The arterial supply of the navicular bone in adult horses with navicular disease


Rijkenhuizen, A.B.M.; Nemeth, F.; Dik, K.J.; Goedegebuure, S.A.

Equine Veterinary Journal 21(6): 418-424

1989


A macroscopical, arteriographical and histological study was made of the arterial supply of the navicular bones of horses with clinical and/or radiograhic signs of navicular disease. Based on the clinical and radiological findings the navicular bones of 40 Warmblood horses are divided into four different groups. In the pattern of the arteriogram obvious changes are noticed: an imbalance and a distal to proximal shift between the distal and proximal arterial supply occur, indicating a reduction of the distal blood supply with a compensatory reaction of the proximal, medial and lateral supply. The changes in the pattern of the arteriogram are histologically defined by arterio(lo) sclerosis and newly formed arteries. The presence of radiologically visible nutrient foramina is associated with a changed pattern in the arteriogram, increased bone remodelling and fibrosis. Ischaemia and increased pressure (hypertension and/or increased intra-articular pressure) are considered to be responsible for chnges in form and number of radiologically visible nutrient foramina.

418
EQUINE
VETERINARY
JOURNAL
Equine
vet.
J.
(1989)
21
(6)
418-424
The
arterial
supply
of
the
navicular
bone
in
adult
horses
with
navicular
disease
ASTRID
B.
M.
RIJKENHUIZEN,
F.
NEMETH,
K.
J.
DIK*,
and
S.
A.
GOEDEGEBUUREt
Department
of
General
and
Large
Animal
Surgery,
Department
of
Radiology*
and
Department
of
Pathologyt,
Veterinary
Faculty,
University
of
Utrecht,
Yalelaan
12,
de
Uithof-3508
TD
Utrecht,
The
Netherlands.
Summary
A
macroscopical,
arteriographical
and
histological
study
was
made
of
the
arterial
supply
of
the
navicular
bones
of
horses
with
clinical
and/or
radiographic
signs
of
navicular
disease.
Based
on
the
clinical
and
radiological
findings
the
navicular
bones
of
40
Warmblood
horses
are
divided
into
four
different
groups.
In
the
pattern
of
the
arteriogram
obvious
changes
are
noticed:
an
imbalance
and
a
distal
to
proximal
shift
between
the
distal
and
proximal
arterial
supply
occur,
indicating
a
reduction
of
the
distal
blood
supply
with
a
compensatory
reaction
of
the
proximal,
medial
and
lateral
supply.
The
changes
in
the
pattern
of
the
arteriogram
are
histologically
defined
by
arterio(lo)
sclerosis
and
newly
formed
arteries.
The
presence
of
radiologically
visible
nutrient
foramina
is
associated
with
a
changed
pattern
in
the
arteriogram,
increased
bone
remodelling
and
fibrosis.
Ischaemia
and
increased
pressure
(hypertension
and/or
increased
intra-articular
pressure)
are
considered
to
be
responsible
for
changes
in
form
and
number
of
radiologically
visible
nutrient
foramina.
Introduction
CIRCULATORY
disturbances
resulting
in
ischaemic
conditions
are
considered
one
of
the
possible
causes
of
navicular
disease
(Walley
1885;
Hickman
1964;
Nemeth
1971).
Various
causes
of
ischaemia
of
the
navicular
bone
have
been
reported;
total
or
partial
occlusion
of
the
main
digital
arteries
as
a
result
of
subintimal
or
intimal
proliferation
(Kohler
1951;
Bibrack
1963
and
Fricker,
Riek
and
Hugelshofer
1982),
arterial
obstruction
associated
with
arteriosclerosis
(Nemeth
1971)
or
thrombosis
(Colles
and
Hickman
1977)
in
the
arteries
of
the
navicular
bone
and
venous
congestion
resulting
in
a
raised
blood
pressure
(Svalastoga
and
Smith
1983;
Colles
1983).
The
arterial
supply
of
the
navicular
bone
of
normal
adult
horses
has
a
uniform
specific
pattern
characterised
by
four
to
eight
arteries
entering
distally
covering
the
central
and
distal
part
of
the
navicular
bone
and
nine
to
14
proximal
arteries
covering
the
proximal
part
of
the
bone,
whereas
the
medial
and
lateral
parts
receive
their
arterial
supply
from
the
arteries
entering
medially
and
laterally
(Colles
et
al
1977;
Rijkenhuizen,
Nemeth,
Dik
and
Goedegebuure
1989a).
Hertsch
and
Dammer
(1987)
describe
changes
in
the
pattern
of
the
arteriogram
of
navicular
bones
of
horses
with
navicular
disease,
corresponding
to
plain
radiological
and
pathomorphological
changes.
Also,
a
recent
study
of
the
arterial
supply
of
young
horses
demonstrates
a
direct
correlation
between
the
arterial
supply
(ie
number
of
arteries
entering
the
navicular
bone
proximally
and
distally,
the
diameter
of
the
arterial
lumen
and
arterial
wall
changes)
and
the
radiographic
changes
in
the
bone,
particularly
the
nutrient
foramina
(Rijkenhuizen,
Nemeth,
Dik
and
Goedegebuure
1989b).
The
purpose
of
this
study
was
to
evaluate
the
arterial
supply
in
the
navicular
bone
of
horses
with
clinical
and/or
radiographic
findings
of
the
navicular
disease.
This
may
help
to
elucidate
the
role
of
the
vascular
system
in
the
pathogenesis
of
navicular
disease.
Materials
and
methods
The
navicular
bones
of
one
or
both
forelimbs
of
40
Warmblood
horses
were
examined.
Eleven
horses
(Group
A)
had
no
history
or
clinical
evidence
of
lameness
related
to
navicular
disease
and
were
destroyed
for
reasons
unrelated
to
forelimb
lameness
(colic:
2;
fracture:
3;
wound:
6).
