOURNAL
OF
BONE
AND
femoral
Sherman
JOINT
head
and
SURGERY
A HISTOLOGICAL
Phemister
1947,
is later
Charnley
inevitably
OF AVASCULAR
et a!. 1957,
followed
by
Sevitt
collapse
NECROSIS
1964)
of the
necrotic
and have
the foveal
region.
revascularised
it is usually
become
These
revascularised
femoral
heads
sometimes
too
small
epiphysial
and
to
with
allow
arteries
any
the
unlikely,
and
of
collapse
expected
methods
subchondral
1963)
that
this
when
the
between
completely
been
they
been
used
are
to
not
union
collapse
is dead and
head
have
correctly
and
try
may
occur,
follows.
bridging
then
dead
diagnose
Veal
1963),
vascular
assays
both
venous
1959,
Harrison
Reynolds
1958)
1962,
Johansson
and more recently
of the vascular
state
and
specifically
sometimes
because
interest
of
between
is realised
be dead,
revascularised
head
head
the
most liable
of attempting
by these
may
head
from
may
As has
almost
impractical
the ultimate
certainly
revascularised
dead
enough
indicates
a totally
dead
without
ingrowing
may
later
occur
INCIDENCE
OF
AVASCULAR
of
the
except
two
than
delay
in treatment.
sixteen
unselected
primary
This
group
47 B,
of sixteen
because
NO.
fracture
the
4, NOVEMBER
initial
about
were
out
numbers
1965
which,
though
vessels
from
half
(Boyd
these
NECROSIS
Lottes
and
the assessment
at random
Calandruccio
the
fixation,
necrosis
upper
part
bony
ofonly
1963)
considerable
from a small
of the
union
part
ofthe
and
a
femoral
this
it may
the
unite,
develop
give more
then this
is unlikely
ligamentum
to become
teres.
joint
Collapse
symptoms
undergoing
Of the
to be alive
of forty-seven
or
and
TRANSCERVICAL
primary
operation
patients,
necrosis.
small
blood
vessels,
might
this site is ischaemic
patients
AFTER
patients
had
thought
are
b, Dahlgren
of
severe
1957).
oftwenty-seven
of avascular
ten
head
twenty-nine
after
in respect
is a total
inaccurate
operation
days
arthroplasty
which
and
further
All
that
and
taken
and
although
of
1950, Arden
and
and Calandruccio
sometimes
good
time
necrosis;
of study is of very
fate of the head
above,
the
incomplete
l958a
(Boyd
because
of the danger
of damaging
prognosis.
If a bone
core from
to warrant
more
sample
and
at
many
with late collapse
of the upper
segment.
An avascular
is therefore
probably
insufficient
evidence
to justify
Indeed
a bone
sample
taken
from
the subfoveal
region,
completely
bone
said
wedge
It is emphasised
head does not appear
to be associated
superior
segment
bone
core
alone
immediate
prosthetic
replacement.
though
perhaps
information
on
been
subfoveal
head
and
Hulth
may
although
1953,
McGinnis,
In some studies
head
union
is
the neck.
in prognosis
femoral
to necrosis.
While
this type
to determine
the ultimate
is a live
result.
the
1956,
ofthe
is slow
revascularisation
unfortunately,
(Rook
l962a).
on a bone
segment
union
substances
(Tucker
Ferguson
1959, Boyd
McNab
depends
which
bony
complete
and
arterial
(Woodhouse
upper
authors.
if there
and
part
that
difference
but
ischaemia
Haas
1962)
oximetry
of the femoral
this is the area
the limitations
sample
(De
upper
inadequate
fixation,
is only forming
from
some
heads;
of distinguishing
in the
It seems
usually
With
callus
interpreted
partly
and
capable
pockets
surface.
line and above
from
and of being
entirely
adequate
fixation
and revascularisation
teres vessels,
especially
when the initial
and the contributions
from
the medial
include
injection
of dyes (Price
1962), radioactive
1953, Boyd et a!. 1955, Arden
1958, Laing
and
these
VOL.
