EXPERIMENTAL MODEL FOR THE ETHIOPATHOGENIC

STUDY OF LEGG-CALVE-PERTHES DISEASE

Nuno Craveiro Lopes M.D.

Orthopedic and Traumatologic Department
Garcia de Orta Hospital
Almada, Portugal

INTRODUCTION

In general, Authors accept as essential, the ischemic factor in the origin of Legg-Calve-Perthes
Disease (LCPD), knowing the precarious blood circulation of the proximal epiphysis of the femur during
the growth stage of the child (TRUETA, 1957; CROCK, 1967; OGDEN, 1974; CHUNG, 1976).
During the last few years there has been indications that two or more successive ischemic
episodes were necessary in order to trigger the typical necrosis of LCPD (SUTHERLAND, 1968;
SANCHIS, 1973; MCKIBBIN, 1974; INQUE, 1976; CATTERALL, 1982; SALTER, 1984; CRAVEIRO
LOPES, 1985; BENCANO, 1989). As origin of those ischemic episodes, there are an abundance of
literature pointing out factors of repeated local vascular network compression, as the prolonged and
habitual vicious positions of the lower limbs and the intra-articular repetitive effusions. (EYRING, 1964;
SOTTO-HALL, 1964; WOODHOUSE, 1964; TACHDJIAN, 1968; GAGE, 1972; GORE, 1974;
BORGSMILLER, 1980; KALLIO, 1985, 1986; SANCHIS, 1986; WINGSTRAND, 1985, 1987;
VEGTER, 1987).
In order to simulate a typical LCPD necrosis in a laboratory, the majority of the Authors utilized
open approaches, including intra-articular injection of wax (KEMPER, 1986), infusion of serum
(VEGTER, 1987), and electro coagulation of the epiphyseal blood vessels (SANCHIS, 1973; BENCANO,
1989; KAMEGAYA, 1990).
These methods have the disadvantage of including a surgical procedure and traumatic
maneuvers, which interfere with the regional circulation and lead to scars and trauma to local structures,
thus introducing foreign factors to the etiopathogeny of LCPD.
The attempts to experimentally reproduce the disease through closed approaches, namely through
forced positioning of lower limbs, were rarely successful. In the majority of these cases it was only
possible to trigger the development of simple necrosis without articular deformity (HENARD, 1970;
NAVARRO-QUILIS, 1979; CALVERT, 1984)
In our opinion, the micro-trauma of walking and physical activity of the child, over the femoral
head, which became quite fragile due to several ischemic episodes, is fundamental to the pathogenesis of
LCPD, triggering a sub-chondral fracture, event that is typical of the initial phase of the disease, as noted
by Salter (SALTER, 1984).
In order to better understand the etiopathogeny of LCPD, we attempted to experimentally
reproduce the morphologic, radiological and histological aspects of LCPD, utilizing a closed approach,
including the repetitive positioning of the lower limbs in extension and medial rotation, alternating with
vibrating micro trauma over the hip.

MATERIAL AND METHOD

Twenty Seven (27) White New Zealand rabbits were used, both male and female, with ages
ranging from 7 to 8 weeks. (weighing from 800 g to 1100 g).
The method used to trigger repetitive ischemic episodes in the epiphyseal nucleus required the
rabbits lower limbs to be extended while rotating them medially. We designed and built flexible

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aluminum splints, covered with rubber sponges. These frames would maintain the limbs in extreme
position while allowing some movement without causing pain to the animal. (Fig.1).
Starting in the early afternoon, the animals were placed in the frames 2 times/week for 6 hours
each time
In order to cause a micro trauma, a vibrating motor was used, with a metal plate adapted to it.

Fig.1 – Splints to maintain the lower limbs in a Fig.2 – Vibration motor to induce micro traumatic
extension-medial rotation position. stress over the hip.

With the rabbit in dorsal decubitus, with the knee and hip 90 degrees flexed, the metal plate was
applied on the femoral condyles, transmitting a non-painful, vibrating micro trauma to the epiphyseal
nucleus of the femoral head (Fig.2).
The vibration was applied for 30 seconds in the morning, exclusively on the right lower limb, the
day after the placement in the splints.
In a preliminary study group of 7 rabbits this type of percussion was done only over the right hip,
using the left hip as a control. The rabbits were sacrificed in groups: 2 after the end of 2 weeks, 3 after
the end of 3 weeks, and 2 after the end of 5 weeks.
There were 20 rabbits in the main study group. These rabbits had 2 weekly cycles of splints
applications on both lower limbs followed by percussion only on the right hip the next morning. The
rabbits were sacrificed in groups: 3 at the end of 1 week, 3 at the end of 2 weeks, 5 at the end of 3 weeks,
5 at the end of 4 weeks, and 4 at the end of 5 weeks.
The preparation of the animals and specimens and the study methods, including direct
examination, radiological examination, evaluation of parameters, diaphanization exam and histological
examination, were performed following the protocol described in a prior paper (CRAVEIRO LOPES,
1993). We have prepared half of the animals for diaphanization and the other half for histological study.