Twenty-nine
horses
(Group
B,
C,
and
D)
were
lame
from
navicular
disease.
Before
signs
of
lameness
occurred
these
horses
were
trained
for
dressage
or
show
jumping.
The
clinical
criteria
used
in
the
diagnosis
of
navicular
disease
were:
History
of
unilateral
or
bilateral
chronic
(two
months
to
three
years)
forelimb
lameness,
usually
intermittent
and
of
gradual
incidence.
Shortening
of
the
supporting
phase
of
the
stride.
Pain
response
to
percussion
of
the
hoof
at
the
centre
third
of
the
frog.
Pain
response
to
hyperflexion
of
the
phalanges
and
an
increase
in
lameness
following
flexion
of
the
phalanges
for
1
min.
Nerve
block
of
the
N.
digitalis
palmaris
medialis
and
lateralis
eliminated
lameness
on
that
foot.
Following
clinical
examination,
radiographs
of
the
navicular
area
were
made
in
dorsopalmar
and
lateromedial
projection
using
the
upright
pedal
route.
Based
on
clinical
and
radiographic
findings
the
material
was
divided
in
four
different
groups
(Dik,
Nemeth
and
Merkens
1978):
Group
A:
No
lameness
or
history
due
to
navicular
disease.
Radiographs
showed
three
or
more
nutrient
foramina
of
moderate
length,
penetrating
the
navicular
bone
distally,
not
passing
beyond
one
third
of
the
distance
between
the
distal
and
proximal
border
of
the
navicular
bone;
and/or
one
to
two
long
nutrient
foramina
passing
beyond
one
third
of
the
distance
between
the
distal
and
proximal
border.
Occasionally
exostoses
along
the
proximal
border
of
the
navicular
bone
were
also
present.
Group
B:
Clinical
evidence
of
navicular
disease
combined
with
the
same
radiological
classification
as
Group
A.
Group
C:
Clinical
evidence
of
navicular
disease.
Radiographs
showing
three
or
more
nutrient
foramina
penetrating
deeply
into
the
navicular
bone,
ie
passing
beyond
one
third
of
the
distance
between
the
distal
and
proximal
border
of
the
navicular
bone.
The
nutrient
foramen
could
have
a
mushroom-like
shape.
In
addition
spur
formation
and
exostoses
along
the
proximal
border
of
the
EQUINE
VETERINARY
JOURNAL
419
TABLE
1:
Details
of
the
warmblood
horses
examined
(see
materials
and
methods)
Group
No.
of
horses
No.
of
navicular
bones
Lameness
++
A
11
22
0 0
B
14
25
12
2
C
13
18
8
5
D
9
12
5
4
Age
(years)
3-
9
(x
6.6)
3-12
(x
8.6)
6-20
(Z
10.6)
6-20
(i
10.8)
Number
of
navicular
bones
investigated
Radiograph
Histological
sections
Undec
DP/LM
Dec
DP/LM
Transverse
Sagittal
Total
Total
Slabs
22 22
2
15
1
25
25
2
18
6
18
18
2
14
5
12
12
4
12
6
+:
slight;
++:
severe;
Undec:
undecalcified;
Dec:
decalcified;
DP:
dorsopalmar
projection;
LM:
lateromedial
projection
TABLE
2:
The
percentage
of
horses
in
each
group
aged
3-6,
7-
Table
3:
The
percentage
of
lesions
on
the
flexor
surface
(FS)
9
and
over
10
years
and
deep
digital
flexor
tendon
(DFT)
in
each
group
Group
Group
A
Group
B
Group
C
Group
D
Age
A
B
C
D
FS
DFT
FS
DFT
FS
DFT
FS
DFT
3-6
years
54
50
8
22
1
39
82
13
65
0
12
0 0
7-9
years
45
29
31
22
2
18
9
26
0
12
24
0
0
?.10
years
0
21
61
56
3
22
9
26
35
19
35
0
0
4
31
0
35
0
69
29
14
14
5
0
0
0 0
0
0
86
86
navicular
bone
were
found
occasionally.
Group
D:
Clinical
evidence
of
navicular
disease,
the
radiographs
not
only
showing
many
long
nutrient
foramina
and
mushroom-
shaped
nutrient
foramina
but
also
cavitations
in
the
centre
or
centrodistally
in
the
navicular
bone.
The
material
is
summarised
in
Table
1
and
2.
The
navicular
bones
from
seven
of
the
40
horses
were
distributed
over
different
groups,
explaining
the
discrepancy
in
total
number
of
horses
in
Table
I.
The
arterial
supply
of
the
navicular
bones
was
studied
after
euthanasia,
using
the
arteriographical
and
histological
methods
described by
Rijkenhuizen
et
al
(1989a).
Before
the
navicular
bones
were
fixed
in
neutral
buffered
formalin
(4
per
cent),
the
dissected
navicular
bones
and
the
dorsal
surface
of
the
tendon
of
the
Musculus
flexor
digitorum
profundum
(deep
digital
flexor
tendon)
were
examined
macroscopically
and
a
dorsopalmar
radiograph
of
the
navicular
bone
was
made.
After
decalcification,
using
a
solution
(1:1)
of
formic
acid
(35
per
cent)
and
sodium
formate
(6.8
per
cent),
dorsopalmar
radiographs
were
made.
Ten
decalcified
navicular
bones
(Table
1)
were
sectioned
sagittally
into
five
to
seven
slabs,
approximately
8
mm
thick,
each
of
which
was
radiographed
in
dorsopahnar
and
lateromedial
projection
to
evaluate
the
course
of
the
arteries
in
dorsopalmar
direction.