(Nicoll
the fracture
of uniting
of the joint
although
segmental
findings
have
operation,
then,
late
especially
If these
are
767
HEAD
segment.
both from
across
appear
capable
exception
serious
negligible
incomplete
the
assumed
weight-bearing
and a revascularised
head may result
from prolonged
both from across the fracture
line and from the ligamentum
necrosis
is only
partial.
When
necrosis
is complete
be
OF THE FEMORAL
This
certainly
seems
true of a completely
dead
head
which
has revascularised
solely
the fracture
line with no or almost
no assistance
from the medial
epiphysial
(ligamentum
arteries.
It is, however,
not necessarily
true ofdogs
(Tovee
and Gendron
1954, Bonfiglio
Brindley
1963)
nor of human
femoral
heads
which
are initially
almost
completely
across
teres)
1954,
are
STUDY
and
delay
prosthetic
because
also
the
twenty-seven
as were
34 per
the
done
FRACTURE
femoral
(see
Table
in treatment
was
necropsy
six of twenty
cent
arthroplasty
there
heads
removed
IV).
may
unavoidable
group
This
have
of twenty,
removed
at
at necropsy,
figure
caused
may
further
be
768
MARY
damage
to
the
blood
enough
material
to
vessels
supplying
obtain
a true
the
CATFO
capital
percentage
fragment.
of
It is hoped
avascular
necrosis
eventually
after
to collect
transcervical
fracture.
DISCUSSION
The
incidence
patients
were
of the femoral
Phemister
of avascular
treated
head
(1934)
necrosis
as assessed
in clinical
studies
apparent
its death
increase
(Santos
by lengthy
immobilisation
an
in the ununited
fracture
indicated
found
an
incidence
of
65
per
femoral
heads
of seventeen
being
examined
radiological
diagnosis
of necrosis
of the femoral
cent
IN THE
HEADS
--_____
AFTER
Partly
SIXTEEN
Completely
patients,
-
----------
Per cent
10
forty-nine
the
made
the
impossible
DAYS
dead
-
Number
in
IV
REMOVED
Live
-------
necrosis
Vv hen
density
1934).
histologically.
Early
walking
has
head in ununited
fractures
almost
TABLE
FINDINGS
of
variable.
of radiological
1930, Phemister
is very
Number
37
Per cent
Number
dead
Total
Per cent
Replacements
.
.
14
52
3
11
27
Necropsy
.
.
6
30
12
60
2
10
20
.
.
16
34
26
55
5
11
47
.
.
2
3
28
47
30
50
60
necrosis
was suspected
clinically.
Total
.
Failed
* Two
nails
late
(Boyd
primary
1957).
prevalence
prosthetic
The
arthroplasty
lowest
of late
cases
incidence
segmental
of
collapse
excluded
because
avascular
avascular
necrosis
in the united
is assessed
by
Garden
(1961)
fracture,
many
authors
finding
by
the
I 5 per cent,
Hargadon
and Pearson
24 per cent,
Cleveland
and Fielding
244
per cent and Brown
and
Abrami
28 per cent,
in patients
followed
for more
than
a year,
and Green
(1960)
345
per cent
in all fractures
followed
for two to nine years.
Linton
(1944) has pointed
out that the incidence
of late
two
segmental
collapse
to three-year
and
increases
follow-up
Cauchoix
and
as the
length
cent
in three
to 56 per
Rey
(1963)
found
that
their
of follow-up
increases
to seven
collapse
years
rate
after
; from
30 per
fracture
increased
cent
in his own
from
255
of a
series,
per
cent
at
379 per cent after two years.
Recently
Charnley
et a!. (1957)
in a series of thirtythree cases ofdisplaced
fracture
treated
by a compression
screw considered,
because
of extrusion
of the screw,
that some
degree
of vascular
damage
was present
in two-thirds
of the cases.
one
year
to
In addition
to clinical
femoral
heads
administration
and
and
b) said
patients
the
given
found
same
and
that
on
Calandruccio
and
two-thirds
examining
femoral
evidence
(1963)
secondary
showed
In twenty-four
histological
loss
ofsome
heads
removed
degree
by autoradiography
after
vascularity;
removed
speicmens
ofsome
examined
arthroplasty
at
primary
head
(1962a
arthroplasty
at necropsy
offemoral
phosphorus32
Woodhouse
Sevitt
necrosis
from
(1964)
found
in twenty-one.
heads (forty-seven)
in the present
study
about
two-thirds
were partly
or completely
it appears
necrotic
IV).
