Abstract
Background: Osteonecrosis of the femoral head is a frequent
complication in adult patients with sickle cell disease. However, little is
known about the natural history of asymptomatic lesions.
Methods: One hundred and twenty-one patients (121 hips) with sickle
cell disease and asymptomatic osteonecrosis of the femoral head that was
contralateral to a hip with symptomatic osteonecrosis were identified with
magnetic resonance imaging between 1985 and 1995. The lesions were graded with
use of the Steinberg classification system. The patients were followed with
annual plain radiographs. The mean duration of follow-up was fourteen
years.
Results: At the time of the initial evaluation, fifty-six hips were
classified as Steinberg stage 0, forty-two hips were classified as Steinberg
stage I, and twenty-three hips were classified as Steinberg stage II. At the
time of the most recent follow-up, pain had developed in 110 previously
asymptomatic hips (91%) and collapse had occurred in ninety-three hips (77%).
Symptoms always preceded collapse. Of the fifty-six hips that were classified
as Steinberg stage 0 at the time of the initial evaluation, forty-seven (84%)
had symptomatic osteonecrosis and thirty-four (61%) had collapse at the time
of the most recent follow-up. Of the forty-two asymptomatic stage-I hips,
forty (95%) became symptomatic within three years and thirty-six (86%) had
collapse of the femoral head. Of the twenty-three asymptomatic stage-II hips,
all became symptomatic within two years and all collapsed; the mean interval
between the onset of pain and collapse was eleven months. At the time of the
final follow-up, ninety-one hips (75%) had intractable pain and required
surgery.
Conclusions: Untreated asymptomatic osteonecrosis of the femoral
head in patients with sickle cell disease has a high likelihood of progression
to pain and collapse. Because of the high prevalence of complications after
total hip arthroplasty in patients with this disease, consideration should be
given to early surgical intervention with other procedures in an attempt to
retard progression of the disease.
Level of Evidence: Prognostic Level II. See Instructions
to Authors for a complete description of levels of evidence.
Osteonecrosis of the femoral head is a frequent complication in patients
with sickle cell disease, and there is a high prevalence of bilateral
involvement1-3.
The natural history of untreated symptomatic osteonecrosis of the femoral head
in patients with sickle cell disease is one of progression to collapse and
degenerative
arthritis1. Several
studies have analyzed the natural history of asymptomatic osteonecrosis of the
femoral head associated with steroids and alcohol
abuse4-6,
but, to our knowledge, there have been no reports on the natural history of
asymptomatic osteonecrosis in adult patients with sickle cell disease and
symptomatic osteonecrosis in the contralateral hip. The purpose of the present
study was to try to define the natural history of asymptomatic osteonecrosis
of the femoral head so that we might devise appropriate and timely treatment
strategies that avoid or delay total hip arthroplasty in patients with sickle
cell disease.
The present study was approved by the institutional review board. Between
1985 and 1995, 121 consecutive patients with sickle cell disease and
symptomatic osteonecrosis of one hip were identified. Because of the high risk
of bilateral osteonecrosis in patients with sickle cell disease, both hips
were evaluated with radiographs and magnetic resonance imaging. The patient
population consisted of seventy men and fifty-one women. The mean age of the
121 patients was twenty-six years (range, eighteen to thirty-one years). The
mean duration of clinical and radiographic follow-up was fourteen years
(range, ten to twenty years). Forty-eight patients were homozygous for
hemoglobin S, fifty-eight had hemoglobin S/hemoglobin C, and fifteen had
hemoglobin S/B thalassemia. No patient who had the sickle cell trait was
included in this series.
All magnetic resonance images were acquired with a 1.5-T superconducting
unit. T1-weighted spin-echo images were acquired with repetition times of 400
to 600 msec and echo times of 20 to 40 msec. Long images with repetition times
of 1500 to 2240 msec and echo times of 30 to 100 msec were used to acquire
images of varying T2 weighting (transverse relaxation time). Images were
acquired with coronal and sagittal sections. The diagnosis of osteonecrosis on
magnetic resonance images was based on abnormal band-like signals and
hypointense band-like zones on T1-weighted images and matching hyperintense
zones on short tau inversion recovery (STIR) images. The volume of
osteonecrosis was also evaluated. The percentage volume of necrosis within the
femoral head was calculated by dividing the volume of the necrotic bone by the
volume of the femoral head.