After
paraffin
embedding,
transverse
sections
(6µ)
for
histological
examination
were
made
at
4
levels:
a.
just
distal
of
the
navicular
bone
in
the
ligamentum
sesamoideum
distale
impar
(distal
sesamoid
impar
ligament),
b.
just
proximal
of
the
distal
articular
surface,
c.
in
the
middle
of
the
navicular
bone
and
d.
proximal
in
the
navicular
bone.
Sagittal
histological
sections
were
cut
laterally
or
medially
of
the
centre
of
the
navicular
bone.
The
sections
were
stained
with
haematoxylin
and
eosin
(H&E),
phosphotungstic
acid-haematoxylin
(PAS),
Azan
and
von
Gieson-elastica
(Bancroft
and
Stevens
1982).
The
diameter
of
the
arteries
(including
the
arterial
lumen
and
wall)
was
measured
using
an
ocular
micrometer.
Results
Macroscopic
examination
The
articular
cartilage
of
all
navicular
bones
was
smooth,
glistening
with
a
bluish-white
colour.
On
average
80
per
cent
(Group
A:
62
per
cent,
B:
69
per
cent;
C:
94
per
cent
and
D:
100
per
cent)
of
the
navicular
bones
showed
a
degree
of
ecchondrosis
on
the
proximal
1:
FS
and
DFT
normal;
2:
FS
thinning,
DFT
impression;
3:
FS
thinning
and
yellow
discolouration,
DFT
yellow
discolouration;
4:
FS
thinning,
yellow
discolouration
and
roughening,
DFT
frayed;
5:
FS
and
DFT
adhesion
border
of
the
articular
cartilage.
The
extent
of
this
varied
from
minimal
to
severe,
with
a
slight
increase
in
extension
from
Group
A
to
B
and
a
more
pronounced
increase
from
Group
B
to
D.
The
distal
articular
surface
was
broad
and
the
palmar
aspect
was
straight.
The
distance
of
the
palmar
aspect
of
the
distal
articular
border
to
the
distal
sesamoid
impar
ligament
varied
from
1
to
3
mm,
which
is
a
normal
variability.
A
summary
of
the
lesions
per
group
found
in
the
fibrocartilage
of
the
flexor
surface
of
the
navicular
bone
is
given
in
Table
3.
The
macroscopic
lesions
of
the
flexor
surface
were
successively
characterised:
thinning,
thinning
and
yellow
discolouration
with
and
without
roughening
and
additional
adhesion
with
the
deep
digital
flexor
tendon.
The
macroscopic
lesions
were
localised
centrally
and
centrodistally
to
the
central
ridge
of
the
navicular
bone
and
ran
vertically
along
the centre
of
the
ridge.
The
size
of
the
lesions
varied
from
2
by
2
mm
to
a
lesion
running
over
almost
the
entire
surface
of
the
navicular
bone.
The
adhesions
of
the
deep
digital
flexor
tendon
occurred
centrally
or
centrodistally
to
the
ridge.
A
positive
correlation
(P<0.001,
Kruskal-Wallis)
was
found
between
the
severity
and
extension
of
the
macroscopic
lesion
of
the
fibrocartilage
and
the
classification
from
Group
A
to
D.
A
summary
of
the
macroscopic
lesions
on
the
dorsal
surface
of
the
deep
digital
flexor
tendon
in
each
group
is
given
in
Table
3.
The
macroscopic
lesions
on
the
dorsal
surface
of
the
deep
digital
flexor
tendon
were
successively
characterised:
impression,
discolouration,
fraying
and
adhesions
to
the
flexor
surface.
The
macroscopic
lesions
were
localised
opposite
the
lesions
of
the
fibrocartilage
of
the
navicular
bone;
the
early
lesions
of
the
tendon
surface
occurring
medially
and
laterally
to
the
ridge
of
the
navicular
bone
and
not
exactly
opposite
this
ridge.
In
more
advanced
cases
the
lesions
also
occurred
directly
opposite
the
ridge.
They
varied
in
size
from
very
small,
at
the
medial
or
lateral
part,
to
the
entire
surface
of
the
deep
digital
flexor
tendon.
Although
a
positive
correlation
was
found
between
the
severity
of
the
macroscopic
lesions
on
the
fibrocartilage
of
the
navicular
bone
and
the
lesions
on
the
surface
of
the
deep
digital
flexor
tendon,
the
deep
digital
flexor
tendon
could
be
normal
despite
the
presence
of
lesions
within
the
fibrocartilage
of
the
navicular
bone.
The
synovial
membrane
on
the
dorsal
aspect
of
the
distal
sesamoid
impar
ligament
in
the
distal
interphalangeal
joint
showed
a
progressive
increase
in
foldings,
villi
and
redness
from
Group
A
and
B
to
D.
Similar
changes,
but
to
a
lesser
degree,
were
observed
in
the
synovial
membrane
of
the
bursa
podotrochlearis.
Arteriographic
examination
The
blood
supply
of
the
navicular
bone
was
derived
from
the
A.
digitalis
tnedialis
W
and
lateralis
(medial
and
lateral
palmar
digital
arteries).
Eighteen
to
20
per
cent
of
the
medial
palmar
digital
arteries
in
every
group
showed
a
locally
narrowed
lumen
over
1
to
4
cm
at
the
height
of
the
proximal
phalanx
or
pastern
joint.
Only
one
medial
palmar
digital
artery
in
Group
D
was
substituted
by
a
narrow
tortuous
collateral
over
the
entire
length
of
the
proximal
phalanx.
No
differences
concerning
the
course
and
the
number
of
branching
arteries
of
the
Ramus
navicularis
distalis
(r.nay.),
the
Ramus
palmaris
phalangis
mediae
(r.palm.)
and
the
Rami
navicularis
mediales
and
laterales
were
found
compared
with
the
normal
adult
horse
(Rijkenhuizen
et
al
1989a).