CORRELATION
Ununited
relative
and
primary
In the small unselected
group
offemoral
about
one-third
remained
viable
and
(Table
found
Boyd
at
tetracycline.
arteriographic
that
studies,
removed
OF
fractures-Although
that
necrotic
increase
ununited
in density
HISTOLOGICAL
AND
Santos
(1930)
and
femoral
heads
showed,
compared
with
the
RADIOGRAPHIC
Phemister
adjacent
usually
APPEARANCES
(1934,
1939,
within
six
osteoporotic
THE
JOURNAL
1940,
months
pelvis
OF
BONE
and
AND
1943,
of
1948)
injury,
distal
femur,
JOINT
SURGERY
a
A HISTOLOGICAL
this
was
not
prevented
in the
seen
the
STUDY
clinical
development
attended
by
Charnley
et a!.
any
Woodhouse
radiographs
of local
change
in
l962a).
Certainly
of density
that
capital
this
in the
was
fragments
accompanied
was
in the
scanty
relatively
early
trabeculae
and
and
increase
unremarkable
been
In
to
laid
rabbits
specially
and
at
femoral
radiographs
and
(Fig.
progressing
towards
subchondral
area
This
surface
revascularised
possibility
and
found
to the
heads
there
in
line
front
when
union,
bone
which
especially
further
ends
Clinical
To
revascularised
on
than
caused
as
from
the
dead
heads
when
this
very
it
between
end
bled
the
47 B,
days
ligament.
not
NOVEMBER
of
was
become
in
the
was
more
as described
of
marrow
calcification
thin and
result
of
the
reossified
by dense
more
collagen
fibrous
a tendency
the
where
new
by Hulth
an
slight
where
was
and
towards
l962a),
trabeculae
by
revascularisation
a slight increase
contains
also the
marked
bone
of the slab radiographs
of the three
patients
29,
for
example.
was
edged
bone
(1961)
seen
and
process
in
had
and
only
of the necrotic
whose
fractures
In
by
patients
notable
1965
become
Case
dense
and
LIGAMENTUM
in
two
bleeding
remaining
found
head.
patients
stated
the
the
apparently
without
density
to those
to x-rays,
seen
in relation
1958).
twenty-four
operation
who
had
excision
or
not
the
ligamentum
end
when
there
whether
acetabular
ligament
did
at
and
TERES
from
Although
small
tissue
necrosis
(Bessler
and
radiological
density
proximal
part of the
and
be analogous
very
and
were
union
and
late
of the contour
increased
Roy-Camille
eighty-nine
a note
fibrous
causing
may
Judet
1 a
fibrous
with
bony
that alteration
densely
trabeculae,
revascularised
bleeding
femoral
had
injury
of the
had
amount
4,
revascularising
(Woodhouse
broadened
In twelve
issue it was
thick
of the
after
there
of the
NO.
recognised
the
become
by
is frustrated
many
briskly,
revascularisation
of the
it was
In
covered
had
there
but
necrotic
(Judet,
thirty-four
which
heads
be
1957,
1961,
extrusion
broadening
dead
Figure
28).
in this
vascularisation
In
foveal
not
While
Santos
(1930),
(1947)
described
a
hip.
it was
area
cases
Slight
in
to
in a pseudarthrosis
sixteen
section.
Boyd
Hulth
evidence
that
was commonly
much
summarise,
most
remained
The
appearances-In
more
1956,
1961,
in the normal
was probably
when
when
36).
(1960).
bony
of progress.
bone
may
the
heads
the
which
bone
was
fracture
in the
was
Harris
femoral
showed
no
indeed
there
of unresorbed
THE
VOL.
femoral
function
great
alteration
in density
heads
was found
in two
of
area,
any
live
Muller
weight-bearing
surface
was the first radiological
evidence
of bone
1961, Barnes
l962a,
Woodhouse
1962a).
