A HISTOLOGICAL FEMORAL

STUDY HEAD
MARY

OF

AVASCULAR TRANSCERVICAL
GLASGOW,
of Pathology,

NECROSIS FRACTURE

OF

THE

AFTER
CATTO,
Department

SCOTLAND
Western Infirmary, Glasgow

From

the

University

The

association

of

transcervical

fractures

of

the pattern in might

femur

with ofbone

avascular

necrosis

of

the

capital
as the and also

fragment
incidence the still with role

was

recognised
necrosis, by that played hope discussion, transcervical

many
the avascular a histological all

years
extent

ago.
and study heads have

Nevertheless
non-union throw at examined

several
death of some

basic
and these light on or January

questions,
revascularisation fractures, these necropsy 1958. and

such
remain other from

ofavascular In the under displaced

necrosis femoral fractures

unanswered. problems patients

removed been

operation since

MATERIAL The from prosthetic became osteitis in of which the For random head or material with arthroplasty redisplaced inadequate the fracture are comparison in forty-six discussed the female falls into ; 3) or failed united the sixty following fractures; heads to unite. but separately upper and end four Femoral preparation secondary in this of male the

AND groups:

METHODS I) as fifty femoral femoral which not was Journal examined from was ranging were included done heads heads procedure infected, in this for (page in sixty-four late 777). necropsies selected years at to eighty-six taken removed when had study. at the Twelve necropsy at primary fracture heads collapse

patients

transcervical

2) seventy-eight excised heads were arthroplasty issue femur subjects of the

a secondary

post-irradiation

histological

segmental

of age

with

an average

of seventy-four.
four femoral head was fixed in 10 per cent formal millimetres thick were cut on a band saw and saline for radiographs at least two were taken

Preparation of specimens-Each weeks. Coronal slices about

on Kodak

K.P.5

or Kodalith

film using

a Victor

Raymax

50 machine

at twenty-five

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 (Massons trichrome), reticulin (Gordon and Sweet), amyloid (congo red) and by some of Lendrum, Fraser, Slidders and Hendersons stains (1962) for demonstrating fibrin (M.S.B., Masson 44/41 , Yellowsolve I). BONE CHANGES IN

NORMAL

ELDERLY

PATIENTS

It is widely
necrosis and
(Jaffe

recognised
especially increases 1934, in with

that

from

early
age and

adult
bone and Majno and

life
with

onwards
deterioration 1951,

some

physiological of the vascular Selakovich the

bone
supply 1957).

occurs, that and this

subchondral advancing Rutishauser

in the

interstitial Sherman

lamellae of and

cortex,

Ponieranz

It was
osteocyte

therefore
loss in the

essential

to examine

control
heads

material

to find
ofsimilar

out
ages

the

pattern
with

and over
to

degree sixty-four the

presence

of

fractures.
years organs empty basophilia
VOL.

Fifty
of or bone and age; infiltration

normal femoral upper femora were

only by seen as cause tumour. the a faint 1965 before for

ofpatients

to those

transcervical

taken
exclusion Bone osteocytes pink

at random
from death actually in the the

from
series

necropsies
was histologically the In these

in those
radiotherapy

pelvic
of its lose

is recognised disappear lacuna.

by the whole control cell cases

lacunae; be

may the

shadow

degree 749

47 B, NO. 4, NOVEMBER

750

MARY

CATTO

FIG.

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.

FIG.

Figure central dilated

3-Living bone and part of the trabecula capillaries are seen

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

STUDY

OF

AVASCULAR

NECROSIS

OF THE

FEMORAL

HEAD

751
of the neck

of

osteocyte

loss

was

always

greater

in the

Haversian

bone

of

the

inferior

cortex

and

in the

subchondral

bone

plate

than

in spongy

bone.

Absence

of osteocytes

in trabecular

bone was essentially bounded by a cement

heads cells some apart None subchondral from small

patchy and it was unusual to find a whole line to be completely devoid of cells (Figs.
trabeculae protrusions showed of live bone a basophilic on the matrix surface.

trabecula or even the area I and 2). In two femoral

and were almost devoid of

of

these

control to precede
of

femoral

heads

showed loss

any

evidence produced
small 6).

of

those

marrow series. ischaemia

fibre

changes In practice after

were were

which it was
fracture present

were not
and

found difficult
that tips

or accompany

of osteocytes necrosis
cases, (Fig.

in the fracture by sudden

of

to distinguish

physiological almost the surfaces

between bone necrosis.

Unexpectedly, at the

in or on

two-thirds

of

the

excrescences Usually few,

bone they

of trabeculae

occasionally

abundant.

More

rarely,

fibre

bone

strands

were

seen

in the

marrow

spaces

(Fig.

5) and

were

distributed unevenly than a third of the

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, of trabeculae sometimes
Both might ofthese wrongly

bone forming on the surface that these became partly-and

spiky when appearance seen after Examination (Fig. injury, 7). they

appeared to follow completely-surrounded

patterns be in the regarded normal

the

borders by bone,
are to it.

of adipose cells so giving a curiously

important because,

femora

as a reaction

that, the

in normal cartilage

of elderly lacunae,
STUDY

articular patients especially

OF

cartilage there was in the

on femoral heads with sometimes a slight patchy layer.

REMOVED WITHIN FRACTURE

no osteoarthritis loss of chondrocytes

showed from

deeper

FEMORAL OF

HEADS

FIFTEEN

DAYS

TRANSCERVICAL

Forty-nine and
the

femoral taken
Table

heads patients
the

were
details.

removed treated

from by internal

patients fixation

undergoing who died

primary within

arthroplasty fifteen days of

ten

were

from
I shows

fracture.

TABLE
NUMBER OF FEMORAL HEADS REMOVED ON EACH OF

I
THE FIRST FIFTEEN DAYS AFTER FRACTURE

Numberofdaysafterfracture Numberofspecimens

2 8

3 8

4 10

5 8

6 4

7 3

8 4

9 2

10 1

11 I

12 2

13 I

14 I

15

Total
. .
6 0 59

HISTOLOGICAL

CHANGES

Fibrin
heads fibroblasts

and
in the

haemorrhage
within area. This

were
twenty-four reaction

present
hours often

at the fracture
of injury, increased

site
there

in all cases
was very days

and,
slight and

in some
proliferation by the

femoral
of fifth was

removed

in subsequent

sometimes appeared of oil cysts

evidence surface

extensive in damaged ringed

bone of new of trabeculae

and marrow

accompanied from about or

at the than spaces five

by

an

increase day

in capillaries. onwards cells

case

Foamy later 8).

days day

macrophages was formation rare

one

the fourth sometimes

fracture site and

and (Fig.

there

by macrophages
formation in less

by giant
or even one in only

It was
of osteoblasts was in some

to see
on the minute

of plumping at four

days,

area
fracture

of

new
site and

bone
in the

apparent.
marrow

Bone

formation
was quite

(Fig.
noticeable

9) on
by the

the

surface

of trabeculae

at
specimens.

the

thirteenth

Changes evidence in areas

VOL.

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.

47 B,

4,

NOVEMBER

1965

752

MARY

CATTO

.1

;;

I
FIG.

FIG.

Irregular

strands

of fibre

bone are seen in the marrow and on the surface of trabeculae normal elderly patients. (Haemalum and eosin, x 100.)

in the femoral

heads

of

p.

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

A HISTOLOGICAL

STUDY

OF AVASCULAR

NECROSIS

OF THE

FEMORAL

HEAD

753 eosinophilic.

These

cells, in a faint

from and

four

days

onwards,

died,

lost

their

nuclei

and

hecame

Often,
seen sometimes

in necrotic occurred 14).

14), of

femoral
ghostlike

heads

removed
(Figs.

many was onwards,

ofthe increased

weeks
12).

after
A

the
similar

fracture,
but less

these
striking

changes nuclei

were (Figs.

manner

10 to

alteration

in fatty three
tags or

marrow four
foveal

and days
end and

accompanied necrosis
ligamentum eosinophilia

by
teres

loss

of lipocyte

13 and
(Fig. by absence

From
nuclei,

or
the

of small

capsular

blood vessels in marrow (Fig. 15) could be recognised

walls.

homogeneity

of the

Changes the that fracture it was

in bone-Loss site rarely

surrounded

of osteocyte present
by

nuclei extent
necrotic

from from day

the the

fragmented fourth
was

bone fifth
and

trabeculae days,
could

crushed it was
be

at

was

to some until
apparently

and later.
slower

but death
not

notable
discerned

complete

the fourteenth

or even

Osteocyte

in uncrushed

trabeculae

marrow

.#{248}#{149}_.

;
....

1.

FIG.

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 the
on

about femoral
In assessing

the heads
surfaces

thirteenth
three the and or state new four

or soon
ofthe bone

fourteenth
There

day.
was head, no

It

was

complete,
of pre-existing proliferation,

or

nearly
trabecular

complete,
death of osteoblasts

at
in

approximately

weeks.

evidence

removed

after
femoral formation

fracture.
fibroblast were taken plumping a blood supply to indicate in the area

bone of

or
loss

immediately
lipocytes of thought cellular to

adjacent of fatty
reaction indicate

to it. marrow,
at the ischaemia.