The
r.
nay.
usually
formed
a
straight
linear
connection
between
the
medial
and
the
lateral
palmar
digital
artery;
occasionally
narrowing
in
the
centre.
In
a
few
cases
the
r.
nav,
bifurcated
and
then
joined
again,
forming
a
diamond
shaped
loop
in
the
centre.
Changes
in
the
pattern
of
the
arteriogram
within
the
navicular
bone
are
summarised
in
Table
4
and
5
and
schematically
depicted
in
Fig
1.
The
following
changes
were
observed:
a.
A
decrease
in
number,
length
and
lumen
of
the
arteries
entering
Table
4:
Changes
occurring
in
the
arteriogram
and
histological
sections
in
each
group
Findings
Group
A
Number
of
arteries
4-7
(x5.5)
entering
distally
Number
of
arteries
9-15
entering
proximally
%
Navicular
bones
50%
with
proximal
arteries
running
beyond
20%
of
distance
between
distal
and
proximal
border
Number
of
arteries
inside
the
nutrient
foramen
arteries
0.13
mm
0.9
arteries
..?.0.04
mm
1.8
Histological
diameter
of
arteries
entering
distally
arteries
X:1.13
mm
0.18
mm
arteries
>_0.04
mm
0.15
mm
nutrient
foramina
2.3
mm
synovial
introversion
0.24
mm
Group
B
Group
C
Group
D
3-8
(x5.3)
1-6
(x5.3)
0-8
(x4.0)
9-15
9-15
9-15
54%
72%
92%
0.8 0.8
1.3
1.7
1.7
2.0
0.20
mm
0.21
mm
0.23
mm
0.15
mm
0.15
mm
0.18
mm
2.6
mm
2.8
mm
2.9
mm
0.24
mm
0.24
mm
0.26
mm
TABLE
5:
Schematic
view
of
the
changes
in
the
arteriogram
In
each
group
Group
A
B
CD
equal
division
of
the
arteries
distal
narrowed
and/or
shortened
arteries
proximal
widened
and
extended
arteries
extension
proximal
arteries
is
equal
to
the
distal
arteries
extension
proximal
arteries
deeper
as
the
distal
arteries
direct
connection
nutrient
foramina
without
distal
arteries
Frequency
of
occurrence
ranging
from
-(absent),
+/-,
+,
++
to
+++
+
+
++
++
+ +
++
++
+/-
+/-
+
+
+
++
+
+
++
+
+
++
+
++
420
EQUINE
VETERINARY
JOURNAL
distally,
particularly
at
the
centre
of
the
navicular
bone
and
also
to
a
lesser
degree
at
the
periphery.
b.
An
increase
in
length
and
lumen
of
arteries
entering
distally
situated
next
to
the
narrowed
and
shortened
arteries.
In
addition,
these
arteries
gave
off
branches
or
tended
to
bow
towards
the
area
which
normally
receives
its
arterial
supply
from
the
narrowed
or
absent
arteries.
c.
An
increase
in
length
and
lumen
of
arteries
entering
proximally
opposite
to
the
area
without
any
or
narrowed,
shortened
arteries
entering
distally
(Fig
2).
The
widened
proximal
arteries
ran
into
the
navicular
bone
beyond
the
usual
level
of
20
per
cent
of
the
distance
between
the
proximal
and
distal
navicular
border.
d.
An
increase
in
lumen
of
the
arteries
entering
medially
and
laterally
as
well
as
the
extent
of
running
into
the
navicular
bone.
e.
Formation
of
a
'direct'
connection
instead
of
the
normal
small
and
narrow
anastomoses
between
the
extended
and
widened
main
a
a
111WILIP
o
rr
f
or
(14,
1
11140.141a.
AMLI
;
gramePtist"
\NVitiliktkike
gewgaw
/
4
i
g
Fig
1:
Diagram
of
the
arterial
anatomy
of
the
navicular
bone
in
dorsopalmar
and
lateromedial
-projection.
a:
Navicular
bone
of
the
'normal'
horse;
b:
Group
A;
c:
Group
B;
d:
Group
C;
e:
Group
D;
f:
Lateromedial
projection
of
a
'direct'
connection;
g:
Lateromedial
projection
of
the
arterial
anatomy
around
a
cyst;
1:
A.
digitalis;
2:
Ramus
palmaris
phalangis
mediae;
3:
Ramus
navicularis distalis;
4:
Rami
naviculares
mediales
and
laterales;
5:
Distal
arteries;
6:
Proximal
arteries;
7:
Distal
network;
8:
Proximal
network;
9:
Ligament
sesamoideum
distale
impar;
10:
Ligament
sesamoideum
collaterale;
11:
Bursa
podotrochleare
pedis;
12:
Musculus
flexor
digitorum
profundus;
13:
'Direct'
connection.
'normal
artery;
narrowed
and
shortened
artery;
!widened
and
extended
artery
t
1!
11.
A
c0.7
piP
1
I
i
t
r
EQUINE
VETERINARY
JOURNAL
421
Fig
2:
Arteriogram
of
the
decalcified
navicular
bone
(Group
C)
in
dorsopalmar
projection,
illustrating
the
arterial
anatomy
Fig
3:
Arteriogram
of
the
decalcified
navicular
bone
(Group
D)
in
lateromedial
projection.
The
arrow
points
towards
the
cyst
proximal
arteries
and
the
narrowed
main
distal
arteries.
f.
A
proximally
and
distally
widened
artery
always
runs
towards
radiolucent
cavitations,
giving
off
many
branches,
thus
forming
an
anastomotic
network
in
and
round
the
cystic
lesion
(Fig
3).
g.
An
increase
of
branching
arteries
occurred
from
Group
B-D
towards
the
centrodistal
and
centropalmar
aspect
of
the
navicular
bone.