The extent of osteonecrosis was graded according to the method of Steinberg
et al.7
(Table I). Because the word
collapse is considered to indicate a major radiographic sign in most
classification systems but is sometimes ambiguous, we used the term collapse
only for hips with Steinberg stage-IV involvement
(Table I). We also graded the
asymptomatic hips on the basis of the size of lesion according to the criteria
of Steinberg, with grade A indicating mild involvement (involvement of <15%
of the femoral head on radiographs or magnetic resonance images), grade B
indicating moderate involvement (involvement of 15% to 30% of the femoral
head), and grade C indicating severe involvement (involvement of >30% of
the femoral head).
All 121 patients were followed at the Sickle Cell Disease Center at our
institution, where we obtained an interval history and performed a clinical
examination annually. In addition, the Harris hip score was determined and
plain radiographs were made. No patient was lost to follow-up during the
study. Because there was little conclusive information on the risk of
progression of asymptomatic osteonecrosis in patients with sickle cell disease
at the beginning of this study, no specific treatment was carried out in these
patients before the appearance of collapse. Clinical progression was defined
as the occurrence of pain. Radiographic progression was defined as an advance
in the Steinberg stage. Because collapse may be difficult to demonstrate in
hips with a small osteonecrotic lesion, all patients were evaluated with an
anteroposterior standard radiograph of the hip, an anteroposterior radiograph
of the hip with an ascendant x-ray beam at 30°, a frog-leg lateral
radiograph, and the false-profile view of the hip described by
Lequesne8.
Radiographs were made at the initial evaluation, annually, and at the time of
the most recent follow-up (average, fourteen years; range, ten to twenty
years).
Survival curves were calculated according to Kaplan-Meier survivorship
analysis and were compared with use of the log-rank test. To construct the
life table, the number of hips at each stage were followed and the number of
failures (a change of stage, collapse, or surgery) was determined for each
year. The first year started with the total number of hips in each stage at
the initial visit. When a failure occurred, the hip was censored and the
number at risk for the stage was calculated again for each successive year.
Multivariate analyses were performed with use of the Cox proportional-hazards
model to identify the independent factors with regard to radiographic signs of
progression and clinical progression and failure. The chi-square test was used
to analyze differences between groups of patients, with the level of
significance set at p < 0.05.
Fate of Hips with Asymptomatic Steinberg Stage-0 Osteonecrosis of the
Femoral Head at the Initial Visit
Fifty-six hips were classified as Steinberg stage 0 (indicating a hip at
risk, with normal findings on plain radiographs and magnetic resonance images)
at the time of the initial evaluation
(Table I). The mean duration of
clinical and radiographic follow-up for these hips was fourteen years (range,
ten to twenty years). Forty-seven (84%) of these fifty-six hips had
development of symptomatic osteonecrosis at the time of the most recent
follow-up evaluation (Fig. 1).
In twenty-eight of these forty-seven hips, a radiographic diagnosis was made
at an annual examination before the onset of symptoms. Eleven of these
twenty-eight hips had progressed to stage I, and seventeen had progressed to
stage II. All twenty-eight hips became symptomatic within three years after
the detection of radiographic signs of progression from stage 0.
The remaining nineteen patients (nineteen hips) presented with symptoms
before radiographic detection of progression of the lesion. Nine newly
symptomatic patients (nine hips) had Steinberg stage-I changes, and ten newly
symptomatic patients (ten hips) demonstrated Steinberg stage-II changes.
Radiographic signs of progression occurred in all forty-seven symptomatic
hips. Thirty-four hips progressed to collapse
(Fig. 2). Symptoms always
preceded collapse. The average time between the initial visit and collapse was
126 months for stage-0 hips. The average time between the onset of pain and
collapse was sixty-two months (range, sixteen to 116 months). The average time
between the initial visit and the onset of pain was sixty-four months (range,
twenty to 204 months). The thirty-four hips with collapse had symptomatic
progression that was sufficient to require surgery
(Fig. 3). Only twenty-two (39%)
of fifty-six hips had had no surgical treatment at the time of the most recent
follow-up; thirteen of these twenty-two hips had progressed to Steinberg stage
II, and nine remained at stage 0 at the time of the most recent follow-up
evaluation.