A zone
of increased
by thick
reossified
trabeculae
was often
found
later in the most
Muller
caused
bled
dead
subfoveal
zone
in the reossified
in
broad
bone
trabeculae
(Figs.
26
segmental
collapse
reported
elsewhere
head
MacNab
and
presumably
head
37).
United
fractures-No
revascularising
femoral
of the
of
patients
34 to
stopped.
mobilisation
femoral
these
two activities.
Sherman
and Phemister
vascularisation
clinical
Bobechko
heads
the
(Figs.
on the
and
Bessler
of ununited
lack
so at the
to x-rays
have
down
by
of
some
was
early
of the
Haas
with
area
because
ofdensity
in
appeared
revascularised
walking.
this
histologically
absolute
patients
thickness
except
in the
This lack of porosis
fibrocartilage
avascular
(De
of this series
slab radiographs
by increased
radiotranslucency;
trabecular
trabeculae.
since
1958,
on the ratio
of
1948,
1949) and
probably
series
769
HEAD
could not have been forecast
on the radiographic
appearances.
marrow
there
may be osteoclastic
resorption
of dead
bone
on the surface
of dead
trabeculae.
The density
to x-rays
of
the reossifying
area
depends
Phemister
(1939,
1940,
1943,
them
OF THE FEMORAL
Necrosis
Bardenstein
in these
and
decrease
in this
density
and
disruption
ofthe
fracture
After
revascularisation
of dead
and laying
down
of new bone
nail
NECROSIS
osteoporosis.
radiological
Bonfiglio
1957,
OF AVASCULAR
not
from
four
bleed
there
and
and
was
the
of the
those
no
four
close
of
teres
was
none
five completely
from
very
state
of a femoral
of five
correlation
vascularity
or
770
Histological
appearances-In
days
sixteen
forty-five
.
S
after
fracture
a small
stump
only
was
was
the
MARY
CATTO
twenty-four
of
whole
still
109
ligamentum
attached
femoral
teres
at the
heads
available
fovea.
For
removed
for study
comparison
more
but
the
than
in a further
ligament
was
:::
S
.
SS5
-S
FIG.
34
Figure
34-Revascularisation
has occurred
from the fovea but is incomplete
in depth.
Broad
seen at the site where revascularisation
has stopped
and these are visible as areas of increased
slab radiograph
trabeculae
are
density
on the
(Fig. 35).
S..’
:
Figure
36-The
(Haemalum
and
broad
eosin,
trabeculae
have central
cores of dead
x 60.)
Figure 37Marrow
calcification
femoral
examined
from
of sixty-four,
the
intervening
head.
There
is no bony reaction.
selected
fifty
femoral
heads
fifteen
from
necropsies
ages.
#{149}
More
than
on
half
the
at
random
infants
ligaments
and
bone covered
by a mass of new, living
is present at the revascularisation
border
(Haemalum
at
necropsy
children
from
and eosin,
the
THE
from
75.)
patients
over
under
fourteen,
and
elderly
controls
showed
JOURNAL
OF
bone.
in this
BONE
AND
JOINT
the
nine
age
from
hyaline
SURGERY
A HISTOLOGICAL
STUDY
OF AVASCULAR
NECROSIS
OF THE FEMORAL
I
I!’
:
771
‘
-
,t.
HEAD
-
‘I
S
S
4!
#{149}?
0
&-
,,,
Figure
teres.
38-Sclerotic
(Haemalum
adjacent
FIG. 38
blood vessels
with concentr.c
fibrosis and
x 140.) Figure 39-A
completely
and eosin,
to several
vascular
FIG.
Figure
40-A
elastica,
>.
47 B,
VOL.
L
completely
225.)
Figure
NO.
4,
channels
40
18-month-old
FIG.
39
very narrow
lumina are shown in the ligamentum
obliterated
vessel in the ligamentum
teres is seen
child.
(Haemalum
and eosin,
x 225.)
FIG.
obliterated
41-A
vein
NOVEMBER
in an
I
41
vessel in the ligamentum
teres still shows elastica
in the wall.
(Weigert’s
from the ligamentum
teres of a 4-month-old
infant shows early hyaline
sclerosis.