In
Group
A
only
a
slight
change
in
number,
length
and
lumen
of
arteries
entering
the
navicular
bone
was
found
compared
to
normal
horses
(Rijkenhuizen
et
al
1989a).
In
Group
B
similar
changes
in
the
pattern
of
the
arteriogram
of
the
navicular
bone
were
noticed
together
with
occasional
'direct'
connections
between
the
proximal
and
the
distal
entering
arteries.
The
changes
in
the
pattern
of
the
arteriogram
distinctly
increased
from
Group
B
to
D.
Radiographically
visible
nutrient
foramina
of
moderate
length
or
deeply
penetrating
the
navicular
bone
distally,
generally
contained
extended
and
widened
distal
arteries,
but
narrowed
and
shortened
arteries
as
well
as
normal
arteries
were
also
found
in
these
foramina.
Proximal
nutrient
foramina
became
visible
radiographically
only
if
the
proximal
arteries
were
widened
and
ran
beyond
the
level
equivalent
to
20
per
cent
of
the
distance
between
the
distal
and
the
proximal
border.
Mushroom
shaped
nutrient
foramina
contained
narrowed,
shortened
distal
arteries
or
no
arteries
at
all.
Extended
and
widened
arteries
were
never
found
in
these
nutrient
foramina.
In
addition,
arteries
branching
off
arteries
entering
proximally,
medially
or
laterally
were
directed
towards
these
foramina.
The
imbalance
and
the
distal
to
proximal
shift
between
the
distal
and
proximal
arterial
supply
of
the
navicular
bone
is
demonstrated
in
Table
5.
In
Group
D,
in
particular,
most
or
all
distal
arteries
were
absent,
the
distal
arterial
supply
being
completely
dominated
by
the
proximally
entering
widened
and
deeply
penetrating
arteries.
Histological
examination
With
the
exception
of
enchondrosis,
no
clear
lesions
were
found
histologically
in
the
articular
hyalin
cartilage
of
the
navicular
bones
of
all
groups.
Nutrient
foramina
along
the
distal
border
of
the
navicular
bone
varied
in
length,
diameter
and
shape.
The
average
diameter
of
the
nutrient
foramina
just
proximal
of
the
distal
articular
border
is
summarised
in
Table
4.
The
opening
of
the
mushroom-shaped
nutrient
foramina
was
small,
whereas
more
proximally
the
diameter
increased
up
to
80
per
cent
of
the
distance
between
the
dorsal
and
palmar
border
of
the
navicular
bone.
Bone
tissue,
surrounding
the
nutrient
foramina,
became
increasingly
irregular
from
Group
A
and
B
to
D.
The
irregularity
was
the
consequence
of
remodelling
in
which
the
bone
resorption
predominated.
Howship's
lacunae
and
osteoclasts
were
found.
The
density
of
bone
tissue
surrounding
the
nutrient
foramen
increased
because
of
new
bone
apposition
which
is recognised
as
woven
bone.
The
remodelling
was
most
intense
around
the
mushroom-shaped
nutrient
foramina.
The
connective
tissue
in
the
centre
of
the
nutrient
foramen,
as
well
as
at
the
periphery,
became
more
fibrous
as
the
remodelling
was
more
intense.
Eighty
per
cent
of
the
nutrient
foramina
contained
synovial
tissue.
In
the
narrow
nutrient
foramina
the
synovial
introversion
did
not
reach
beyond
half
the
proximodistal
length
of
the
radiolucency.
In
wide
and
mushroom-shaped
nutrient
foramina
the
synovial
introversion
extended
more
deeply
than
in
the
narrow
nutrient
foramina
but
did
not
reach
into
the
proximal
end
of
the
nutrient
foramina.
The
diameter
of
the
synovial
lumen
bounded
by
the
synovial
membrane
in
the
distal
part
of
the
nutrient
foramen
is
summarised
in
Table
4.
More
proximally
this
lumen
was
enlarged
to
a
great
extent
in
the
widened
nutrient
foramina
and
even
more
so
in
the
mushroom-shaped
nutrient
foramina.
The
synovial
membrane,
introverted
into
the
nutrient
foramina,
showed
villous
hypertrophy,
which
increased
from
Group
A
and
B
to
D.
The
superficial
layer
was
hypertrophied
locally
over
a
greater
T.
1.,
-11
t4itt,.;
•••
q
IFF
kr
,
I.
1.•
.••
1191
,10
t:-
.;
4
111/
r•••••
4
'
t
.
422
EQUINE
VETERINARY
JOURNAL
\
,
•'`
,
,Ik
Ir
,t
74
.1
'
(
1
t
$
'
t
:
1
total
number
of
arteries
number
obliterated
arteries
%
arteries
changed
%
intima
changed
proliferation:
local
circ.
conn
circ.
musc
%
media
changed
hyalinisation
disruption/thinning
fibrosis/hyperplasia
Arrows
point
towards
changed
vessels
Fig
4:
Transverse
section
of
the
synovial
membrane
(H&E.
x100).
%
internal
elastic
membrane
changed
absent
splitting
local
2
layers
more
fragmentation
or
lesser
degree.
circ.
conn:
circular
thickening
with
staining
characteristics
of
Group
A
and
B
to
D
and
the
amount
of
vessel
sections
increased
connective
tissue;
circ.
musc:
circular
thickening
with
staining
greatly
(Fig
4).
These
vessels
were
small
(0.10
mm),
thick-walled
characteristics
of
muscular
fibres
and
had
a
small
lumen.
The
vessels
were
not
composed
of
muscular
fibres,
did
not
contain
elastic
fibres
and
had
a
narrow
lumen.
Obliterated
vessels
and
hyalin
vessel
walls
occurred
frequently.