Fate of Hips with Asymptomatic Steinberg Stage-I Osteonecrosis of the
Femoral Head at the Initial Visit
Forty-two hips were classified as Steinberg stage I at the time of the
initial evaluation. Forty (95%) of these forty-two hips with asymptomatic
stage-I osteonecrosis at the time of the initial visit became symptomatic by
the time of the most recent follow-up (Fig.
1), and thirty-six hips (86%) demonstrated collapse after the
onset of symptoms (Fig. 2). The
mean duration of clinical and radiographic follow-up for the forty-two
patients (forty-two hips) was fourteen years (range, ten to twenty years). The
mean interval between the diagnosis and the first symptoms (mild pain) was
twenty-eight months (range, four to 156 months). Thirty-three hips became
symptomatic within three years, but the delay between the diagnosis and the
first symptoms (mild pain) was as long as thirteen years
(Fig. 1).
The onset of pain occurred when the disease was at radiographic stage I in
ten patients. In thirty patients, radiographic signs of progression to stage
II preceded the onset of the first symptoms. Overall, thirty-six (86%) of the
forty-two hips demonstrated collapse (Fig.
2). Collapse was always preceded by pain. The average interval
between the onset of pain and collapse was twelve months (range, three to
thirty-eight months). The average time between diagnosis at the initial visit
and collapse (Fig. 2) was forty
months (range, fourteen to ninety-six months). Symptoms increased after
collapse, and, at the time of the most recent follow-up evaluation, all
thirty-six hips had progressed to stage V and had deteriorated enough to
require surgery (Table I and
Fig. 3).
At the time of the most recent follow-up, only six hips had not undergone
surgical treatment: two hips (including one with stage-I and one with stage-II
disease) were asymptomatic, and four hips (all with stage-II disease) were
mildly symptomatic.
Fate of Hips with Asymptomatic Steinberg Stage-II Osteonecrosis of
the Femoral Head at the Initial Visit
Twenty-three hips in the study group initially had stage-II radiographic
abnormalities (Table I). All
became symptomatic within two years (Fig.
1). The average duration of clinical and radiographic follow-up
for this group was thirteen years (range, ten to twenty years). For all
twenty-three hips, collapse (Steinberg stage-IV involvement) occurred at an
average of eleven months (range, four to thirty-one months) after the onset of
pain (Fig. 2). After collapse,
all hips had radiographic signs of progression to stage V or VI. Twenty-one
hips had surgery at an average of forty-five months (range, twenty-six to
seventy-two months) after the onset of symptoms and at an average of fifteen
months (range, six to thirty-two months) after collapse
(Fig. 3). Only two hips with
stage-IV disease had had no surgical intervention at the time of the latest
follow-up.
Analysis of Radiographic and Clinical Progression of All
Hips Radiographic Signs of Progression
Progression in the stage of the lesion occurred regardless of the stage at
the time of the initial visit. At the time of the initial visit, fifty-six
hips were classified as stage 0, forty-two were classified as stage I, and
twenty-three were classified as stage II. At the time of the most recent
follow-up, only nine hips were still without evident osteonecrosis on magnetic
resonance imaging, one hip was graded as stage I, and eighteen were graded as
stage II; all of the other ninety-three hips had progressed to collapse
(Table I).
Progression in the size of the lesion was not observed. In the group of
forty-two hips that were designated as Steinberg stage I at the time of the
initial visit, the mean area of the lesion (expressed as the percentage of
involvement of the femoral head) was 36% (range, 8% to 48%) as determined with
magnetic resonance imaging. In the group of twenty-three hips that were
classified as stage II at the time of the initial visit, the mean area of the
lesion was 41% (range, 11% to 52%) as determined on anteroposterior
radiographs. In the group of fifty-six hips that were classified as stage 0 at
the time of the initial visit, forty-seven had development of osteonecrosis.
The size of the lesion was determined on magnetic resonance imaging or on
anteroposterior radiographs at the time of the diagnosis of osteonecrosis. The
mean area of the lesion was 43% (range, 13% to 49%). With the numbers
available, no significant changes in the mean size of the lesion were noted in
the groups from the beginning to the end of the follow-up period (the last
radiograph before surgery). Spontaneous resolution of the lesion or
spontaneous decrease in size was not observed even in hips that remained at
stage I or II as determined with magnetic resonance imaging at the time of the
most recent follow-up.