Agglomeration the
fracture In an

with
site and

necrosis
osteocyte case

of haemopoietic marrow
loss at the fourth

marrow, vessels,
fifth day

total

presence
occasional

of necrotic

blood
or

complete
trabeculae in which

absence
were

in the

uncrushed

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

MARY

CATTO

At this

time

marrow

necrosis

in affected

areas

appeared

to be complete,

the boundary

between

dead and living but the changes

was ample

marrow was more readily were even more pronounced

there was no real

defined and osteocyte loss was becoming apparent; by the sixteenth day. In practice, provided there
problem in deciding the extent of necrosis in femoral

material,

FIG.

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
FIG.

:;

12

haemopoietic marrow five days after fracture loss ofnuclei with the shadows of agglomerated injury. (Haemalum and eosin, x 100.)

heads femoral

removed head

more were

than
available

sixteen
for

days material,

after

the such
or

fracture.
It seems

Usually
foolhardy,

three until

or four osteocyte

blocks
to give

of the
a firm

examination. three weeks

however, of fracture.
OF BONE AND

opinion
expected

on
to

smaller
be complete,

amounts
often

of

as
more

bone
from
THE

cores,
the time
JOURNAL

loss

can

be

JOINT

SURGERY

A HISTOLOGICAL

STUDY

OF AVASCULAR
DISCUSSION

NECROSIS

OF THE

FEMORAL

HEAD

755

Various bone alive, lacunae and

interpretations after it has ischaemia. been suggested

have

been Some that \

placed believe if the

on that blood

the until

slow the

disappearance osteocytes can be restored / ,,

I

of disappear

osteocytes the fifteen -

from bone days is

supply
..

within
\

L
\\..
...-

,r,p

ID

\.

t r

. 1

\..
1
:

.-

p.-.

FIG.

13

V.

.-

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.)

necrotic is also

marrow necrosed.

devoid Some

FIG.

15

Necrotic

blood

vessels

are

seen

in the

ligamentum

teres.

(Haemalum

and bone necrosis twelve eighteen

VOL.

eosin, Woodhouse

x 85.) (l962a occlusion persistence and of

death hours.

will in the days,

not femoral Sevitt might 4,

occur (1964) be

(Patrick heads of suggested

1960). dogs after that

b), however,
of the

produced

bone

temporary the late

blood

supply
for

for
example

only
at

osteocytes,

the
1965

result

of necrosis

some

days

after

injury.

It is not,

however,

47 B, K

NO.

NOVEMBER

756 necessary
after the

MARY

CATTO

to accept
interruption

this The Bonfiglio or at the of vessels

expanation,
blood

for
supply

osteocyte
to the

loss
femoral

was
head

not

complete
(Bonfiglio

until osteocyte and the

three
1954,

weeks
Brown

of the

of dogs

and bone

Catto is dead

1964). shortly 1948, 1960) tearing

consensus the time or, 1954,

seems vascular Campbell been

to injury

be

that, (Sherman

in spite 1947, whether internal

of the Sherman this fixation,

slow

loss, of

the 1947,

after

Phemister time 1959,

Phemister (Crawford by actual 1962a), follows greatly Phemister

tendency Potter and

1961), and more

is at and (Smith

fracture

of manipulation as has

whether

it is caused Woodhouse death terms quickly would by

recently

suggested

by their occlusion from torsion. If it is generally accepted the vascular injury, then a more accurate application of simplify (1948,
to write Driscoll

that bone descriptive

others, there

the

interpretation and

of the

voluminous

literature.
and

In spite 1945;
clinical

of admonitions
is a general

1949a
about

b), Sherman (1947), Hodges (1954) late avascular necrosis (Whitman

Christophe,
recognition

Howard,
of this

1953

; Cave

1960),

when

in

fact

it

is the

complication conception Similarly manifestations that dead

that is late. of the processes there and to imply

In particular, the term late segmental involved and late segmental collapse

necrosis

indicates

a false its clinical

is more

suitable. for

is a tendency that

to

reserve way

the

term

avascular from dead

necrosis bone:

it is in some

different

Ifwe

are correct heads are incidence

in the vast majority of these and have to be revascularised, (Cleveland Wallace 1942,

fractures with definite displacement of the femoral it is not surprising that there is a continuing high and Fielding 1954). The term Brindley 1963) without clearly dead
HEADS

of avascular necrosis used (Compere and femoral distinction.

STUDY

viable

head

indicating revascularised-an
SIXTEEN

is sometimes whether this is a

head

which

has
OF

never
FEMORAL

been

or one

which

has
MORE

been

important
DAYS

REMOVED FRAcTURE
FEMORAL

THAN

AFTER
VIABLE

READS

Some (Phemister to separate considered

fracture.

necrosis

is

known

to

occur

in

any

bone

immediately

adjacent ruling fracture closed,

to one

to

fracture

1930, Hatcher 1952, Ham femoral heads in which within

Femoral

and Leeson the amount those in which is damaged

death

1961), and an arbitrary of bone death at the it was excessive. side ofa
to half

had to be made site might be and Urist (1954)

from

usual halfa
heads

limits, centimetre
which

from
showed

McLean

said that at least

ofshaft

on either
confined

non-comminuted
centimetre

of bone

the fracture line have commonly surrounded in all eighteen femoral slight
similar

been considered the nail track heads judged depth

lower

to be alive. The narrow margin was also regarded as normal and to be alive by these criteria (Table bone
the

of dead bone which ignored. There were II). Eight showed a site were and
a small

increase
increase

in the
at the

of dead
edge where

at the
inferior

upper
cortex

edge

of the
neck

fracture
presented

two
spur.

a but

of the

It is not simply that was found histologically

lower part

intended

to imply

that

all

the

blood

vessels

to the

live

heads

intact,

sufficient viable vessels remained both from studying the operation that any remaining retinacular
of the head and were, presumably,

to prevent necrosis except at the fracture notes and from examining the femoral vessels were almost invariably attached
the inferior metaphysial group. In

site. It heads to the

only one

femoral of the
to

head was retinaculum.

there histological In one specimen

evidence of live vessels in the the vessels of the ligamentum

still attached teres alone

superior part were sufficient to be the (1924), viable presence Purser

SURGERY

only

nourish the remaining

whole femoral head in which the surgeon had soft-tissue attachment. Similar observations (1948) and Sevitt (1964). heads removed from sixteen present not, at the fracture a guarantee site. however, of bony days union
THE

specifically were made months of good (Charnley,

noted this by Schmorl after fixation Blockey injury the and

JOINT

Santos

(1930), Phemister In the live femoral was invariably head was

to ten

callus

In the

absence

of a live

JOURNAL

OF

BONE

AND

A HISTOLOGICAL

STUDY

OF

AVASCULAR

NECROSIS

OF THE

FEMORAL

HEAD

757 injury and in

1957).
four

In one
other

unfixed at the

fracture
in whom

there site.

was

fibrous
was

union
inadequate

eighteen
dense

weeks

after

the
and

patients

immobilisation

collagen

fibrocartilage

were

conspicuous

fracture
NECROSIS

OF

THE

WHOLE

FEMORAL

HEAD

Thirty-six had taken place

femoral and

heads at the time

were

completely which
TABLE

dead. ranged
II

In fifteen from

of these sixteen days

no

revascularisation weeks

ofremoval,

to forty-two

MATERIAL of all femoral

Details

heads

removed over days T #{220}l

0

Removed sixteen Failed Primary Necropsy nails

.
.

under days
0

Removed sixteen
60

60

replacement
. .

49
10

29
20

78
30
168

Total

59

109

Details Lower head spared 3

of femoral Foveal Small H 11

4

heads triangle

removed spared

after

sixteen

days Complete necrosis

-

Alive
___________

Medium 8
6
I

Large 6
3

Total 25
13

R vasculisei 17
4

revascularised 13
0

Total 30
4

Failed

nails

2 10

Primary replacement
Necropsy Total . .

I 6

3 18

4 18

4 13

11 49

0 21

2 15

2 36

Sex and Iige

of subjects

with femoral

heads

removed

after sixteen Total

18

days Average
78

Male
Live heads dead
.

Female
14

age

Completely

6 7
17

30 48
92

36
55 109 I

72 74

Partly

dead Total
.

after
any

fracture,
vestige of

with

an

average

of

eleven

weeks,

the

head remaining

remained

totally

necrotic heads, which

without were

cellular

reaction

(Table

II).

In the

twenty-one

removed weeks, only shred notable

case

from three weeks some revascularisation zone tissue early in the was fibrous of soft

to three years after fracture, with an average had occurred, but in thirteen this was very foveal attached. which union region In varied between or at the only from eight about a dead inferior of the 1 5 per and margin thirty-six cent of the to almost femoral

time of twenty-nine slight and consisted fracture heads complete. head and line where was a live there In one neck a

of a tiny

revascularisation, there 5). 47 B,

NO.

was

unrevascularised

(Case
VOL.