Collagen
fibres
arranged
themselves
circularly
around
one
or
more
ifr"
vessels.
The
more
vessels
that
were
present,
the
more
fibrous
was
the
connective
tissue
in
the
synovial
membrane,
especially
close
to
the
bone.
No
increased
numbers
of
inflammatory
cells were
found
subsynovially
and
inside
the
nutrient
foramen.
The
percentage
of
arterial
wall
changes
of
the
main
arteries
inside
the
nutrient
foramina
with
a
diameter
greater
than
0.13
mm,
are
summarised
in
Table
6.
The
arterial
wall
changes
predominated
in
the
intimal
layer
and
were
classified
as
local
or
circular
intimal
thickening.
As
a
consequence,
the
thickening
produces
a
decrease
of
the
arterial
lumen.
The
staining
characteristics
of
the
cells
of
these
thickenings
resembled
those
of
connective
tissue
and,
occasionally,
muscle
cells.
The
intimal
thickening
was
associated
frequently
with
local
or
circular
splitting
in
two
or
more
layers,
fragmentation
or
absence
of
the
internal
elastic
membrane
(Fig
5).
Media
hyperplasia,
fibrosis,
hyalinisation,
thinning
or
disruption
occurred
only
if
the
associated
narrowing
of
the
arterial
lumen.
Obliterations
of
arteries,
with
or
without
an
intact
elastic
internal
membrane,
were
found
mainly
in
the
navicular
bones
of
Group
B
(Fig
6).The
diameter
of
the
arteries
is
summarised
in
Table
4.
In
the
navicular
bones
of
Group
C
and,
especially
Group
D
a
large
number
of
thin
walled
large
arteries
were
found,
with
an
average
diameter
of
0.20
mm.
These
arteries
had
a
wide
lumen,
the
staining
characteristics
of
the
vessel
wall
were
of
muscular
or
connective
tissue
fibres
without
elastic
internal
membrane.
In
counting
the
number
of
arterial
wall
changes
these
arteries
were
not
included.
Approximately
9
per
cent
of
the
arteries
of
the
distal
sesamoid
impar
ligament
per
navicular
bone
showed
arterial
wall
changes,
eg
intimal
thickening
with
or
without
splitting,
fragmentation
or
absence
of
the
internal
elastic
membrane
and
media
alterations.
In
Groups
A
to
D,
an
average
of
one
to
two
large
thick-walled
veins
surrounded
by
small
veins
were
found
in
the
distal
part
of
the
nutrient
foramen;
whereas,
in
the
nutrient
foramina
of
navicular
bones
of
normal
adult
horses,
one
or
two
large
thin
and/or
thick
walled
veins
surrounded
by
small
veins
were
found.
Marked
Fig
6:
Transverse
histological
section
of
an
obliterated
artery
(H&E,
findings,
compared
to
normal
navicular
bones,
were
the
complexes
x200)
The
subsynovial
became
fibrous
from
tissue
more
,
45
59
63
57
2
9
3
3
56 58
41
40
100
100
100
100
30
42
30
25
45
50
70
65
25
8
0
10
15
38
21
65
15
10
0 0
0
10
40
0
100
80
60
100
75
69
65
90
0
0
20
28
20
44
33
22
13
11
0
4
67
28
40
44
0
17
7
0
intima
and/or
internal
elastic
membrane
were
already
changed.
Fig
5:
Transverse
histological
section
of
an
artery
with
splitting
of
the
internal
elastic
membrane
(von
Gieson
elastics.
x200)
With
of
arterial
wall
there
the
occurrence
changes,
was
TABLE
6:
Percentage
arterial
wall
changes
of
the
arteries
A.13
mm
in
the
nutrient
foramina
per
group.
intima,
media
and
internal
elastic
membrane
changes
as
a
percentage
of
the
changed
arteries
and
the
type
of
lesions
as
a
percentage
of
the
changed
intima,
media
or
internal
elastic
membrane
Group
A
BCD
size
of
arteries
().13
W
-
7
EQUINE
VETERINARY
JOURNAL
423
of
thin
or
occasionally
thick-walled
veins
more
proximal
in
and
above
the
nutrient
foramen.
Above
the
nutrient
foramina
they
were
arranged
in
the
intratrabecular
spaces
(Fig
7).
These
complexities
were
observed
in
an
average
of
25
per
cent
of
the
navicular
bones
of
Group
B
and
in
all
navicular
bones
of
Groups
C
and
D.
Venous
wall
changes
like
pale
coloured,
loosening
of
the
longitudinally
oriented
collagen
fibres,
blood
vessels
in
the
wall
or
narrowing
of
the
lumen,
did
not
reach
beyond
10
per
cent
of
each
navicular
bone.
Locally
the
synovial
membrane
of
the
distal
sesamoid
impar
ligament
showed
villous
hypertrophy
and
hyperplasia
of
the
lining
cells,
increasing
from
Group
A
and
B
to
D.
The
vascularity
of
the
synovial
membrane
was
increased
in
almost
every
navicular
bone
except
in
30
per
cent
of
the
navicular
bones
of
Groups
A
and
B.
The
increased
vascularity
was
represented
by
vessels
which
could
not
be
identified
as
arteries
or
veins.
These
vessels
were
small
(0.10
mm),
had
a
narrow
lumen,
consisted
of
collagen
fibres
without
muscular
fibres
or
internal
elastic
membrane.
Obliterated
and
hyalin
vessels
occurred
frequently.
Collagen
fibres
arranged
circularly
around
one
or
more
vessels.
The
greater
the
number
of
vessels,
the
more
fibrous
the
connective
tissue
in
the
synovial
membrane,
especially
close
to
the
bone.
No
increased
number
of
inflammatory
cells
were
found.