RESULTS

Preliminary Group
The comparison of the specimens included in this group did not show differences between the hip
on which the micro trauma was applied and control side.
Measurement of the parameters on those hips, revealed statistically non-significative differences
when compared with the control hips. The p value was always higher than .005, in the epiphyseal index
(EI)(m-50% var-44 to 56 right, m-48.7 var-44 to 50 left) in the epiphyseal angle (EA)(m-46.5 var-42 to
50 right, m-47.4 var-44 to 52 left) and the trochanter-head height (THH) (m-4.1 var-3 to 5.7 right, m-4.2
var-3.5 to 6.8 left).

Main Group
In this group, the results varied according to the lapsed time the rabbits were sacrificed and the
side in which the percussion technique was applied.

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 Fig.3 – Direct examination of proximal femurs. Fig.4 - Radiografic examination of proximal
Rabbits sacrificed one week after the procedure. femurs. Rabbits sacrificed one week after the
procedure.

The 3 rabbits sacrificed at the end of one week of application of the bilateral splints, with
percussion to the right side, did not show any significant differences between the right -left hip and the
control hips from the preliminary group. These findings were the same in the direct examination (Fig. 3),
radiological examination (Fig. 4) and in the diaphanization examination (Fig. 5).

Fig.5 – Diaphanized examination of the right Fig.6 – Histological examination of bone trabecula
proximal femur. Rabbit sacrificed one week after of the right femoral epiphysis. Rabbits sacrificed
the procedure. one week after the procedure.
(Hematoxilin-eosin, 20X)
The histological examination showed an articular cartilage of similar structure and thickness as
the hips from the preliminary group (12 mm with 10X magnification) (Fig. 7), a normal structure of the
osteoid and myeloid epiphyseal tissue (Fig. 6), and also a normal growth cartilage in regards to structure
and thickness (Fig. 8).

Fig.7 - Histological examination of articular Fig.8 - Histological examination of growth plate of

cartilage of the right femoral epiphysis. Rabbits the right femoral epiphysis. Rabbits sacrificed one
sacrificed one week after the procedure. week after the procedure.

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 (Hematoxilin-eosin, 10X) (Hematoxilin-eosin, 4X)
The measurement of the parameters revealed values of epiphyseal index (EI) of 44, 47, 46 to the
right and 45, 45, 44 to the left, of epiphyseal angle (EA) of 53, 48, 55 to the right and 50, 53, 47 to the
left, and of the trochanter-head height (THH) of 4.5, 3.5, 4 to the right and 4, 3.5, 3.5 to the left.
The group of 3 animals sacrificed at the end of 2 weeks showed the following alterations:
Right Hip: In 2 animals, on the direct examination a slight flattening of the head of the femur
(EA-40, 39, 44) without distortion of the neck’s axis or growth arrest (EA-50, 56, 45 THH-4, 5, 3.5). The
radiological and the diaphanization examinations confirmed the slight collapse of the epiphyseal nucleus
(Fig. 9). The hips of the animal prepared for a histological examination presented signs of necrosis,
specially at the level of the osteoid tissue which showed trabecular structure with necrosis in the central
zone, enveloped by new viable bone tissue, surrounded by large quantities of osteoblasts. (Fig. 10). At the
myeloid tissue level we observed the reduction of the number and dimension of the adipocites and the
increase of the number of the fibroblasts.

Fig.9 - Diaphanized examination of the right proximal Fig.10 - Histological examination of bone trabecula of the
femur. Rabbit sacrificed two weeks after the right femoral epiphysis. Rabbits sacrificed two weeks
procedure. after the procedure. (Hematoxilin-eosin, 20X)

Left Hip: In 2 of the animals, no alterations were found when compared to the control hips of the
preliminary group (EI-46, 49, 49; EA-52, 54, 53; THH-5, 5, 4.5). During the radiological examination,
we observed in one animal, thickening of the articular cartilage and an increase in density of the
epiphyseal nucleus. The histological exam presented similar images to those mentioned regarding the
right hip.
The following was observed in the group of 5 rabbits sacrificed at the end of 3 weeks:
Right Hip: Direct exam and well as the measurement of the parameters showed flattening of the
epiphyseal nucleus in 4 cases (EI-32, 41, 42, 41, 45; EA-51, 56, 50, 55, 58; THH-5.6, 4.5, 5, 4, 4.5)
(Fig.11). This alteration was confirmed in the radiological examination and on the 3 diaphanized hips,
which also showed increase in the thickness of the articular cartilage without other alterations.