(Haemalum
and eosin,
x 315.)
1965
772
MARY
sclerosis
chiefly
Elmore,
Malmgren
in the
affecting
acetabular
mentioned
small
and
fat pad
briefly
veins.
Sokoloff
and
These
(1963)
in
prepatellar
by Chandler
and
CATTO
appearances
synovial
fat.
Sclerosis
Kreuscher
(1932)
was
material
then
(Fig.
a solid
mass
and 40).
Perivascular
group
of obliterated
that
the
hyaline
38)
material
was
as being
as collagen.
The hyalinisation
was found
also
Sclerosis
these
months
ages
patchy
ascribed
obliterative
not
bounded
seen.
lying
amyloid,
intermediate
between
lumen
sclerotic
fibrin
or any
and
vascular
of the
of the
changes
is that
femoral
head.
they
but
The
was
earliest
material
became
between
replaced
The
lamina
vessel
(Figs.
39
was patchy,
a
stains
showed
described
it did,
by
Lendrum
in all its stages,
by reduplication
teres in two
of elastic
ofthe
fifteen
stain
laminae.
children
(Figs.
41 and 39), in the few ligaments
at
after fracture.
The reason
for describing
might,
the
ligament
obliterated.
material
in the absence
at the time of fracture,
arteries
and
thereby
While
of the
lesions
Special
by
especially
(1938).
elastic
of these
ones.
collagen,
was sometimes
accompanied
in the vessels
ofthe
ligamentum
of the blood
vessels
to involve
principally
become
external
The distribution
adjacent
to normal
fibrin
vessels
detail
sites
of hyaline
whole
media
might
in
many
by Nordenson
by the
and eighteen
months
respectively
and in the ligaments
and retinaculum
to damage
phase
revascularisation
the
substance
described
from
in the blood
infiltration
Later,
the
eventually
fibrosis
was not
vessels
sometimes
et a!. (1962)
aged four
intermediate
and
of hyaline
been
vessels
and
change
found
in the present
series
was an eccentric
the smooth
muscle
fibres
of the media
of venules.
by hyaline
have
blood
number
ofcontrol
or be thought
influence
the
of ligaments
available
material,
be
in their
viability
later
or
after
fracture
is too small to attempt
any correlation
with the vascular
state of the head,
it seems
unlikely
that obliteration
of small groups
of veins would
have any notable
effect.
It was striking
that there
was no vascular
thrombosis
in any of the sixty-nine
ligaments,
although
occasionally
a thrombosed
periphery
of the head.
stump
of the ligamentum
heads
to
which
tiny
had
The
vessel
failed
to revascularise
periphery
of the
the fovea
all tissue
was necrotic
the whole
ligamentum
to a depth
of about
half a centimetre,
alive
patent.
and
CHANGES
Degenerative
changes-The
degenerative
normal.
of the
joint
The
surface
of fibrillation
advanced
and
in the
attached
loss
with
layers
in the
retinacular
more
in the
than
remarkable
showed
deep
three
ARTICULAR
that
controls
were
cartilage
of none
of the
were
most
osteophyte
covering
after
in
these
no evidence
Nicoll
of a dead
(1963)
femoral
of the
years
all
frequent
and
necrotic
weight-bearing
fracture,
“
examined
femoral
in the
cyst
perhaps
was
cases
confined
in which
in
heads
relation
was
to
entirely
“
lower
head.
formation.
took
is “ doomed
there
the
(Hatcher
too
gloomy
from
the
almost
cartilage
1952,
a view
start.”
Three
Of the
but there
and the
this
patients
109 femoral
was no other
control
group.
patchy
loss of chondrocytes
occurred
In the femoral
heads
removed
after
bone
area
was
specimens
of disintegration
head
the
CARTILAGE
elderly
elderly
subjects
some
of the articular
cartilage.
cartilage
zone
at
and showed
necrosis
of
parts
of the vessels
being
were
usually
slow
patchy
normal
loss of chondrocytes
was rarely
exceeded
until months
had passed.
The loss exceeded
normal
in twenty-five
of the 109 femoral
marked
tag
were those
of superficial
flaking
and of fibrous
replacement
the fovea
and at the periphery
of the head.