Discussion
The
imbalance
and
distal
to
proximal
shift
between
the
distal
and
proximal
arterial
supply
indicated
a
reduction
of
the
distal
arterial
blood
supply
with
a
compensatory
reaction
of
the
proximal,
medial
and
lateral
supply.
This
is
accomplished
by
the
histological
finding
of
thin
walled
arteries
with
a
large
lumen,
without
an
internal
elastic
membrane
or
a
clear
difference
between
the
intima,
media
and
adventitia
in
Groups
C
and
D,
which
are
considered
to
be
newly
formed
arteries
as
a
reaction
to
the
decreased
distal
arterial
blood
supply.
Hertsch
et
al
(1987)
described
the
same
changes
in
the
pattern
of
the
arteriogram
in
horses
with
radiographically
visible
lengthened
and
mushroom-shaped
nutrient
foramina.
Their
material
corresponds
with
Group
C
from
this
study
and
with
the
navicular
bones
of
horses
without
clinical
and
radiological
signs
of
navicular
disease,
described
by
Rijkenhuizen
et
al
(1989a).
Hertsch
et
al
(1987)
also
considered
the
extension
of
the
proximal
supply
as
a
compensatory
reaction
to
a
decreased
distal
supply.
Fricker
et
al
(1982)
suggested
that
in
horses
with
occluded
digital
arteries,
the
small
artery
under
the
fetlock
joint
connecting
try
btft,
Fig
7:
Transverse
histological
section
of
the
venous
complexes
(HE.
100X)
the
palmar
digital
arteries
cannot
function
as
a
collateral
vessel,
resulting
in
navicular
disease.
Based
on
the
observations
of
the
arteriograms
in
our
study,
there
was
no
indication
of
obliteration
of
the
main
palmar
digital
arteries
as
a
cause
for
circulatory
disturbances.
Also,
in
this
study,
the
r.
nay.
and
the
r.
palm
show
no
changes
in
the
arteriogram
and
it
seems
likely
that
the
blood
supply
towards
the
r.
nav,
and
the
r.
palm,
is
sufficient
in
horses
with
navicular
disease.
The
changes
in
the
pattern
of
the
arteriogram
are
histologically
defined
by
the
presence
of
arterio
(lo)
sclerosis
and
newly
formed
arteries.
Earlier
descriptions
of
progressive
arterial
obstruction
associated
with
arteriosclerosis
(Nemeth
1971;
Colles
1982)
in
the
arteries
of
the
navicular
bone
are
confirmed;
however
no
signs
of
thrombosis
(Colles
et
al
1977)
are
found.
The
high
incidence
of
arterio
(lo)
sclerosis
in
and
around
the
nutrient
foramen
indicate
that
the
cause
of
the
changes
is
inside,
or
close
to,
the
distal
aspect
of
the
navicular
bone.
The
changes
in
the
intima
precede
the
media
changes
because
media
changes
are
not
observed
without
the
presence
of
changes
in
the
intima,
whereas
the
opposite
is
found
frequently
when
changes
are
present.
Thickening
of
the
intima
as
the
earliest
change
in
arteriosclerosis
is
reported
by
several
authors
(Pannier
and
Verstraeten
1966;
Leaf
and
Cotran
1980;
Niewiarowski
and
Rao
1983;
Taussing
1984;).
The
damage
to
the
intima
may
be
caused
by
a
number
of
factors
including
chronic
hypertension,
mechanical,
chemical,
immunological
and
viral
agents.
Local
hypertension
may
be
considered
to
be
a
cause
of
navicular
disease
in
the
distal
part
of
the
navicular
bone,
but
mechanical
causes
cannot
be
excluded.
Immunological,
chemical
and
viral
causes
are
less
plausible,
because
they
are
not
considered
to
be
as
localised.
Wheras
vascular
factors
are
involved
in
the
mechanism
of
remodelling,
any
disturbance
in
the
vascular
conditions
can
result
in
a
change
in
osteogenesis
(Brookes
and
Helal
1968).
Atrophy
of
bone
and
marrow
follow
obstructive,
inflammatory
and
degenerative
circulatory
disturbances
(Burkhardt
et
al
1987).
As
the
centrodistal
part
of
the
navicular
bone
is
mainly
dependent
on
the
distal
arterial
supply
(Rijkenhuizen
et
al
1989a),
and
the
distal
supply
is
insufficient,
an
effect
on
the
subchondral
bone
beneath
the
flexor
surface
can
be
expected.
Subchondral
changes
beneath
the
flexor
surface
in
navicular
disease
have
been
reported
(Wintzer
1964;
Svalastoga
1983;
Diehl
and
Cordey
1983;
Doige
and
Hoffer
1983).
Therefore,
the
distal
reduction
of
blood
supply
is
of
importance
in
the
pathogenesis
of
navicular
disease
and
contributes
to
the
development
of
irreversible
changes
in
the
bone.
As
indicated
by
Colles
(1979),
at
least
two
distal
arteries
must
be
effected
by
thrombosis
before
clinical
signs
appear.
The
results
of
this
and
earlier
studies
(Rijkenhuizen
et
al
I
989a)
confirm
the
importance
of
the
degree
to
which
the
arteries
must
be
affected
to
result
in
radiological
and
clinical
signs.
However,
the
role
of
the
vascular
system
in
the
pathogenesis
of
navicular
disease
is
apparently
more
significant
in
the
early
stages.
The
decrease
in
the
percentage
arterial
wall
changes
per
navicular
bone
from
Group
B
to
D
is
probably
due
to
stabilisation
or
reduction
of
the
number
of
arteries
affected
by
the
aetiological
agents,
combined
with
resorption
and
histological
disappearance
of
the
changed
arteries.
Additionally
the
arterial
supply
seems
to
be
restored
by
collateral
circulation
as
indicated
by
the
compensatory
proximal,
medial
and
lateral
supply
and the
formation
of
new
arteries.