Fig.11 - Direct examination of proximal femurs. Fig.12 - Histological examination of bone trabecula of
Rabbits sacrificed three weeks after the procedure. the right femoral epiphysis. Rabbits sacrificed three
weeks after the procedure. (Hematoxilin-eosin, 20X)

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The histological exams available on 2 hips showed a total disorganization of the trabecular structure, an
alveolar aspect of the osteoid tissue with anarchic disposition, similar to the woven bone, described for
LCPD. The myeloid tissue contained fibrosis, rich in fibroblasts, but with no evidence of adipocites and
an accentuated decrease in the myeloid cells (Fig. 12). The articular cartilage had more than doubled in
thickness when compared to the hips from the preliminary group (28mm when amplified 10X) (Fig. 13).
Left Hip: After a direct examination and the measurement of the parameters, we found no
significant differences when compared with the control hips in the preliminary group (EI-47, 47, 45, 46,
48; EA-50, 56, 50, 46, 58; THH-4, 3.5, 3.5, 4, 3.5). In the radiological examination we observed the
thickening of the articular cartilage that was also revealed on the 3 rabbits available for diaphanization.
On the two histological exams in this group, 1 was considered normal and the other showed signs of
simple trabecular necrosis and repair, although no alterations were found through direct examination.

Fig.13 - Histological examination of articular cartilage Fig.14 - Direct examination of right proximal femur.
of the right femoral epiphysis. Rabbits sacrificed three Rabbits sacrificed four weeks after the procedure.
weeks after the procedure. (Hematoxilin-eosin, 10X)

The following was observed in the group of 5 rabbits sacrificed at the end of 4 weeks:
Right Hip: Both the direct examination and the measurement of parameters showed accentuated
flattening of the epiphyseal nucleus in all the hips, except 1 that was considered normal (EI-40, 41, 40,
39, 52). On 3 of the cases there was an elevation of the lateral zone of the epiphyseal nucleus by extrusion
of the epiphyseal nucleus outside the acetabulum (Fig. 14). These findings were confirmed on the
radiological examination that also showed thickening of the articular cartilage. The parameter
measurements in these cases had a tendency to varus (EA-35, 38, 40, 50, 54) and the raising of the greater
trochanter. The 3 diaphanized specimens showed thickening of the articular cartilage and in 2 of the
cases showed the aspect of extrusion of the lateral zone of the epiphyseal nucleus, observed in direct and
radiological examinations.

Fig.15 - Histological examination of bone trabecula of Fig.16 – Sub-chondral fracture. Rabbits sacrificed four
the right femoral epiphysis. Rabbits sacrificed four weeks weeks after the procedure.
after the procedure. (Hematoxilin-eosin,10X) (Hematoxilin-eosin 10X)

Histological examination of one normal hip, showed nothing abnormal. However, in another
pathological hip, there was a disorganization of the trabecular structure with viable osteoid zones,

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alternating with zones of trabecular necrosis, profusely invaded by fibrous and cartilaginous tissue and a
total substitution of the myeloid tissue by mesenquimatous tissue, rich in fibroblasts (Fig. 15) and a sub-
chondral fracture line was clearly visible (Fig. 16).
The growth plate in the pathological hip showed an irregular structure, thinner in width. It was
possible to note on the metaphyseal side, the preserved osteoid and the myeloid tissue, but on the
epiphyseal side both tissues were altered, with the myeloid tissue showing severe fibrosis (Fig. 17).
Left Hip: Both the direct exam and the measurement of the parameters did not show significative
differences in 3 cases when compared to the control hips of the preliminary group. The other 2 cases
showed a slight collapse (EI-41, 40, 48, 48, 49; EA-50, 52, 55, 48, 55; THH-4, 3.5, 3.5, 3.5, 4). The
radiological examination showed thickening of the articular cartilage, which was also confirmed on the 3
available diaphanized specimens. On two histological exams in this group we observed signs of both
simple trabecular necrosis and repair.