Osteoarthritic
cartilage
normal
deeper
changes
fracture,
an
fracture
none
showed
advanced
osteoarthritis
in respect
of degenerative
changes
between
of chondrocytes-In
especially
in
teres was also available
the more
proximal
THE
normal
articular
osteoarthritis
heads
removed
after
appreciable
difference
Loss
The
least severe
changes
cartilage
around
showed
IN
fifty
changes.
changes
seen
and in three in which
revascularisation
head at the fracture
line.
In one of the
at the
areas
was
only remarkable
vascular
change
was that the vessels
of the foveal
teres were completely
necrotic
in ten out of eleven
necrotic
femoral
of the
head.
complete
kept
its
Hulth
ThE
only
loss
and
one
head,
depth
and
the
years
most
removed
of chondrocytes.
normal
It was
contour
and
1961).
in suggesting
Cellular
In
to develop
and sometimes
heads
and was
loss
JOURNAL
that
the
is usually
OF
articular
slow
BONE
AND
cartilage
and
JOINT
Phemister
SURGERY
A HISTOLOGICAL
(1934)
believed
the
that
cartilage
segmental
OF AVASCULAR
if revascularisation
would
cartilaginous
give rise to
STUDY
survive.
changes
symptoms.
seen
collapse
once
of
Even
the
NECROSIS
underlying
if it eventually
in these
femoral
This
is in contrast
deformity
OF THE FEMORAL
bone
dies
it may
occurred
fail
to
of the joint
surface
is established.
osteophytes,
osteoarthritic
occur-changes
which
cysts
“
inevitably
and
“
give
reasonably
rise
sometimes
to joint
quickly
The
minor
seemed
unlikely
to
may occur
in late
In these
covering
the still unrevascularised
upper
segment
usually
the revascularised
bone at the periphery
of the head may
Vascularisation
ofthe
cartilage
from below,
resumption
ofendochondral
773
disintegrate.
heads
with normal
contours
to the severe
changes
which
cartilage
covering
of
HEAD
cases
while
the
retains
its thickness,
that
show severe
osteoarthritis.
ossification,
formation
formation
of a new
joint
surface
may
symptoms.
SUMMARY
1 . Loss
of osteocytes
in the bone
patients
was patchy
and distinguishable
2.
Changes
in
the
haemopoietic
trabeculae
from that
marrow
ischaemia,
loss of osteocytes
rarely
3. In 109 femoral
heads
removed
determined
supply
These
by
arteries,
Some
affected.
from
heads
A variable
this
site
that
All
of the
became
inferior
of the
revascularisation
partly
or completely
heads
which
were
revascularising,
line
and
heads
there
from
described
ligamenturn
7.
the
being
elsewhere
teres
Avascular
necrosis
did
issue
appear
of
was
deposition
minimal.
of new
on
dead
bone
elderly
fracture.
indicators
of
damage
to
the
be
vascular
region
of the fracture
teres and sometimes
the
line.
by
head.
The
were
only
partly
alive
and
it was
segment
of
sole
of uniting
by vessels
with
united
the
upper
capable
bone
but
completely
be
others
remained
the
femoral
region
was usually
the last to revascularise.
remained
alive following
fracture
and twoappeared
which
to
fracture,
commonly
contrasted
to revascularise
not
sensitive
“
weeks
after fracture.
the viability
could
some
following
necrotic
This
8. Necrotic
bone showed
no alteration
revascularisation
sometimes
caused
associated
with halted
revascularisation.
suffered
region
into
of the
teres.
failed
necrotic
subfoveal
necrotic.
partly
necrotic
in this
vessels
“
most
apart
from
the
of the ligamentum
its subchondral
heads
a third
invasion
ligamentum
and
of
normal
necrosis
after
group.
spread
head least often remained
alive and
5. In a group
of unselected
femoral
thirds
were
6. Femoral
earliest
had
alive
vessels
completely
amount
the
of these
head remained
by the blood
usually
femoral
were
femoral
heads
from avascular
being complete
until three
or four
more than sixteen
days after fracture
means.
but in a number
the
heads
were nourished
retinacular
4.
histological
of the
resulting
the
in the
from
completely
of
completely
the
fracture
necrotic
absence
and developed
cause
and
across
of
femoral
proliferation
late segmental
of
collapse.
non-union.
in radiological
density.