4,

NOVEMBER

1965

758
PARTIAL

MARY

CATTO

NECROSIS

OF

THE

FEMORAL

READ

In fifty-five
cases) was of

femoral
a wedge of

heads
living (more

necrosis
bone, than

was
with

partial.

The

most

common

pattern

(forty-nine

varying
roughly

in size
classified

from

a few (Fig.

trabeculae 17); the

its base in the to more than half the

33 per cent) (Fig. 16),

subchondral head. The

medium (10-33

region of the fovea, size of this wedge was

per cent) and small

as large

(less

than

10 per

cent)

numbers

in each

group

are

shown

in Table

II.

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 invariably, also from the ligamentum teres. histologically metaphysial In all cases and it is likely that arteries and probably, in which there was partial in this group though not survival of

11

16

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
head.

is shown. The in the fernoral

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

after heads at the

than

one

episode
OF

apart

from

slight

local

damage

FEATURES

REVASCULARISATION

Revascularisation

of the

marrow

was recognised macrophages (Figs.

by proliferation 18 and
THE

of fibroblasts This
OF

and

leashes followed
SURGERY

ofcapillaries

with

groups

offoamy

19).

was
BONE

usually
AND JOINT

JOURNAL

A HISTOLOGICAL

STUDY

OF AVASCULAR

NECROSIS

OF THE

FEMORAL

HEAD

759

;:
.

T
-

j/
,

{\;
,.L

Figure
eosin,

18-Foamy, fat-laden I 20.) Figure 19-The

right. Numerous thin

macrophages are seen at the edge of an area ofrevascularisation. edge of an area of revascularisation is seen, still necrotic
walled capillaries are present but no osteoblast activity

marrow
is seen.

(Hacmalum remaining
(Haemalum

and on

the

and

eosin,

x 55.) f_
/,

\
,-;

,,,t,

r
.

;#;;.r.

p--.

It
... I,

:-

#{149}

#{149}#{149} .

..
A

._.c
.;.

.
,

(:

.:

#{149}

:T
-.

!
\:: .
-,.

1
I,. P,

rT

.j.
,pr ,

;4
+...
1

.I.;e.:\:J.

..,.:

. ..

.1
FIG.

V,
.

#{149}.

.-,..

..

:iThI
FIG.

Figure 20-Both revascularised.

osteoclasts (Haemalum

20 and osteoblasts are seen on the surface and eosin, x 125.) Figure 21-No cellular

of dead reaction

21 bone. The marrow has been is seen in relation to dead bone

here.
VOL.

The marrow
NO.

is mostly
NOVEMBER

fibrous
1965

and only small capillaries

are present.

(Haemalum

and cosin,

x 60.)

47 B,

4.

760 by osteoclasis (Fig. 20), of poorly slight, of dead bone and laying

MARY

CATTO

down

of new

bone

on

the

surface

of dead

trabeculae

though sometimes vascularised fibrous

all cellular reaction appeared tissue in the marrow spaces laying down the marrow of new changes

to be inhibited by the formation (Fig. 21). Often osteoclasis was it was possible

the striking feature being the In the early months after fracture

bone (Fig. 22). were so clear cut that

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
was far

by normal fatty or haemopoietic marrow of new bone surrounded by very cellular, decreased but central cores of unresorbed even when the borc.er (Fig.
covered

persisted
advanced, to

revascularisation

for several years. This made it possible, deduce with a fair degree of certainty throughout
was

between bone which, that which had been

having never been dead, contained osteocytes dead and now, after marrow revascularisation,

by

3), and living

S4

#{149}

bone (Fig. 4). If resorption had been unusually active the area of dead bone could
appear

itially.
i.) ..

be smaller It is emphasised
to

than it had that clearly

entombed

been indefined
in living

areas

of

bone

necrosis

bone
.

were

not

seen

in the

femoral

heads

of

:
.

..

elderly controls but in bones of young

,.

they were a feature adults with caisson were

disease.

The the
tion

patterns

of revascularisation

same
was

femoral

in the completely and partly dead heads. In most cases revascularisaconfined to a wedge-shaped area

around articular

the fovea. surface

This had its base on the and advanced into the (Fig. there
still part

r.
, . #.

marrow When
usually
,
. #{149}1

in a narrower spearhead it reached the fracture line

a shallow necrotic triangle in the of inferior bone

23). was
reof the

#{149}. ..-.

. 1

maining

head superior
small

and

a larger part of

area the

of necrosis head. Sometimes

in the a
was

. .
--

.:

; I;
.
. .

ii

..a..,

#{149}<.

contribution

to revascularisation

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.)
FIG.

made inferior
these of

by
were

vascular margin of
not usually

attachments the fracture

enough on

at site
their

the but
own

to supply the
the

any inferior part

last

sizeable cortex of the

area

area of femoral

and the

any neck head,

spurs were and

slow
especially

to

regain
the

a blood
subchondral

supply.
region,

The
was

upper
almost

weight-bearing
invariably

to become

revascularised

(Figs. a blood
mass

26 and In most

31). of these capital fragments it was clear that no contribution to the restoration of

group group head

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 in which may have 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

STUDY

OF AVASCULAR

NECROSIS

OF THE FEMORAL

HEAD

761

millimetres was and

surface

to more very formation

of

than active

a centimetre revascularisation bone

there on the

always much or was

of new trabeculae. necrotic of

pletely there

dead partly evidence

In five cornfemoral heads a vascular contriunion

bution from the neck with attempted and these are described below.

DISCUSSION

The femoral

normal head

vascular and neck

pattern of in adults (Kolodny 1949; Trueta

the has 1925; and and

been widely investigated Wolcott 1943; Tucker Harrison Dunoyer adopted blood
The

1953;
1955)

Judet, and

Judet, the

Lagrange nomenclature

by vessels

Trueta and Harrison for the has been used in this paper.
head

FIG.

23
from around revascularised

femoral

is supplied

with

blood

by

Revascularisation

cervical spaces (medial

vessels which cross the marrow from below, by the ligarnenturn teres epiphysial artery arising from along the neck beneath metaphysial branches

the fovea.

of dead bone is occurring The extent of the base of the wedge is marked by arrows.

the obturator

artery)and

chiefly

by the retinacular group which

arteries

which run all superior

the synovium. The superior retinacular and then a larger lateral epiphysial artery

gives offfirst of within the head

S_.#{149}#{149}

S.

;:i; i- .
.

\\
..

\4$4

;_
S

, .

.,. ,. S

.;,.,.

%..

S.

.
-%

#{149}_) .

. S

#{149}

&5.,5 ,

.S

I,

#{149}

,,

I
.

..

..

..

t:L.
. .
S #{149}

#{182} .... . .

.S\

iS.

3-r

-.5

4,,
S..

4P

FIG.

Figure shows

24-Revascularisation on the proximal

attempt

24 of the femoral head has clearly not side fibrin and shattered dead trabeculae.
has occurred here: dead callus 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

A frustrated

at union

eosin,
VOL.

\/ 80.)

47 B,

NO.

4,

NOVEMBER

1965

762 forms cartilage an arcade plate. of These vessels vessels which supply run the

MARY

CATTO

parallel medial

to and

but

above parts

the

line of the

of head

the

old while

epiphysial the lowest

upper

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. much after the
Hulth

As described destruction manipulation upper

1958a

above

it was

concluded

that

there

were

usually, whether were more

in these

displaced

fractures, or in

and damage of retinacular attachments but that when vessels survived they of the
and

at the time of fracture often in the lower than Cormier 1956, Boyd

part are always the

vessels,

head

(Harty

1953,

Merle

dAubign#{233} and (1960) believes of the femoral teres apparent Judet in practice head. varied remaining The from teres head et

1957,

arteries
extent
retinacular

b, Mathon 1959) torn. In general, epiphysial especially Harrison the various the

although Claffey the blood supply

the inferior metaphysial head depends to a great extent on the in injection

was

on

medial and
between

arteries in the ligamentum inferior ones. It was 1953, groups the from by the that the arteries Cheynel whole alone any 1954, of vessels,

and to a lesser that, although a!. such 1955) blood trabeculae metaphysial to keep vulnerable by many of the supply

studies
demonstrated

(Trueta frequently by the head. entire of the

anastomosis

as remained which fovea the arteries alive other to necrosis studies was to was lower is at the

was the half the

insufficient medial The head.

to nourish epiphysial contribution or aided It is seen area. This

amount a few inferior vessels, most

head

supplied sometimes upper

sufficient femoral weight-bearing

alone,

ligamentum area of the finding

histological

is supported

such as venography (Hulth 1958a and b), phosphorus32 injection (Boyd, Zilversmit and Calandruccio 1955; Boyd and Calandruccio (Woodhouse l962b) and most recently by Sevitts (1964) elegant
injection patterns.

and autoradiography 1963), tetracycline maps necropsy radio-opaque there slow and is no significant often of small

Some contribution

revascularisation from the foveal

may

occur

across epiphysial)

the

fracture vessels

line

but

when

(medial

it is extremely

amount. This detail elsewhere head remained

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 about from very by necrosis redisplaced active marrow of the distal femoral neck fragment fractures, there was invariably, revascularisation with the slow medial epiphysial occasionally it
fibrous

of revascularisation was brought in the neck samples examined varying

and callus

because, in spite of across variable, then the

the seen at dead the

degrees the

ofinitial
(Judet

necrosis,

and

much

reossification

formation

et a!. 1955).