Fig.17 – Histological examination of growth plate of Fig.18 - Radiografic examination of proximal

the right femoral epiphysis. Rabbits sacrificed four femurs. Rabbits sacrificed five weeks after the
weeks after the procedure. At your right, normal procedure.
metaphyseal bone, at your left, altered bone. At the
middle, a thinner and disorganized growth plate.
(Hematoxilin-eosin 10X)

The following was observed in the group of rabbits sacrificed at the end of 5 weeks:
Right Hip: Both the direct exam and the measurement of parameters showed the existence of an
accentuated flattening of the epiphyseal nucleus in all cases (EI-40, 40, 35, 38). Three specimens showed
an extrusion of the lateral zone of the epiphyseal nucleus; in all the specimens, there was a varus effect
(EA-37, 37, 40, 39) and great trochanter lifting (THH-7, 6.9, 7, 6.9). These findings were confirmed by
the radiological examinations that showed, in one case, an increase in density of the epiphyseal nucleus,
and in the other, the typical “swinging rope” sign, seen in sequels of LCPD, combined with a thickening
of the articular cartilage (Fig. 18). The measurement of parameters showed in the entire group, an
accentuated collapse of the epiphyseal nucleus, varus of the neck and greater trochanter lifting.
On the hip prepared for diaphanization, we observed the increase in thickness of the articular cartilage
and the lateral extrusion of the epiphyseal nucleus also seen on the direct and radiological examinations.
On the available histological exams of the 3 hips, we observed similar images to the pathological hips of
the prior group.
Left Hip: We found in 2 cases, no significant alterations on the direct examination nor on the
measurement of parameters, when compared to the hips in the control preliminary group, while observing
a slight collapse on the 2 remaining samples (EI-44, 43, 50, 49; EA-50, 49, 48, 50; THH-4.5, 4, 4.5, 4.5).
The radiological examinations showed a thickening of the articular cartilage, which was also seen on the
diaphanized hip. There were 3 available histological exams. One was normal; in one of the other two,
aspects of simple trabecular necrosis and repair was observed and on the other, there was a total
disorganization of trabecular structure, with alveolar aspect of the osteoid tissue with anarchic disposition,
the myeloid tissue showing fibrosis, and with the disappearance of adipocites similar to the images of
“woven bone” typical of LCPD.

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 DISCUSSION

The importance of multiple and fractional ischemic episodes in the origin of LCPD has been
extensively documented. However, it is indicated that there are multiple factors that trigger the onset of
the disease, making it necessary a specific sequence of chained conditions in order for LCPD to develop.
The first signs on the importance of multiple ischemic episodes were brought up in experimental
research performed in dogs by Freeman (FREEMAN. 1969), on rabbits by Sanchis (SANCHIS, 1973),
and later by Bencano (BENCANO, 1989) they were able to simulate the disease through repeated, total
surgical section of the vascular network to the femoral head.
Mckibbin (MCKIBBIN, 1974), Inoue (INOUE, 1976) and Catterall (CATTERALL, 1982)
presented histological studies performed on femoral heads of patients with LCPD. These patients revealed
images of necrosis superposed to zones of bone regeneration of a prior ischemic insult, confirming the
theory of the repetitive ischemic episodes in the origin of LCPD.
The first references to the importance of traumatic or micro traumatic factors in the origin of the
disease, are from Salter (SALTER, 1968, 1984), substantiated by the experimental work of Douglas
(DOUGLAS, 1981).
During our experimental research, we observed that the existence of a repeated micro trauma to
the hip, will not in itself, produce alterations on the proximal femoral epiphysis, even after 10 episodes
over 5 week time, which is equivalent to 4 years on a child.
Vegter (VEGTER, 1987), through the use of intra-articular injection of serum under pressure on
the hip of a rabbit, demonstrated the importance of the repeated fractional necrosis, provoked by the
increase of intra-articular pressure on the onset of the disease, indicating that the probable cause of the
deformity of the head, is a reduction of its mechanical resistance due to superposing of new necrotic
episodes over a reconstruction process in progress.
Eyring (EYRING, 1964), Soto-Hall (SOTO-HALL, 1964), Kallio (KALLIO, 1985), Vegter
(VEGTER, 1987), and Schoenecker (SCHOENECKER, 1978), demonstrated that the positioning of lower
limbs in prolonged and repeated medial rotation and extension, is sufficient to increase the joint pressure
on the hip, although these authors only reached values superior to the systolic pressure when, there was a
simultaneous intra-articular effusion, even if small.
Our experimental research on the hips subject to repeated posture in medial rotation and
extension showed us only the first signs of simple necrosis to the epiphyseal nucleus after the 3rd or 4th
positioning episode and after the end of 2 weeks of evolution (Fig. 19 and 20). These first signs did not
seem to have been related to the simultaneous existence of microtrauma, because they developed
indifferent on the hips subject to this micro trauma and those not subject to micro trauma.
According to our data and in agreement to the research of the mentioned authors, the first
positioning episodes do not provoke an ischemic episode and subsequent necrosis, probably because the
joint pressure does not increase enough to block blood circulation in the retinacular vessels, but they
induce an intra-articular effusion.
As subsequent positioning episode occur, the previously induced intra-articular effusion creates the
necessary conditions to obtain sufficiently high pressure inside the joint in order to provoke ischemic
episodes.
We observed that these first necrosis signs were those of simple and fractional necrosis of the
myeloid and osteoid tissue, followed by phenomena of regeneration and rapid reconstruction of the
trabecular bone structure, with the abundant presence of osteoblasts along side the necrotic trabeculae and
the formation of bone tissue of a lamellar aspect (Fig. 10 and 20). These aspects show the integrity of the
bone canals, capable of being rerouted and reactivated soon after the ischemic episode, as was observed in
Vegter’s research (VEGTER, 1987).

