PATHOLOGY OF BLOOD CIRCULATION
Blood Vessels And Lymphatics In Organ Systems
D. W. Lennox and D. S. Hungerford
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abnormalities of bone blood vessels underlie a number of clinical
entities. Several of the better known of these are discussed
number of eponymic disorders, including Legg-Calve-Perthes'
disease, Osgood-Schlatter's disease, Sindig-Larrsen-Johannson
disease, Kohler's disease, Freiberg's disease, Schuermann's
disease, Panner's disease, and Thiemann's disease, were believed
to originate from a similar vascular abnormality of bone blood
vessels. It now appears that those conditions about the patella
or patellar tendon represent avulsion fractures.
Legg-Calve-Perthes' disease: One theory regarding the
development of this entity is that circulatory embarrassment
from retinacular vessel disruption in the region of the physis
plays a very important role (Ponseti, 1956). In comparing
the effect of venous tamponade of the hip capsule on femoral
head blood flow in mature and immature dogs, Launder et
al. (1981) reported a significant rise in femoral head
pressure in puppies following capsule inflation but noted
no significant change in either pressure or flow in adults.
These results were attributed to the absence of an intact
intramedullary venous drainage of the femoral head in the
immature animal. The validity with which these data can be
applied to humans, as in the case of Legg-Calve-Perthes'
disease, is unclear. Heikkinen et al. (1980) reported
delayed venous drainage from the femoral neck to be indicative
of a of a poor prognosis in this disorder. Heikkinen et
al. (1976) found that after treatment by intertrochanteric
osteotomy, venous outflow patterns became normal at 4-15 months
following surgery. Suramo et al. (1964) have demonstrated
that venous drainage of the femoral neck occurs via capsular
veins in the normal child's hip, but via the intramedullary
route in children with Perthes' disease and with an intact
growth plate. In a study of intracapsular tamponade in puppies,
Tachdjian and Grana (1968) reported partial vascular obstruction
at 80-100 mm Hg pressures and avascular necrosis with pressures
of 200 mm Hg maintained for 10 hr. Utilizing a similar approach
but measuring flow with the hydrogen washout technique, Borgsmiller
et al. (1980) eliminated epiphyseal flow at 150 mm
Hg pressure and on the basis of their findings concluded that
Legg-Calve-Perthes' disease resulted from arterial rather
than venous tamponade. Woodhouse (1962, 1964) found that in
adult dogs, avascular necrosis developed after exposure to
hip intracapsular pressures of 50 mm HG for 12 hr following
femoral neck osteotomy. In puppies, a similar tamponade, but
without osteotomy, also produced femoral head necrosis at
12 hr. This worker concluded that avascular necrosis resulted
from venous tamponade, capillary engorgement, fluid extravasation,
microcapillary sludging, and irreversible intravascular thrombosis.
FRACTURES AND DISLOCATIONS
sufficient to produce a fracture or dislocation can result
in damage to the blood supply to an entire bone, e.g., the
talus in subtalar dislocation, or a portion of a bone, e.g.,
the femoral neck in femoral neck fracture. With severe circulatory
compromise, avascular (ischemic) necrosis may result. Particularly
vulnerable to the development of ischemia are intracapsular
fractures, as occur in the hip and shoulder. In these locations,
blood supply is marginal and damage to surrounding soft tissue
may be sufficient to induce irreversible ischemia. The duration
of the ischemia appears to be a critical factor since better
results are obtained in cases of hip dislocation reduced within
12 hr than in those treated after that time period. In fractures
of the femoral neck, bone scans have been recommended as diagnostic
tools to deterimine the viability of the femoral head.
necrosis of the femoral head in children is a complication
following reduction and cast immobilization, as in the treatment
of congenitally dislocated hips. Schoenecker et al.