In comparison from the although

non-osteoblastic to

revascularisation arteries, though was not, and

the fracture, was quicker,

revascularisation trabeculae.

rate of revascularisation and often continuing,

front consisted of dense contributions additional

tissue were

surrounding sometimes

Small

revascularisation

periphery arteries
necrotic or

of the of the very

bone

head necrotic that still

where

there teres

had which heads

been play and

reattachment an this important head

of soft part

tissue. Sevitts

It is, however, findings was union Small bony

the of the

ligamentum the

in the with Boyd

revascularisation

partly striking the

femoral last

is in agreement to become 1954,

in 1964. almost of their an

times

It was invariably
necrotic

area

of the femoral region (Bonfiglio

revascularised 1957). with

upper
were

subchondral

pockets of with
four

fractures

(Cases

1 and head

present (Figs. 26 and 31) in two patients 2) and in one with fibrous union (Case 4). non-union
is well known.

The
avascular

association
femoral

of

and a necrotic (Brown

redisplacement
Phemister (1949a)

of fragment 1964) were,

THE

transcervical
non-union

fractures
to be

found

more and and

common in a recent submitted

in fractures follow-up to histology

with study

capital and Abrami

than

in those femoral

with

a live heads or
JOINT

one; partly

all of the initially,

JOURNAL OF

excised

because

of redisplacement

completely
BONE AND

SURGERY

A HISTOLOGICAL

STUDY

OF AVASCULAR

NECROSIS

OF

THE

FEMORAL

HEAD

763
is difficult.

necrotic.

The

interpretation

of

this

association

between

non-union

and

necrosis

It

has

been

suggested
are factors

(Compere
leading

and

immobilisation

Wallace 1942) that to death of the head and

inadequate that fibrous

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.

28

extension

of

necrosis

in a partly

necrotic there were

head no

(Coleman histological likely

and that

Compere in this necrosis

1961). material of the

The capital

evidence, to suggest fragment

however,
more
VOL.

is unconvincing than one episode

NOVEMBER

and

features

of ischaemia.
1965

It is more

47 B, NO. 4,

764

MARY

CATTO

Case
fracture

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.

I-_.

Figure Fibrous

a few

30-Case 3. Callus union has occurred tiny upper subchondral

is seen bridging
and

the fracture
was with

line.
at the arrows.

(Haemalum
beginning This half is the

and

eosin,

30.)

Figure

31-Case
except which

4.
for was

the head which pockets marked

necrotic has only fracture

revascularised in the series

probably,

at least

initially,

undisplaced.

THE

JOURNAL

OF

BONE

AND

JOINT

SURGERY

A HISTOLOGICAL

STUDY

OF AVASCULAR

NECROSIS

OF THE

FEMORAL

HEAD

765 it is certainly

contributes not

to non-union

by failure

of callus

formation

on the

head

side

though

the sole cause with a completely

of non-union (Barnes l962b, 1964 ; Nicoll or partly necrotic capital fragment may

1963). unite.

As is shown

below,

fractures

FRACTURE

HEALING

IN NECROTIC

FEMORAL

HEADS

Although

in some

live

or revascularised

heads

there

was

early

callus

formation

adjacent

to the fracture site, in most not yet organised, separated

been partly or totally necrotic

of these there still remained the head from the neck.

showed progress towards

broken trabeculae In five cases femoral

union. This seems

and fibrin which, heads which had

a very small number

but and
in the

in many most
early

the
weeks

femoral specimens
after

head from
fracture

had
(Table

been necropsy

removed or III).
TABLE III

because

of redisplacement arthroplasty

of the were

fracture removed

of the

primary

prosthetic

TIME

BETWEEN

FRACTURE

AND

REMOVAL

OF

FEMORAL

HEAD

2-4
weeks

5-8
weeks 7

9-12
weeks

13-26
weeks

27-52
weeks 14
-

12-18
months 5
I

19-24 months I
-

I More than 24 months 2

-

Failed Primary
Necropsy

nails

10

12
-

9 4
1

replacement
. . . .

I2
13

12
3

Total

35

22

12

14

15

Case right years

I-A
femur

seventy-six-year-old
which was fixed with

woman
a sliding

suffered
nail

plate.

a transcervical fracture of the neck She died of bronchopneumonia arthroplasty for There
which

of the

her two left

been

and
the right

three head after

femur.

months
On avascular,

later

following fracture
only a small

prosthetic four foveal which years

the examination

late was had

collapse sound
beginning

of bony

femoral
of almost

a transcervical
histological

before.
head,

union apart

in the

had

completely

area was

being demarcated

spared,

revascularised, tissue and

from

a small

superior

subchondral (Figs. 26 to 28).

area

by fibrous

edged

by broad
Case displaced

trabeculae

2-An

eighty-three-year-old
subcapital fracture of her

woman
right

with
femur,

osteoporosis
which was

and
fixed

senile
by

dementia
nail

sustained
plate.

a She

a sliding

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

femoral

head.

fracture Case
necropsy

and 3-This eight

ofa remained

early

bony

union

There was abundant had occurred (Fig. woman fell was attributed
and of bone a spread

vascular 29). and

callus

on both

sides

bridging

the

seventy-seven-year-old weeks later her

medium-sized subchondral necrotic. foveal

death
wedge saucer

fractured the neck to bronchopneumonia.

ofrevascularisation upper segment and

of

her femur. There had

ofthe of the

At been head

sparing although cortex

to much a spur

a shallow

in the

inferior

fovea
itself time,

and
was bony

that
already union

revascularised
bridged should

In places from
by not vascular have

there the
occurred.

was neck

a gap across
(Fig. 30)

between the area revascularised the fracture line, but the

and there seemed no reason

from fracture
why,

the line
given

callus

Case 4-A seventy-three-year-old months before his death. This

VOL.
47 B,

man fracture,

fell and fractured unlike the others,

the neck of his was presumably

femur initially

twenty-two impacted,

NO.

4, NOVEMBER

1965

766 but
fibrous ununited. segment patients of

MARY

CATTO

later

became
union the of Two fracture

partially
the small head been fracture more

displaced. No treatment had been given and at necropsy in its inferior part, the upper part of the fracture line
areas half by of internal which of

there was remaining the Had upper this

subchondral than treated

bone
had

necrosis
initially it seems

were
been possible

still
necrotic

present
(Fig. that more

in 3 1 ).

fixation

satisfactory

union
Case which

might
5-This was

have

occurred.
woman fixed by a sustained Smith-Petersen a displaced nail. fracture Eleven of months her femoral later the neck nail

seventy-six-year-old manipulated and

was
showed

extruded
that

and,
the

although of the
head

there neck
had

was were
been

no redisplacement removed
necrotic

of the a prosthesis
only about

fracture, was
one

the inserted.
millimetre

head

and
depth

a small
of dead

attached marrow fracture

trimming
entire

when
and that

Microscopy of the neck and in

at the fovea line (Figs.

had 32 and

been

replaced lower

by dense part

fibrous of the head

tissue. had

Some occurred

revascularisation from the

33) and

P-w .

:
S

r.:
.

..:
.. .5 S

-:

. ?

41

_._J,
:;,. #{149}
5

.5

.....r1..
.

__.;-.

,%

. .

5%

:-

-.-

from the fovea. marrow adjacent

(Haemalum

Early revascu.arisation to the fracture line

and eosin, x 70.)

ot dead is seen.

places
and

new
here and

bone
there

had

formed.
along the

Some
fracture

revascularised
line nodules

marrow
of hyaline

spaces
or

contained
fibrocartilage

dense
were

collagen
present,

probably indicating might eventually revascularised

a barely sufficient unite it appeared aid from the

blood unlikely fovea;

supply. While it seemed possible that the fracture that any substantial part of the head would be later the necrotic bone might have collapsed.

without

DISCUSSION

While

it has

been

generally

accepted

that

union

may

occur

between

a dead

femoral

head

and

a live

neck

(Axhausen

1922,

Santos

1930,

Palmer

1934,
THE

Phemister
OF BONE

1934,
AND

Sherman
JOINT

and
SURGERY

JOURNAL

A HISTOLOGICAL

STUDY

OF AVASCULAR

NECROSIS

OF THE FEMORAL

HEAD

767 that this

Phemister
is later

1947,
inevitably

Charnley
followed

et a!. 1957,
by collapse

Sevitt
of the

1964)

it is usually

assumed
segment.