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 Fig.19 – Evolution of affected hips by weeks of procedure.

After the 3rd week of positioning and repetitive micro-traumatic stress, we observed the presence
of a severe disorganization of the trabecular structure of the epiphysis, similar to the aspect of LCPD
“woven bone” (12 and 20), described by Kenzora (KENZORA, 1978), Inoue (INOUE, 1976), Vegter
(VEGTER, 1987) and others. In our opinion, this type of response to repetitive ischemic episodes is
responsible for the reduction of mechanical resistance of the epiphysis, making it more susceptible to
micro-traumatic insults.
On all groups sacrificed after the 4th week of positioning and micro-traumatic stress, we observed
a sub-chondral fracture line and the collapse of the epiphyseal nucleus, with crushing of myeloid and
vascular canals, making impossible a primary osteogenic replay. This way we observe the slow
substitution of the bone sequestrum by poorly vascularized mesenquimatous tissue, rich in fibroblasts and
by cartilaginous tissue (Fig. 17 and 20), that originates the characteristic aspect of collapse, fragmentation
and lateral extrusion of the epiphyseal nucleus, leading to the “head at risk” signs of LCPD (Fig. 14 and
15), described by Catterall (CATTERALL, 1971), followed by the remaining stages of the disease as
described by Waldenstrom (WALDENSTROM, 1923).

Fig.20 – Evolution of the bone pattern by weeks of procedure. A – Normal

bone. B – Simple necrosis. C – Woven bone. D – LCPD.

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 The results of the current experimental research, which are in agreement with our daily clinical
experience and with the work of the aforementioned Authors, lead us to believe that there may be the
existence of a new clinical entity, independent of LCPD.
This new entity, we propose to call Ischemic Disease of the Growing Hip (IDGH), is
characterized by the existence of repetitive ischemic episodes of the proximal femoral epiphysis, in
susceptible children and shows a particular biotype and symptomatology.
In the presence of certain rhythm and sequence of ischemic episodes, along with traumatic or
micro-traumatic factors in a certain stage, IDGH can progress to Legg-Calve-Perthes Disease (LCPD).
The relation between IDGH and LCPD is similar to the relation between coronary ischemic
disease and the myocardium infarction, because in both situations there is an intermittently insufficient
circulatory terminal network that, in certain situations can lead to a massive necrosis of the involved
tissue.

CONCLUSIONS

The prolonged and repeated positioning of lower limbs in medial rotation and extension induced
a sufficient increase of hip joint pressure to provoke an ischemic episode and an epiphyseal necrosis of the
femoral head.

After this necrosis, a process of rapid reconstruction was observed, with revascularization and
primary rehabilitation of the necrotic structures, without loss of mechanical resistance and distortion of
the structure of the epiphysis.
The repetition of ischemic episodes establishes a unique pathologic entity with particular
characteristics that behaves as an intermittent ischemic disease, leading to a distortion of the osteogenic
reaction, with weakness of the mechanical structure of the epiphysis.
Under these circumstances, the existence of micro-traumatic aggression over the hip, led to a
sub-chondral fracture, collapse of the epiphysis, destruction of the primitive vascular network,
proliferation of fibrous tissue with condensed aspect of the trabecular structure, and formation of a true
bone sequestrum, which constitute the initial phase of Legg-Calve-Perthes Disease.
On these circumstances, the epiphyseal reconstruction includes a slow substitution of the bone
sequestrum by mesenquimatous tissue with profusion of fibroblasts from surrounding viable myeloid tissue
and cartilaginous tissue from deep layer of the articular cartilage, thus initiating the fragmentation stage
of LCPD.
The results of this experimental research are in accordance with the existence of a new clinical
entity, we called “Ischemic Disease of the Growing Hip” (IDGH), which, in determined circumstances,
can evolve to Legg-Calve-Perthes Disease.

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