The
changes
in
the
pattern
of
the
arteriogram
associated
with
arterio
(lo)
sclerosis
seem
to
precede
radiological
changes
which,
in
turn,
precede
clinical
evidence
of
navicular
disease.
This
conclusion
is
based
on
(a)
changes
in
the
pattern
of
the
arteriogram
occurring
before
clinical
signs
are
evident
(Group
A)
(b)
similar
changes
in
the
pattern
of
the
arteriogram,
but
not
as
severe
as
in
Groups
C
and
D,
and
arterio
(lo)
sclerosis
in
navicular
bones
of
young
sound
horses
(Rijkenhuizen
et
al
1989a),
(c)
the
positive
correlation
of
the
imbalance
and
the
distal
to
proximal
shift
between
the
distal
and
proximal
arterial
supply
of
the
navicular
424
EQUINE
VETERINARY
JOURNAL
bones
with
the
radiological
scoring
system
(Dik
et
al
1978;
Macgregor
1986)
and
the
clinical
evidence
of
navicular
disease.
Enlargement
of
the
nutrient
foramina
is
reported
by
Colles
(1979)
as
a
result
of
thrombosis
of
the
nutrient
arteries.
Dammrich,
Schebitz
and
Wintzer
(1983)
consider
the
enlarged
and
widened
nutrient
foramina
to
be
the
result
of
changing
pressure
loads
on
the
navicular
bone.
Hertsch,
Wissdorf
and
Zeller
(1982)
consider
the
form
of
the
nutrient
foramina
dependent
on
the
load
upon
the
distal
interphalangeal
joint;
the
synovia
is
pushed
into
the
nutrient
foramina
thereby
defining
the
form
of
the
nutrient
foramina.
Scott
(1968)
reports
that
bone
involvement
in
pigmented
villonodular
synovitis
occurs
because
of
the
growth
of
synovial
membrane
through
vascular
channels.
The
intrusion
expands
the
foramina
and,
following
the
path
of
least
resistance
along
the
course
of
the
osseous
vessels,
may
pass
deeply
into
the
bone
where
its
growth
produces
intraosseous
cysts
by
a
process
of
pressure
atrophy;
through
pressure,
the
nutrient
foramen
enlarges.
Scott
suggests
a
gradual
obliteration
of
vessels
by
pressure
of
invading
synovial
tissue.
Milgram
(1983)
considers
osseous
remodelling
secondary
to
the
expansion
of
soft
tissue
contents
and
in
a
later
stage
vascularisation
and
fibrosis.
In
this
study
the
surroundings
of
the
lengthened
and
mushroom-shaped
nutrient
foramina
were
irregular;
active
remodelling
takes
place
in
which
bone
resorption
predominates.
The
connective
tissue
of
the
nutrient
foramina
as
well
as
that
of
the
synovial
membrane
become
more
fibrous.
Arteriographically,
the
lengthened
nutrient
foramina
contain
extended
and
widened
arteries
and
lengthening
may
be
the
result
of
increased
pressure
of
the
arteries
upon
surrounding
bone
and
reflect
the
tendency
for
compensation
of
the
disturbed
arterial
supply.
The
mushroom-shaped
nutrient
foramina
contain
narrowed,
shortened
distal
arteries
or
no
arteries
entering
distally
and
also
the
synovial
membrane
introverted
into
the
nutrient
foramen
is
hypertrophied.
Widening
of
these
nutrient
foramina
probably
results
from
increased
pressure
of
the
synovial
tissue
upon
the
surrounding
bone
as
well
as
ischaemia
due
to
insufficient
blood
supply.
The
presence
of
nutrient
foramina
is
associated
with
a
changed
arteriogram,
increased
bone
remodelling
and
the
presence
of
fibrous
connective
tissue.
Therefore,
increased
pressure
(hypertension
and/or
increased
intraarticular
pressure)
and
ischaemia
may
be
responsible
for
the
changes
in
form
and
number
of
the
radiographically
visible
nutrient
foramina.
The
severity
and
extension
of
the
macroscopic
lesion
of
the
fibrocartilage
of
the
flexor
surface
of
the
navicular
bone
are
positively
correlated
(P<0.001,
Kruskal-Wallis)
with
the
classification
from
Groups
A
to
D.
In
the
early
stage
of
navicular
disease
the
flexor
surface
is
not
necessarily
changed,
whereas
changed
flexor
surfaces
are
also
noticed
in
navicular
bones
of
sound
horses
without
radiological
signs
of
navicular
disease
(Rijkenhuizen
et
al
1989a).
Although
a
positive
correlation
was
found
between
the
severity
of
the
macroscopic
lesions
on
the
fibrocartilage
of
the
navicular
bone
and
the
lesions
on
the
surface
of
the
deep
digital
flexor
tendon,
the
deep
digital
flexor
tendon
could
be
normal
despite
the
presence
of
lesions
within
the
fibrocartilage
of
the
navicular
bone.
Therefore,
the
lesions
on
the
deep
digital
flexor
tendon
are
secondary
to
those
on
the
flexor
surface
of
the
navicular
bone.
Lesions
of
the
fibrocartilage
of
the
navicular
bone
could
develop
independent
from
arterio
(1o)
sclerosis
within
the
underlying
bone.
The
results
of
this
study
indicate
that
disturbances
of
the
distal
arterial
supply
may
be
of
importance
in
the
pathogenesis
of
navicular
disease.
To
confirm
this
theory,
a
model
should
be
developed
in
which
the
results
of
a
diminished
distal
arterial
supply
are
observed.
The
effects
of
occlusion
of
the
arteries
entering
distally
on
the
navicular
bone
may
help
to
elucidate
the
aetiopathogenesis
of
navicular
disease.
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Received
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20.10.88
Accepted:
20.2.89