(Nicoll

1963)

weight-bearing

across teres) 1954,

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 become These allow any revascularised femoral heads
with the exception

necrotic and have the foveal region.

revascularised

both from across appear capable

of subchondral

the fracture of uniting

pockets

line and above from and of being entirely

in the upper part which

sometimes

are

too

small

to

serious

collapse

of the joint

surface.

It seems

that

bony

union

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
epiphysial arteries especially findings negligible then, although union may

adequate fixation and revascularisation teres vessels, especially when the initial and the contributions from the medial
occur, usually revascularisation

is slow union is the neck.

may

and
unlikely,

incomplete
If these

and

late
when have used

segmental
the head been to try

collapse is dead and and partly

diagnose

follows. bridging dead heads; between

With callus
then of some

inadequate fixation, is only forming from

difference in prognosis

correctly and

interpreted ischaemia

be

expected
have

between
been

completely not capable

but
the

unfortunately,
femoral head

although
at the

many
time of

methods

operation,
these

they

are

of distinguishing

complete

and

incomplete

necrosis;

Veal 1963),

include injection of dyes (Price 1962), radioactive 1953, Boyd et a!. 1955, Arden 1958, Laing and vascular assays both venous (De 1962) oximetry head the upper Haas and 1962, Johansson and more recently state of the femoral from most liable of attempting authors. is a live specifically and arterial (Woodhouse depends segment

substances (Tucker Ferguson 1959, Boyd 1956, (Rook l962a). sample head Hulth l958a

1950, Arden and and Calandruccio and b, Dahlgren Lottes and the assessment taken Calandruccio at random 1963) considerable from a small part union
ofthe

McNab

1959, Harrison Reynolds 1958) of the vascular and sometimes because interest sample
head

1953, McGinnis, In some studies sometimes and (Boyd

on a bone ofthe

this is the area the limitations is realised

may

to necrosis. While this type to determine the ultimate As has subfoveal been
that

of study is of very fate of the head although the upper bony

part

by these if there
may

said wedge

above, and

of the and
femoral

be dead,
head

good
necrosis

fixation,
ofonly

revascularised

result.

It is emphasised

initial

head does not appear to be associated superior segment bone core alone immediate prosthetic replacement. though perhaps information on
almost certainly

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, blood vessels, might this site is ischaemic
unite, is unlikely

impractical the ultimate

indicates

because of the danger of damaging prognosis. If a bone core from

a totally dead head which, though

give more then this

to become

it may

revascularised the dead bone enough

completely may occur further

without later and operation

ingrowing about (Boyd

vessels half these 1957).

from patients

the

ligamentum develop joint

teres.

Collapse severe

of

symptoms

to warrant

INCIDENCE All except two

OF of

AVASCULAR the twenty-nine

NECROSIS patients

AFTER undergoing

TRANSCERVICAL primary

FRACTURE prosthetic arthroplasty

more
delay are which inaccurate
VOL.

than
unselected

sixteen

days
This

after
group were out numbers 1965

fracture

had

this

operation
patients,

done
and also

because
the

there
necropsy

was
group

unavoidable
of twenty,

in treatment. arthroplasty is a total because

NO.

oftwenty-seven

in respect ten of sixteen the

of avascular thought

necrosis.
or and

Of the
34 per the delay

twenty-seven
cent (see Table

femoral
IV). may

heads
This have

removed at necropsy,
figure may further

at
be

primary

to be alive
small

as were

six of twenty
in treatment

removed

of forty-seven are

caused

47 B,

4, NOVEMBER

768
damage enough to the blood to vessels obtain supplying a true

MARY the

CATFO fragment. avascular It is hoped necrosis after eventually transcervical to collect fracture.

capital of

material

percentage

DISCUSSION

The

incidence treated head

of avascular

necrosis

as assessed

in clinical apparent its death

of

studies increase (Santos

in

is very

variable.

Vv hen density 1934).

the

patients were of the femoral

Phemister

by lengthy immobilisation an in the ununited fracture indicated

an incidence of 65 per cent

of radiological 1930, Phemister

forty-nine patients,

(1934)

found

necrosis

femoral heads of seventeen being examined radiological diagnosis of necrosis of the femoral
TABLE
FINDINGS IN THE HEADS

histologically. Early walking has head in ununited fractures almost

IV
AFTER SIXTEEN DAYS

made the impossible

REMOVED

------Number Replacements Necropsy

. . . . . . .

Live

--_____
Per cent
37

Partly Number
14

dead
----------

Completely Number 3 2
5

dead Total

Per cent
52

Per cent 11
27

10

30

12

60

10
11

20
47

Total

16

34

26

55

Failed
* Two late

nails
primary

2 arthroplasty

3 cases excluded

28 because

47 avascular

30 necrosis

50 was suspected

60 clinically.

prosthetic

(Boyd

1957).

The

lowest

incidence

of

avascular

necrosis

is assessed

by

many

authors

by

the

prevalence

of late

segmental

collapse

in the united

fracture,

Garden

(1961)

finding

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 and one segmental and collapse follow-up Rey increases to 56 per (1963) found as the cent that length in three their of follow-up to seven collapse years rate increases after increased ; from fracture from 30 per 255 per cent cent of a series, at to three-year Cauchoix
year to

in his own

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. In addition femoral
administration

to clinical heads
and

studies, at
that found

Boyd primary
two-thirds

and

Calandruccio and
showed

(1963)
ofsome

examined
vascularity;

by autoradiography after phosphorus32

(1962a Woodhouse

removed same on

secondary
loss

arthroplasty removed at primary

head

and patients

b) said given

the
and

examining In twenty-four
evidence

femoral
ofsome

heads
degree

arthroplasty Sevitt (1964)

in twenty-one.

from found

tetracycline.
histological

speicmens

removed
offemoral

at necropsy

arteriographic

necrosis

that (Table

In the small unselected group offemoral about one-third remained viable and IV).
CORRELATION OF HISTOLOGICAL Santos ununited in density femoral compared

heads (forty-seven) in the present study about two-thirds were partly or completely

it appears necrotic

AND

RADIOGRAPHIC

APPEARANCES

Ununited found relative that

fractures-Although necrotic increase

(1930)
heads with the

and
showed,

Phemister
usually

(1934,
within

1939,
six pelvis
OF BONE

1940,
months and
AND

1943,
of distal
JOINT

1948)
a femur,
SURGERY

injury,

adjacent

osteoporotic
THE JOURNAL

A HISTOLOGICAL this was not seen in the change 1957,

STUDY

OF AVASCULAR

NECROSIS

OF THE FEMORAL

HEAD

769 presumably may Boyd Hulth not be 1957, 1961, of the

clinical
in

radiographs osteoporosis.
radiological

in this
density

series Necrosis
(De Haas

since
and

early of the and

mobilisation femoral head 1956, 1961, the

prevented
attended

the
by

development
any

of local and

MacNab

Charnley Woodhouse
nail

et a!.

Bonfiglio Certainly

Bardenstein patients

1958, with

Bessler dead

Muller heads

l962a).

in these

femoral

extrusion

disruption ofthe fracture After revascularisation of dead and laying down of new bone the reossifying area depends Phemister (1939, 1940, 1943, decrease
them that

and

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 on the ratio of 1948, 1949) and area
of lack because of

these two activities. Sherman and Phemister femoral

in the

While Santos (1930), (1947) described a it was

In the

of density
this was

in the
probably

revascularised

of ununited
function

heads
hip.

recognised
revascularising

by

capital
was

fragments accompanied trabecular trabeculae.

early

of this series slab radiographs by increased radiotranslucency; thickness except in the This lack of porosis
walking. In some

showed no indeed there which bone

much

evidence that was commonly in the normal was probably

broadening

revascularisation a slight increase contains also the

of more l962a), the

in the scanty relatively

subfoveal zone in the reossified

there was

thin and result of

reossified

patients

trabeculae
and absolute

and

this

was
and ofdensity

specially
at the

so at the
vascularisation

fracture
front

line

when
when it area

it was
had

covered
become

by dense

collagen
and

fibrocartilage

fibrous

avascular unremarkable
appeared

histologically
increase

(Figs.