Clinical failure was defined as the need for surgical intervention because
of collapse and intractable pain (Fig.
3). At the time of the initial visit, all 121 hips were
asymptomatic. At the time of the most recent follow-up, only eleven hips
(including nine with stage-0 disease, one with stage-I disease, and one with
stage-II disease) were still asymptomatic. Ninety-one hips had deteriorated
enough clinically to require surgery. At the time of the last examination
before surgery, the mean Harris hip score for these ninety-one hips was 55
points (range, 23 to 68 points). Forty-two hips were treated with total hip
arthroplasty, twenty-three hips underwent a valgus femoral osteotomy, and
twenty-six hips had injection of cement into the femoral head. During this
latter procedure, low-viscosity cement is injected into the junction of the
living and necrotic bone and into the crescent line to buttress and restore
hip sphericity of the collapsed articular
cartilage9.
Risk Factors for Progression
The occurrence of pain in the asymptomatic hip was an important predictor
of collapse. Symptoms always preceded collapse; the mean time between the
onset of symptoms and collapse was thirty-five months (range, three to 116
months).
The stage of the lesion at the time of the initial visit was a risk factor
for progression to collapse. Hips that presented with stage-II disease
exhibited more rapid progression to collapse than did those with stage-I or
stage-0 disease (log-rank test, p < 0.01 and p < 0.001, respectively)
(Fig. 2). Hips that presented
with stage-I disease exhibited more rapid radiographic signs of collapse than
did hips with stage-0 involvement (p < 0.01). Kaplan-Meier analysis
(Fig. 2) showed that the
duration of survival before collapse was significantly longer for the
fifty-six hips that had stage-0 involvement at the time of the initial visit
than it was for the hips that had stage-I or stage-II involvement at the time
of the initial visit (p < 0.01).
Kaplan-Meier survivorship analysis, with any surgical intervention after
collapse considered as the end point of the natural history of the hip, showed
a significantly longer duration of clinical survival before surgery for hips
that had stage-0 involvement than for those that had stage-I and II
involvement at the time of the initial visit (log-rank test, p < 0.001)
(Fig. 3). The duration of
clinical survival was also significantly longer for hips that had stage-I
disease than for hips that had stage-II disease (log-rank test, p < 0.01).
However, the stage of the lesion at the time of the initial visit had a
limited effect on the final clinical outcome; of the 121 hips that were seen
at the time of the initial visit, ninety-three collapsed and ninety-one
deteriorated enough to require surgery.
When the lesion size was determined according to the system described by
Steinberg et al.7 on
radiographs or on magnetic resonance images (with grade A indicating mild
involvement, grade B indicating moderate involvement, and grade C indicating
severe involvement), Kaplan-Meier analysis demonstrated the influence of the
extent of involvement on the risk of collapse
(Fig. 4). Comparison of the
survivorship curves showed that stage-0, I, and II hips with mild involvement
had significantly longer durations of survival before collapse than did hips
with moderate or severe involvement (p < 0.01 for all; log-rank test).
However, the extent of the lesion had a limited effect on the final clinical
outcome because, of the 112 hips with evident osteonecrosis, all but
twenty-one progressed clinically to intractable pain and surgery. Furthermore,
no significant difference in the mean size of the lesion was noted between the
group of ninety-one hips that needed surgery and the group of twenty-one hips
with osteonecrosis that had had no surgery by the time of the most recent
follow-up (p > 0.05).
Eight patients had another risk factor (a history of steroid therapy or
alcohol abuse) associated with sickle cell disease. With the numbers
available, no significant relationship was found between these two risk
factors and an increased risk of clinical or radiographic failure (p > 0.50
for all).
For the patients with stage-I or stage-II osteonecrosis at the time of the
initial visit, age, gender and genotype, level of anemia, hematocrit,
frequency of painful crises, and duration of pain in the contralateral hip
were not found to be significantly associated with the risk of progression to
symptoms and collapse, with the numbers available, on either univariate or
multivariate analyses (p > 0.50). The stage of the contralateral hip and
the amount of head involvement were analyzed to determine the risk of
progression as seen radiographically for patients with stage-I or II
osteonecrosis. With use of the chi-square test with Yates corrections and a
discriminator level of collapse or no collapse in the contralateral,
symptomatic hip at the time of the initial visit, patients with collapse in
the contralateral, symptomatic hip at the time of the initial visit had a
greater likelihood (p = 0.032) of occurrence of symptoms in the nonsymptomatic
hip within one year than did patients without collapse in the contralateral,
symptomatic hip at the time of the initial visit.