Reossifying
bone in areas
of
an absolute
increase
of radiodensity
especially
when
This increase
of radiological
opacity
was the result
with
broadening
of the
9. Obliterative
sclerosis
of venules
in the ligamentum
even in infancy.
No thrombosis
was seen in the ligaments
heads
were completely
necrotic
and not revascularised
10. There
appeared
to be no increase
in degenerative
trabeculae.
Marrow
calcification
teres was found
in
normal
“ patients
following
fracture
butwhere
the femoral
the ligaments
were often also necrotic.
changes
in the articular
cartilage
of the
“
femoral
heads following
fracture
compared
with fifty elderly controls.
Some loss of chondrocytes
in the deep zone of the weight-bearing
area was found
in about
a quarter
of the femoral
heads.
In only one head was the cartilage
almost
completely
acellular.
An almost
normal
depth
and
a smooth
My
contour
grateful
Hospital,
of the
thanks
Glasgow,
are
due
articular
to the
for their interest
cartilage
were
orthopaedic
surgeons
retained.
of the
and for access to their records;
Western
Infirmary
to the medical
and
Southern
staff of the Glasgow
General
Royal
Mental
Hospital
and to Dr Rhoda
Taylor of Foresthall
Hospital
for autopsy
material;
to Dr A. M. McDonald
of the Royal Hospital
for Sick Children
for the samples
ofjuvenile
ligamentum
teres; to Mr Matthew
Findlay
for the histological
preparations
; and to Mr George
Kerr for the photographs.
I am particularly
indebted
to
Professor
Mr W.
a grant
VOL.
Roland
Sillar
from
47 B,
for
the
NO.
Barnes
and Mr J. T. Brown
many
of the early
Advisory
Committee
4,
NOVEMBER
1965
for their help, encouragement
arthroplasty
on Medical
specimens.
Research
and constructive
Part of the expenses
of the Department
of this
of Health
criticism
study
were
for Scotland.
and to
borne
by
774
MARY
CATTO
REFERENCES
G. P. (1958): Modern
Journal,
34, 541.
ARDEN,
G. P., and VEALL,
Trends
ARDEN,
Necrosis
in the
N.
Femoral
in the Treatment
The Use of Radioactive
Neck of Femur.
(1953):
Head
of the Fractured
in Fractured
of Femur.
Neck
Phosphorus
in Early
Proceedings
of the
Postgraduate
Detection
Royal
Society
Medical
of Avascular
of Medicine
46, 344.
AXHAU5EN,
G. (1922): Die Nekrose
des proximalen
Bruchst#{252}cks beim Schenkalhalsbruch
und ihre Bedeutung
f#{252}r
des H#{252}ftgelenk. Archivfur
Klinische
Chirurgie,
120, 325.
BADGLEY,
C. E. (1960):
Fractures
of the Hip Joint-Some
Causes
for Failure
and Suggestions
for Success.
Instructional
Course
Lectures,
American
Academy
of Orthopaedic
Surgeons,
17, 106.
BARNES,
R. (1962a)
: Intracapsular
Fractures
of the Neck
of the Femur.
In Modern
Trends
iii Orthopaedics
3.
London:
Butterworths.
BARNES,
R. (196Th): The Diagnosis
of Ischaemia
of the Capital Fragment
in Femoral
Neck Fractures.
Journal
of Bone
and Joint
Surgery,
44-B, 760.
BARNES,
R. (1964): The Unsolved
Fracture.
Scottish
Medical
Journal,
9, 45.
BESSLER,
W., and MULLER,
M.
(1961):
Le diagnostic
pr#{233}coce de la n#{233}crose
de Ia t#{234}te
f#{233}morale. Annales
de
Radiologie
(Paris),
4, 21.
BOBECHKO,
W. P., and HARRIS,
W. R. (1960): The Radiographic
Density
of Avascular
Bone.
Journal
of Bone
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