34 to

36).
in the

To most

summarise, cases
by

there but more

was
(Woodhouse

a tendency where
where new seen

towards
slight

an
and had

to x-rays

revascularised broadened

in
to have Bobechko

clinical
stopped.

radiographs
This was (1960).

in
caused

marked

the (1961)
in

process
bone

trabeculae

been
rabbits

laid
by

down heads

on the (Fig. 37).

surface
and Harris

of unresorbed

dead
Slight

bone
marrow

as described
calcification

by Hulth
was

and
only

in
two

femoral

United fractures-No revascularising femoral

progressing subchondral towards area of

great alteration in density heads was found in two

bony bone union, which as in Figure necrotic remained

of the slab radiographs of the three patients

29, for was example. edged by In dense

of the necrotic whose fractures

Case 1 a fibrous very tissue

and were
small and

broad bone trabeculae (Figs. 26 segmental collapse reported elsewhere

of the

to

28). in this

In twelve issue it was

patients notable

with bony that alteration

union and late of the contour

Muller caused any

and

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 area,
when further

necrosis (Bessler and radiological density proximal part of the apparently density
seen

revascularised possibility
found

especially

when The

this very

had thick

become trabeculae,

densely causing
may

fibrous

and

without to x-rays,
in relation

of progress. ends

increased
to those

vascularisation

is frustrated

be analogous

to the

bone

in a pseudarthrosis

(Judet,

Judet

and

Roy-Camille

1958).

THE Clinical head bled on appearances-In more than section. sixteen In many thirty-four days there after was

LIGAMENTUM of the eighty-nine a note from stated

TERES patients whether acetabular the did who or had not end excision the when there from of a femoral teres was four vascularity none of five or

injury

ligamentum

bleeding

from
dead

the
heads

foveal
which

end

of the
had not

ligament.
become

Although
revascularised

the twenty-four
at

ligament
not

from
bleed

four
and

of the
those

five completely correlation

live
between

heads
the

bled

briskly,
amount of the of

in

the
bleeding

remaining
found

there
and

was
the

no

very
state of

close

operation

revascularisation
VOL.

femoral
1965

head.

47 B,

NO.

4,

NOVEMBER

770 Histological sixteen appearances-In only

MARY

CATTO

twenty-four

of

109 teres fovea.

femoral available For

heads comparison

removed but the

more ligament

than was

days

after

fracture stump

was was

the still

whole attached

ligamentum at the

for study

in a further

forty-five

a small

:::

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

trabeculae are density on the

slab radiograph

(Fig. 35).

S..

:
Figure 36-The (Haemalum and broad eosin,

#{149}

trabeculae have central cores of dead x 60.) Figure 37Marrow calcification

bone covered by a mass of new, living is present at the revascularisation border

bone. in this

femoral
examined from fifty

head.

There
heads

is no bony reaction.
selected at random

(Haemalum
at necropsy

and eosin,
from

75.)
patients over the age

femoral

of sixty-four, the intervening

fifteen ages.

from More

necropsies than half

on the

infants ligaments

and

children from the

THE

under elderly
JOURNAL

fourteen, controls
OF BONE

and showed
AND JOINT

nine

from hyaline
SURGERY

A HISTOLOGICAL

STUDY

OF AVASCULAR

NECROSIS I

OF THE FEMORAL

HEAD

771

I!

,t.
&-

S
S

#{149}?

0
I

,,,

4!

Figure teres.

38-Sclerotic (Haemalum adjacent

FIG. 38 blood vessels

and eosin, to several vascular

with concentr.c fibrosis and x 140.) Figure 39-A completely

channels in an 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.

40

FIG.

41

Figure
elastica,

40-A
>.

completely 225.) Figure

obliterated 41-A vein

vessel in the ligamentum teres still shows elastica in the wall. (Weigerts from the ligamentum teres of a 4-month-old infant shows early hyaline sclerosis. (Haemalum and eosin, x 315.)

VOL.

47 B, L

NO.

4,

NOVEMBER

1965

772
sclerosis Elmore, in the chiefly Malmgren affecting and small Sokoloff veins. (1963)

MARY

CATTO

These in

appearances synovial blood

have vessels

been from

described many sites

in

detail especially

by

acetabular briefly

fat pad

and

prepatellar and

fat. Kreuscher

Sclerosis (1932)

in the blood and infiltration Later, the might by the

vessels

of the (1938).

ligament The

was earliest

mentioned

by Chandler

by Nordenson

change found in the present series was an eccentric the smooth muscle fibres of the media of venules. by hyaline was then material a solid (Fig. mass 38) and eventually substance seen. lying the lumen of hyaline bounded

of hyaline whole media become external of these ones.

material

material became lamina

between replaced The vessel 39 (Figs.

obliterated. elastic lesions Special

described

and 40). Perivascular group of obliterated

that the hyaline material

fibrosis was not vessels sometimes

was not amyloid,

The distribution adjacent to normal

fibrin or any of the

was patchy, a stains showed

by Lendrum stain

et a!. (1962)

as being

intermediate

between

fibrin

and

collagen,

but

it did,

in all its stages, of elastic ofthe fifteen

as collagen.
Sclerosis aged four intermediate these patchy ascribed obliterative

The hyalinisation was found also months ages

was sometimes accompanied in the vessels ofthe ligamentum

by reduplication teres in two

laminae. children

and eighteen months respectively and in the ligaments and retinaculum vascular changes is that they of the blood vessels to involve principally of the femoral head.

(Figs. 41 and 39), in the few ligaments at after fracture. The reason for describing might, in the absence ofcontrol material, in their viability after be later or or be thought influence the available

sclerotic

to damage phase

at the time of fracture, arteries and thereby While the number of ligaments

revascularisation

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 vessel was seen in an attached retinacular tag at the

periphery of the head. stump of the ligamentum heads

to tiny

The

only remarkable vascular change was that the vessels of the foveal teres were completely necrotic in ten out of eleven necrotic femoral and in three in which revascularisation head at the fracture line. In one of the teres was also available the more proximal
ARTICULAR CARTILAGE

which
areas

had

at the

failed to revascularise periphery of the

was cases

confined in which

the fovea all tissue

alive and

was necrotic the whole ligamentum to a depth of about half a centimetre,

patent. CHANGES IN THE

and showed necrosis of parts of the vessels being

Degenerative degenerative normal. of the changes showed The surface

changes-The joint changes.

fifty The

normal articular

elderly cartilage

controls of none

were of the

examined femoral heads

in

relation was entirely

to

least severe changes cartilage around and osteoarthritis cartilage

were those of superficial flaking and of fibrous replacement the fovea and at the periphery of the head. Osteoarthritic loss with were most frequent and

of fibrillation advanced

in the

lower

head.

Three

patients

osteophyte

cyst

formation. this

Of the but there and the

109 femoral

heads removed after appreciable difference

Loss fracture, of chondrocytes-In

fracture none showed advanced osteoarthritis in respect of degenerative changes between

normal

was no other control group.

especially

in the changes

deeper in the

layers cartilage

elderly subjects some of the articular cartilage. covering necrotic bone

patchy loss of chondrocytes occurred In the femoral heads removed after were usually slow to develop and the years most It was
contour and

patchy normal loss of chondrocytes was rarely exceeded until months had passed. The loss exceeded normal in twenty-five of the 109 femoral
marked more remarkable in the deep zone of the weight-bearing area of the kept head. its normal In only

and sometimes heads and was

one and head,

removed

than

three
that

years
in all

after
these

fracture,
specimens

was
the

there

almost 1952, a view

complete Hulth Cellular

ThE

loss

of chondrocytes.
depth

cartilage

showed of a dead

no evidence Nicoll (1963) femoral head

of disintegration perhaps took too is doomed

(Hatcher gloomy from the

1961). that is usually

OF BONE

in suggesting loss
JOURNAL

the

articular slow
AND

cartilage Phemister
SURGERY

start.

and
JOINT

A HISTOLOGICAL (1934) believed that

STUDY

OF AVASCULAR of the

NECROSIS underlying

OF THE FEMORAL bone occurred

HEAD reasonably

773 quickly

if revascularisation

the

cartilage

would changes symptoms. collapse

survive. seen once

Even

if it eventually

dies

it may

fail

to

disintegrate.

The

minor

cartilaginous give rise to segmental cartilage covering

of

in these femoral This is in contrast of the joint

heads with normal contours to the severe changes which surface is established.

seemed unlikely to may occur in late cases while the

deformity

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 osteophytes, osteoarthritic
which inevitably

retains its thickness, that show severe osteoarthritis. ossification, formation of a new joint surface may

cysts
give

and
rise

sometimes
to joint

formation

occur-changes

symptoms.