(1978) demonstrated in dogs that a position of forced frog-leg
abduction and internal rotation obliterated or drastically
reduced circulation to the femoral head.
and Shim (1977) reported that in rabbits with trauma-induced
dislocation of the hip, circulatory compromise was present
in both adult and immature animals, but it was worse in immature
rabbits, reaching a maximum effect after 24 hr of continued
dislocation. Aseptic necrosis was evident in the specimens,
particularly in the case of immature animals. Duncan and Shim
found that in the adult rabbit, the anastomotic connection
between epiphyseal and metaphyseal vessels afforded some protection
to the femoral head from the insult to the extraosseous nutrient
system, whereas in the immature animal, without such a vascular
arrangement, damage to the system of supply and of drainage
could result in necrosis.
infarcts, which are believed to arise from arterial obstruction,
in many instances are asymptomatic, being noted incidentally
in roentgenograms or bone scans performed for other reasons.
Long bones are involved almost exclusively. Most commonly,
lesions are a few millimeters in size but may vary to involve
a large portion of the shaft; the ends of long bones are more
often involved than other areas. Roentgenograms demonstrate
areas of mottled sclerosis. In contrast, areas of infarction
and necrosis involving a periarticular region are associated
with a considerably different clinical pattern, roentgenographic
picture, pathologic changes, and prognosis (see Section D-5,
and/or vascular surgery may greatly alter circulation in bone.
For example, internal fixation devices in the treatment of
fractures can affect bone blood supply. In this regard, Rand
et al. (1981) compared the vascular effects of open
intramedullary nailing after reaming with those of compression
plate fixation of a tibial fracture in the dog. Bone blood
flow remained elevated for longer periods and reached a higher
level overall in the intramedullary rod group than in that
with compression plate fixation. However, the latter approach
provided mechanical strength at the fracture site sooner than
did rod fixation. Similar effects on bone healing were noted
with both extraperiosteal and subperiosteal plate placement,
with fracture healing occurring by different mechanisms in
the two groups. Whereas with the intramedullary rod group,
fracture healing was predominantly by periosteal callus, in
the compression plate group, endosteal callus formation occurred.
Both open intramedullary nailing after reaming and intramedullary
rod insertion damage the medullary vasculature and produce
avascularity of a portion of the cortical diaphyseal region
(Trueta and Cavadias, 1955; Göthman, 1961; Rhinelander,
1974). Compression plate fixation damages cortical efferent
blood flow beneath the plate (Olerud and Danckwardt-Lilliestrom,
et al. (1978) studied the effects of periosteal stripping
and medullary reaming on regional blood flow in the tibias
of mature and immature rabbits. By stripping tibial epiphyseal
periosteum, the epiphyseal circulation was eliminated, as
measured by the hydrogen washout technique. In mature rabbits,
the epiphyseal flow was markedly reduced by periosteal stripping,
but no change in blood flow was noted following wide reaming
of the epiphyseal center in both mature and immature animals.
Diaphyseal and metaphyseal flow was unchanged following separate
medullary reaming or periosteal dissection in both groups.
When intramedullary reaming and periosteal stripping were
performed, cortical diaphyseal flow ceased, but metaphyseal
flow persisted. Whiteside et al. (1978) concluded that
both venous drainage and arterial supply systems traverse
endosteal and periosteal systems and that either can sustain
a number of orthopedic implants, including total hip replacement
and total knee replacement prostheses, utilize the polymer
polymethylmethacrylate (PMMA) to secure components to bone,
the vascular response elicited by this substance was studied
by Brookes and Gallanaugh (1975). They implanted a plug of
methylmethacrylate into the rat tibia and calculated blood
flow using 51Cr- and 59Fe-tagged resin
particles. At both 14 and 112 days postoperatively, both blood
volume and blood flow were significantly depressed in the
tibias in which the acrylic cement had been implanted. The
extent to which this factor may be operative in the case of
human joint replacement is uncertain. Theoretically, however,
devascularized bone appears prone to infection, and this may
be a contributing factor in the major problem of loosening
in joint replacements.