For the fifty-six patients with stage-0 involvement at the time of the
initial visit, age, gender and genotype, level of anemia, hematocrit, and
frequency of painful crises were not found to be significantly associated with
an imminent risk of the occurrence of osteonecrosis (stage-I or II
involvement) on univariate or multivariate analyses (p > 0.50 for all).
However, for patients with stage-0 involvement, three factors were found to
increase the imminent risk of the occurrence of osteonecrosis (stage-I or II
involvement): the occurrence of collapse in the contralateral hip, the
occurrence of any surgical procedure (either orthopaedic or non-orthopaedic),
or the occurrence of pregnancy in women. Patients with one of these three risk
factors had a greater likelihood (p = 0.024) of rapid onset of osteonecrosis
(within less than two years).
Aclinical dilemma that commonly arises in the assessment of an asymptomatic
hip at risk for osteonecrosis of the femoral head in the presence of a
symptomatic contralateral hip is whether to treat or merely observe the
asymptomatic
hip10-12.
In the present study, spontaneous resolution of osteonecrosis of the femoral
head13 was not
observed in the asymptomatic hips. Pain developed in 110 previously
asymptomatic hips (91%), and collapse occurred in ninety-three hips (77%) by
the time of the most recent follow-up.
The first important finding of our study is that pain developed within
three years after a magnetic resonance imaging diagnosis in 95% of the hips
with stage-I involvement and within two years for all of the hips with
stage-II involvement. This finding suggests that clinical progression of
osteonecrosis of the femoral head in patients with sickle cell disease is more
frequent and more rapid than has been widely reported in association with
asymptomatic nontraumatic osteonecrosis due to other
causes14-19,
particularly for stage-I hips. In several combined studies involving
eighty-three hips with asymptomatic stage-I osteonecrosis of the femoral head
associated with steroid use, alcohol abuse, or an idiopathic
etiology14-19,
only twenty-seven (33%) progressed to symptoms after 6.5 to thirty-six months
of follow-up (Table II).
The second important finding of this study is that ninety-three (77%) of
the 121 hips had collapsed by the time of the most recent follow-up. Our
results suggest that in patients with sickle cell disease, the rate of
radiographic signs of progression of asymptomatic stage-I and II osteonecrosis
may be also somewhat more rapid and more frequent than previously assumed in
association with osteonecrosis related to steroid use or alcohol
abuse14-19.
The present study confirms that small asymptomatic lesions progress more
slowly than large asymptomatic lesions do, but, as previously reported in
another study5 of
patients with osteonecrosis of the femoral head associated with other risk
factors (corticosteroid use or alcohol abuse), hips with a small area of
osteonecrosis collapse in a large percentage of patients; thus, patients with
very small lesions should be followed carefully over a long period of
time.
The unfavorable outcome for most patients with an asymptomatic hip and
osteonecrosis of the femoral head in the contralateral hip related to sickle
cell disease suggests that careful screening of the asymptomatic hip should be
performed on a regular basis. We recommend that the asymptomatic hip be
screened at six-month intervals after presentation of the symptomatic hip,
particularly when the volume of the osteonecrosis is large and when there has
been collapse of the contralateral hip, because these two factors have been
found to be associated with the rate of clinical and radiographic progression
in the asymptomatic hip in patients with osteonecrosis of the femoral head
associated with corticosteroid use or alcohol
abuse20. We also
recommend evaluating the patient as soon as possible after the onset of pain
because symptoms always preceded collapse. The intervals between the onset of
pain and collapse may be as short as three months, and in the present study
the mean time between pain and collapse was only thirty-five months.
Discussion of alternatives for the treatment of asymptomatic osteonecrosis
of the femoral head in patients with sickle cell disease is beyond the scope
of this report. However, our finding that most of the asymptomatic hips with
stage-I or II osteonecrosis of the femoral head collapsed within three years
is an argument for considering a prophylactic surgical procedure while the
patient is undergoing surgical intervention for the symptomatic, contralateral
hip. This prophylactic procedure is particularly important for these patients
because anesthesia and transfusion pose substantial risks for these patients
and because there is a high prevalence of complications following total hip
arthroplasty in patients with sickle cell disease. Since 2000, we have
performed percutaneous autologous bone-marrow
grafting21 in the
asymptomatic hip at the time we are performing surgery on the symptomatic
contralateral hip. Other operative
interventions22,23
for the early treatment of osteonecrosis, such as core decompression,
osteotomy, or grafting, may of course be considered for these patients.