SUMMARY

1 . Loss of osteocytes in the bone patients was patchy and distinguishable

2. Changes in the haemopoietic

trabeculae from that

marrow were

of the resulting
the

femoral heads from avascular

and most

of normal necrosis after

elderly fracture.
of

earliest

sensitive

indicators

ischaemia, loss of osteocytes rarely 3. In 109 femoral heads removed determined supply These retinacular 4.
from

being complete until three or four more than sixteen days after fracture All of these alive vessels group. necrotic
into the

weeks after fracture. the viability could damage to the vascular

be line. by

by

histological

means.

had

suffered

some

but in a number the heads were nourished arteries, femoral A variable

this site that

head remained by the blood of the inferior completely of the

spread

apart from the of the ligamentum following

head. The

region of the fracture teres and sometimes others remained

segment

usually heads amount

Some

became

fracture,
upper

were alive
of

only and
the

partly it was
femoral

affected.

subfoveal

region

commonly

revascularisation

head least often remained alive and 5. In a group of unselected femoral thirds were 6. Femoral revascularising,
line and from

its subchondral heads a third

region was usually the last to revascularise. remained alive following fracture and twoappeared bone but
cause with

partly or completely heads which were there

the

necrotic. partly necrotic of the

This teres.

capable by vessels
the

of uniting from absence

completely

and across of
necrotic

completely the fracture

femoral

being
ligamentum

invasion in this

necrotic
contrasted

heads
7.

described teres
Avascular

elsewhere vessels
necrosis did

issue
to

which
be the

united completely
sole

in the
of

proliferation collapse.

of

ligamenturn

failed
not

to revascularise
appear

and developed
non-union.

late segmental

8. Necrotic bone showed no alteration revascularisation sometimes caused associated with halted revascularisation.
of

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 trabeculae. Marrow calcification

was

deposition minimal.

of new

on

dead

bone

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

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 grateful

contour
thanks

of the
are due

articular
to the

cartilage
orthopaedic

were
surgeons

retained.
of the Western
Infirmary

and

Southern

General

Hospital,

Glasgow,

for their interest

and for access to their records;

to the medical

staff of the Glasgow

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 for the NO.

Barnes

and Mr J. T. Brown

for their help, encouragement

specimens. Research

and constructive
of this of Health

criticism

and to
borne by

many of the early Advisory Committee

arthroplasty on Medical

Part of the expenses of the Department

study were for Scotland.

47 B,

4,

NOVEMBER

1965

774

MARY

CATTO

REFERENCES G. P. (1958): Modern Journal, 34, 541. ARDEN, G. P., and VEALL,
ARDEN,

Trends
N. (1953):

in the Treatment

of the Fractured

Neck

of Femur. in Early
of the

Postgraduate

Medical

Necrosis (Section

in the

Femoral

Head

in Fractured

The Use of Radioactive Neck of Femur.

Phosphorus
Proceedings

Detection
Royal Society

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 and Joint Surgery, 42-B, 626. BONFIGLIO, M. (1954): Aseptic Necrosis of the Femoral Head in Dogs : Effect of Drilling and Bone Grafting. Surgery, Gynecology and Obstetrics, 98, 591. BONFIGLIO, M., and BARDENSTEIN, M. B. (1958): Treatment by Bone-Grafting of Aseptic Necrosis of the Femoral Head and Non-union of the Femoral Neck (Phemister Technique). Journal of Bone and Joint Surgery, 40-A, 1329. BOYD, H. B. (1957): Avascular Necrosis of the Head of the Femur. Instructional Course Lectures, American Academy of Orthopaedic Surgeons, 14, 196. BOYD, H. B., and CALANDRUCCIO, R. A. (1963): Further Observations on the Use of Radioactive Phosphorus (P32) to Determine the Viability of the Head of the Femur; Correlation of Clinical and Experimental Data in 130 Patients with Fractures of the Femoral Neck. Journal of Bone and Joint Surgery, 45-A, 445. BOYD, H. B., ZILVERSMIT, D. B., and CALANDRUCCIO, R. A. (1955): The Use of Radio-active Phosphorus (P32) to Determine the Viability of the Head of the Femur. Journal of Bone and Joint Surgery, 37-A, 260. BRINDLEY, H. H. (1963): Avascular Necrosis of the Head of the Femur. An Experimental Study. Proceedings of the American Academy of Orthopaedic Surgeons in Journal of Bone and Joint Surgery, 45-A, 1541. BROWN, J. T., and ABRAMI, G. (1964) : Transcervical Femoral Fracture. Journal of Bone and Joint Surgery, 46-B, 648. BROWN, J. T., and CATrO, M. (1964): Unpublished work. CAMPBELL, C. J. (1961) : Aseptic Necrosis of Bone. Instructional Course Lectures, America,z Academy of Orthopaedic Surgeons, 18, 234. CAucHoIx, J., and REY, J. C. (1963): Sur le traitement des fractures r#{233}centes du cot du femur. (Une s#{233}rie de 203 ens cons#{233}cutifs.) Revue de Chirurgie Orthop#{233}dique, 49, 315. CAVE, E. F. (1960): Fractures of the Femoral Neck. Instructional Course Lectures, America,: Academy of Orthopaedic Surgeons, 17, 79. CHANDLER, S. B., and KREUSCHER, P. H. (1932): A Study ofthe Blood Supply ofthe Ligamentum Teres and its Relation to the Circulation of the Head of the Femur. Journal of Bone and Joint Surgery, 14, 834. CFIARNLEY, J., BLOCKEY, N. J., and PURSER, D. W. (1957): The Treatment of Displaced Fractures of the Neck
of Orthopaedics),

of the Femur
CHEYNEL,

by Compression.
: Introduction

Journal

ofBone

and

Joint de

Surgery, Ia Hanche.

39-B,

45.
Anatomiques Personelle.

J. (1954)

la Pratique

Chirurgicale

Recherches

Paris: G. Doin et cie. CHRISTOPHE, K., HOWARD, L. 0., POrrER, T. A., and DRISCOLL, A. J. (1953): A Study ofOne Hundred and Four Consecutive Cases of Fracture of the Hip. Journal ofBone and Joint Surgery, 35-A, 729. CLAFFEY, T. J. (1960): Avascular Necrosis of the Femorat Head. An Anatomical Study. Journal ofBone and Joint Surgery, 42-B, 802. CLEVELAND, M., and FIEt..rnNG, J. W. (1954): A Continuing End-Result Study of Intracapsular Fracture of the Neck of the Femur. Journal ofBone and Joint Surgery, 36-A, 1020. COLEMAN, S. S., and COMPERE, C. L. (1961): Femoral Neck Fractures : Pathogenesis of Avascular Necrosis, Nonunion and Late Degenerative Changes. Clinical Orthopaedics, 20, 247. COMPERE, E. L., and WALLACE, G. (1942): Etiology of Aseptic Necrosis of the Femur after Transcervical Fracture. Journal of Bone and Joint Surgery, 24, 831. CRAWFORD, H. B. (1960): Conservative Treatment of Impacted Fractures of the Femoral Neck. A Report of Fifty Cases. Journal ofBone and Joint Surgery, 42-A, 471. DAHLGREN, S. (1959): Venography in Fractures of the Femoral Neck. Acta Chfrurgica Scandinavica, 117, 494.
Deductions Chirurgicales Pratiques.
THE

JOURNAL

OF BONE

AND

JOINT

SURGERY

A HISTOLOGICAL DE
HAAS,

STUDY I. (1956):

OF AVASCULAR Fractures of the Neck

NECROSIS

OF THE FEMORAL

HEAD

775

W., and S. M.,

andJoint

MACNAB,

of the Femoral
ELMORE,

Head.
Surgery,

South

African

MedicalJournal,

MALMGREN,

Bone
GARDEN,

R. S. (1961): 43-B, 647. GREEN, J. T. (1960): Management

American
HAM,

R. A., and SOKOLOFF, 45-A, 318. Low-Angle Fixation in Fractures

of the Femur; a Method ofAssessing the Viability 30, 1005. L. (1963): Sclerosis of Synovial Blood Vessels. Journal of of the Femoral Neck.
Journal ofBone andJoint Course Surgery, Lectures,

of Fresh

Fractures

of the Neck

of the Femur.

instructional

Academy

of Orthopaedic

Surgeons,

A. W., and LEESON, T. S. (1961): Histology. edition, p. 329. London: Pitman Medical Publishing Co. Ltd. HARGADON, E. J., and PEARSON, J. R. (1963): Treatment of Intracapsular Fractures of the Femoral Neck with the Charnley Compression Screw. Journal ofBone and Joint Surgery, 45-B, 305. HARRISON, M. H. M. (1962): A Preliminary Report of Vascular Assay in Prognosis of the Fractured Femoral Neck. Journal ofBone and Joint Surgery, 44-B, 858. HARTY, M. (1953): Blood-Supply of the Femoral Head. British Medical Journal, ii, 1236. HATCHER, C. H. (1952): The Role of Aseptic Necrosis of Bone in Skeletal Disease and Injuries. Chapter 16. In The Musculoskeletal System. Edited by M. Ashford. New York : MacMillan. HODGES, P. C. (1954): Normal Bone, Diseased Bone, Dead Bone. American Journal of Roentgenology, 71, 925. HULTH, A. (1958a): Femoral-Head Phlebography: a Method of Predicting Viability. Journal ofBone and Joint Surgery, 40-A, 844. HULTH, A. (1958b): The Vessel Anatomy of the Upper Femur End with Special Regard to the Mechanism of Origin of Different Vascular Disorders. Acta Orthopaedica Scandinavica, 27, 192. HULTH, A. (1961): Necrosis ofthe Head ofthe Femur. A Roentgenological, Microradiographic and Histological Study. Acta Chirurgica Scandinavica, 122, 75. JAFFE, H. L., and POMERANZ, M. M. (1934): Changes in the Bones of Extremities Amputated Because of Arteriovascular Disease. Archives of Surgery, 29, 566.
JOHANSSON, Acta
JUDET,

17, 94. Fourth

S. H. Chirurgica

(1962):

Prognostic

Assessment

in Fractured

Neck

of Femur

Using

131

I and

Venography.