ISCHEMIC NECROSIS OF THE FEMORAL HEAD
Theories of pathogenesis: A number of hypotheses have
been proposed with regard to the pathogenesis of ischemic
necrosis of the femoral head. One of these, the infarction
theory, was espoused by Chandler (1948), who attributed the
condition to compromise of the lateral retinacular vessel,
with subsequent infarction of the anterolateral segment of
the femoral head. According to him, with revascularization
of the infarcted segment, the femoral head then becomes softened
and finally fails mechanically. However, McFarland and Frost
(1961) suggested that it is the accumulation of microfractures
without repair that eventuates in macrofractures, causing
the femoral head to collapse.
view, the embolization theory, is based on the assumption
that fat emboli produce infarction and ischemic necrosis.
Jones and Sakovich (1966) demonstrated that rabbits given
intraarterial injections of Lipiodol were found to have fat
droplets in a subchondral location in the femoral head. Of
interest in this regard is the finding that hyperlipidemia
is a common abnormality in ischemic necrosis patient populations
(Cruess et al, 1975; Fisher, 1978; Jones, 1971). Although
fat emboli have been reported in ischemic necrosis of the
femoral head, it is still not possible to state unequivocally
that they are responsible for the disease and, if so, whether
the basis is one of arterial or arteriolar infarction.
the progressive ischemia theory has been proposed to explain
the mechanisms responsible for the development of ischemic
necrosis of the femoral head. In this regard, Michelsen (1967)
and Wilkes and Visscher (1975) have offered the analogy between
circulation in bone and the functioning of a Starling resistor,
with the rigid canister of the resistor corresponding to the
rigidity of cortical bone. Thin-walled tissues, the vessels,
traverse the canister but do not open into it. Under such
conditions, structures outside the vascular space but within
the container of bone (the elements of marrow) can modulate
blood flow by changes in tissue pressure. Thus, an increase
in pressure in the compartment (elevated bone marrow pressure)
could collapse such thin-walled vessels as sinusoids and veins,
increase peripheral resistance, and diminish flow.
concept of bone and its circulation as functioning in a manner
similar to a Starling resistor is supported by the common
finding of elevated intramedullary pressure in a number of
different pathologic circumstances, including ischemic necrosis
of the femoral head (Arlet and Ficat, 1964; Ficat and Arlet,
1968; Hungerford, 1979; Hungerford and Zizic, 1978).
the case of Gauchers disease, proliferating reticuloendothelial
cells could increase bone marrow pressure, with resultant
diminished flow. With regard to caisson disease, the nitrogen
bubbles generated by decompression could expand extravascularly,
increase bone marrow pressure, and compromise flow. Essentially
any circulatory injury that produces ischemia could result
in fluid extravasation into the extravascular (bone marrow)
space, with resultant increased bone marrow pressure and circulatory
and Rabinowitz (1973) reported no evidence in support of sudden
infarction in an examination of 82 femoral heads studied at
various times following femoral neck fracture. Multiple areas
of ischemia were distributed throughout the femoral head after
fracture. With time and the added stress of weight bearing,
the ischemic areas were localized to that portion of the femoral
head that assumed the weight-bearing load. Hungerford (1983)
presented several examples of ischemic necrosis of the femoral
head that were localized not to the anterolateral fracture
but rather at a site that, although previously a non-weight-bearing
region, was rotated into a weight-bearing position by the
fracture. This argues for the role of biomechanical factors
in determining the region of morphologic change in ischemic
Diagnosis: Bone marrow pressure can be measured clinically
and is elevated in all phases of ischemic necrosis, even at
the preclinical stages in some patients (Hungerford, 1979).
In this disorder, venograms, performed by injecting the radiopaque
material intraosseously, demonstrate poor filling of the metaphyseal
veins, stasis, and diaphyseal reflux on films taken 5 min
and Ficat (1964) and Ficat and Arlet (1968) studied necrosis
of the femoral head utilizing bone marrow pressure measurements
and venograms, together with a bone biopsy obtained from the
femoral neck and head. They found that core decompression
(removal of a core or plug of bone) resulted in pain reduction,
and in some cases this procedure retarded radiologic progression
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