Scandinavica,

J., JUDET, R., LAGRANGE, J. (1955): A Study of the Arterial Vascularisation of the Femoral Neck in the Adult. Journal ofBone and Joint Surgery, 37-A, 663. JUDET, R., JUDET, J., and ROY-CAMILLE, R. (1958) : La vascularisation des pseudarthroses des os longs dapr#{232}s une #{233}tude clinique et exp#{233}rimentale. Revue de Chirurgie Orthop#{233}dique, 44, 381. KOLODNY, A. (1925): The Architecture and the Bloodsupply of the Head and Neck of the Femur and their Importance in the Pathology of Fractures of the Neck. Journal of Bone and Joint Surgery, 7, 575. LAING, P. G., and FERGUSON, A. B., Jun. (1959): Radiosodium Clearance Rates as Indicators of Femoral-Head Vascularity. Journal of Bone and Joint Surgery, 41-A, 1409. LENDRUM, A. C., FRASER, D. S., SLIDDERS, W., and HENDERSON, R. (1962): Studies on the Character and Staining of Fibrin. Journal of Clinical Pathology, 15, 401. LINTON, P. (1944) : On the Different Types of Intracapsular Fractures of the Femoral Neck. Acta Chirurgica Scandinavica, Supplementum 86. MCGINNIS, A. E., LomS, J. 0., and REYNOLDS, F. C. (1958): Femoral Arteriograms; use to Demonstrate Circulation of the Hip Following Neck Fractures of the Femur. Missouri Medicine, 55, 31. MCLEAN, F. C., and URIST, M. R. (1955): Bone. An Introduction to the Physiology ofSkeletal Tissue. Chicago:

123, 298. J., and DUNOYER,

University
MATHON,

of Chicago

Press.

J. F. (1959): Practicien, 9, 795.

DAUBIGNE,

Etude R.,
Revue

de larchitecture
CORMIER

et de Ia vascularisation N#{233}crose traumatique 42, 246. of Osteoid Tissue.

du col et de Ia t#{234}te du femur. de Ia t#{234}te du femur en

Revue

du

MERLE

and
de

(1956):

dehors

des

pseudarthroses.
MEYER,

Chirurgie

Orthop#{233}dique,

P. C. (1956): The Histological Identification Journal ofPathology and Bacteriology, 71, 325. NICOLL, E. A. (1963): The Unsolved Fracture. Journal ofBone and Joint Surgery, 45-B, 239. NORDENSON, N. G. (1938): Sur Ia vascularisation de Ia t#{234}te du femur par Ia voie du ligament rond f#{233}moral. Lyon Chirurgical, 35, 178. PALMER, I. (1934): (Jber die Ausheilungsbedingungen der medialen SchenkelhalsbrUche nach Osteosynthese mit einem Nagel aus rostfreiem Stahl, illustriert durch eine histologische Untersuchung. Acta Chfrurgica Scandinavica, 75, 416. PATRICK, J. (1960): Avascular Necrosis and the Head of the Femur. Proceedings of the British Orthopaedic Association in Journal of Bone and Joint Surgery, 42-B, 650. PHEMISTER, D. B. (1930): Repair of Bone in the Presence of Aseptic Necrosis Resulting from Fractures, Transplantations and Vascular Obstruction. Journal of Bone and Joint Surgery, 12, 769.
VOL.

47 B, NO. 4,

NOVEMBER

1965

776
PHEMISTER, D.

MARY B. (1934) : Fractures of Neck of Femur,

CATFO Dislocations
Surgery,

of Hip,
Gynecology

and
and

Obscure
Obstetrics,

Producing
PHEMISTER,

Aseptic

Necrosis

of Head

of Femur.

D. B. (1939): The Pathology of Ununited Fractures ofthe Neck ofthe Femur to the Head. Journal ofBone and Joint Surgery, 21, 681. PHEMISTER, D. B. (1940): Changes in Bones and Joints Resulting from Interruption of Circulation. I. General Considerations and Changes Resulting from Injuries. Archives ofSurgery, 41, 436. PHEMISTER, D. B. (1943): Circulatory Disturbances in the Head of the Femur. American Academy of Orthopaedic Surgeons Lectures, 1, 129. PHEMISTER, D. B. (1948): Lesions of Bones and Joints Arising from Interruption of the Circulation. Journal of the Mount Sinai Hospital, 15, 55. PHEMISTER, D. B. (1949a): Treatment of the Necrotic Head of the Femur in Adults. Journal ofBone and Joint Surgery, 31-A, 55. PHEMISTER, D. B. (1949b) : In discussion on paper by PATRICK, J. Intracapsular Fractures of the Femur Treated with a Combined Smith-Petersen Nail and Fibutar Graft. Journal of Bone and Joint Surgery, 31-A, 67. PRICE, E. R. (1962): The Viability of the Femoral Head after Fracture of the Neck of the Femur: a Preliminary Communication on a Dye Clearance Technique. Journal of Bone and Joint Surgery, 44-B, 854. RooK, F. W. (1953): Arteriography of the Hip Joint for Predicting End Results in Intracapsular and Intertrochanteric Fractures of the Femur. American Journal of Surgery, 86, 404. RUSSELL, N. L. (1956): A Rapid Double-embedding Method for Tissues Using an Automatic Tissue Processing Apparatus (Histokinette-Histokine). Journal of Medical Laboratory Technology, 13, 484. RUTISHAUSER, E., and MAJNO, G. (1951): Physiopathology of Bone Tissue. Bulletin of the Hospital for Joi,zt Diseases, 12, 468. SANT05, J. V. (1930): Changes in the Head of the Femur After Complete Intracapsular Fracture of the Neck. Archives ofSurgery, 21, 470. SCHMORL, G. (1924): Die pathologische Anatomie der Schenkethalsfrakturen. M#{252}nchener Medizinische Wochenschrift, 71, 1381. SEVITT, S. (1964): Avascular Necrosis and Revascularisation ofthe Femoral Head after Intracapsular Fractures. Journal ofBone and Joint Surgery, 46-B, 270. SHERMAN, Mary S. (1947): In discussion on paper by BoYD, H. B., and GEORGE, I. L. Complications of Fractures of the Neck of the Femur. Journal ofBone and Joint Surgery, 29, 327. SHERMAN, Mary S., and PHEMISTER, D. B. (1947): The Pathology of Ununited Fractures of the Neck of the Femur. Journal of Bone and Joint Surgery, 29, 19. SHERMAN, Mary S., and SELAKOVICH, W. G. (1957): Bone Changes in Chronic Circulatory Insufficiency. Journal ofBone and Joint Surgery, 39-A, 892. SMITH, F. B. (1959): Effects of Rotatory and Valgus Malpositions on Blood Supply to the Femoral Head: Observations at Arthroplasty. Journal ofBone andJoint Surgery, 41-A, 800. TOVEE, E. B., and GENDRON, E. (1954): The Use of Radioactive Phosphorus in the Determination of the Viability of the Femoral Head in Dogs after Subcapitat Fractures. Journal of Bone and Joint Surgery,
36-A,
TRUETA,

Vascular Disturbances 59, 415. with Special Reference

185.

J., and
Journal

HARRISON,

M. H. M. (1953):
and Joint Surgery,

Man.
TUCKER,

of Bone

Joint
TUCKER,

F. R. (1949): Arterial Supply Surgery, 31-B, 82. F. R. (1950): The Use of Radioactive

The Normal Vascular Anatomy of the Femoral Head in Adult 35-B, 442. to the Femoral Head and its Clinical Importance. Journal of Bone and Phosphorus in the Diagnosis of Avascular 32-B, 100. Commentary on the Campaign for the Establishment
Joint Surgery,

Necrosis of the
Surgery,

of the Positive 27, 334. Neck : an

Femoral
WHITMAN,

Head.
R. (1945):

Journal

of Bone

and

A Retrospective

Standard

of Treatment

for Fracture

of the Neck of the Femur.

77,

Journal

ofBone

and

Joint

WoLCorr, W. E. (1943): The Evolution of the Circulation Anatomic Study. Surgery, Gynecology and Obstetrics, WOODHOUSE, C. F. (1962a): Anoxia of the Femoral Head. WOODHOUSE, C. F. (196Th): Tetracycline Vascular Maps
Research Society in Journal of Bone and Joint Surgery,

in the 61.

Developing
52, 55.

Femoral

Head

and

Surgery,

of the 44-A,

Femoral 1029.

Head.

Proceedings

of

Orthopaedic

THE

JOURNAL

OF

BONE

AND

JOINT

SURGERY