Hips without evidence of osteonecrosis on magnetic resonance imaging at the
time of the initial visit (stage-0 hips) should really be considered as
"hips at risk for osteonecrosis" in patients with sickle cell
disease. In a series of forty-six patients with unilateral symptomatic
osteonecrosis who had received steroid treatment or who had a history of
alcoholism, the authors reported that the magnetic resonance imaging findings
remained normal for an average of 8.6 years in the contralateral, asymptomatic
hip24. In contrast,
in our series of patients with sickle cell disease, thirty-three (59%) of the
fifty-six asymptomatic hips with stage-0 disease had evidence of osteonecrosis
on magnetic resonance imaging within nine years and forty-seven (84%) had
osteonecrosis after a mean duration of follow-up of fourteen years. At the
present time, we do not have sufficient data to recommend early surgical
intervention for asymptomatic hips with stage-0 involvement; however, frequent
evaluations should be performed, particularly in patients with collapse of the
contralateral hip, for at least two years following a surgical procedure that
was performed with the patient under general anesthesia or following
pregnancy25.
?
Hernigou P, Bachir D, Galacteros F. The
natural history of symptomatic osteonecrosis in adults with sickle-cell
disease. J Bone Joint Surg Am.2003;85:
500-4.85500
2003
[PubMed]
Hernigou P, Galacteros F, Bachir D,
Goutallier D. Deformities of the hip in adults who have sickle-cell disease
and had avascular necrosis in childhood. A natural history of fifty-two
patients. J Bone Joint Surg Am.1991;73:
81-92.7381
1991
[PubMed]
Milner PF, Kraus AP, Sebes JI, Sleeper
LA, Dukes KA, Embury SH, Bellevue R, Koshy M, Moohr JW, Smith J. Sickle cell
disease as a cause of osteonecrosis of the femoral head. N Engl J
Med.1991;325:
1476-81.3251476
1991
[CrossRef]
Aaron R, Lennox D, Stulberg B. The
natural history of osteonecrosis of the femoral head. In: Urbaniak JR, Jones
JP, editors. Osteonecrosis: etiology, diagnosis, and treatment.
Rosemont, IL: American Academy of Orthopaedic Surgeons; 1997. p
261-5.261
1997
Hernigou P, Poignard A, Nogier A,
Manicom O. Fate of very small asymptomatic stage-I osteonecrotic lesions of
the hip. J Bone Joint Surg Am.2004;86:
2589-93.862589
2004
[PubMed]
Jergesen HE, Khan AS. The natural
history of untreated asymptomatic hips in patients who have non-traumatic
osteonecrosis. J Bone Joint Surg Am.1997;
79: 359-63.79359
1997
[PubMed]
Steinberg ME, Hayken GD, Steinberg DR. A
quantitative system for staging avascular necrosis. J Bone Joint Surg
Br.1995;77:
34-41.7734
1995
Lequesne M. Les coxarthroses. Notions
statistiques et étiologiques. [Coxarthrosis, statistical and
etiological concepts]. Rev Prat.1974;24: 4261,
4265-6, 4269-70. French.244261
1974
[PubMed]
Hernigou P, Bachir D, Galacteros F.
Avascular necrosis of the femoral head in sickle cell disease. Treatment of
collapse by the injection of acrylic cement. J Bone Joint Surg
Br.1993;75:
875-80.75875
1993
Ohzono K, Saito M, Takaoka K, Ono K,
Saito S, Nishina T, Kadowaki T. Natural history of nontraumatic avascular
necrosis of the femoral head. J Bone Joint Surg Br.1991;73:
68-72.7368
1991
[PubMed]
Mont MA, Hungerford DS. Non-traumatic
avascular necrosis of the femoral head. J Bone Joint Surg Am.1995;77:
459-74.77459
1995
[PubMed]
Bradway JK, Morrey BF. The natural
history of the silent hip in bilateral atraumatic osteonecrosis. J
Arthroplasty.1993;8:
383-7.8383
1993
[CrossRef]
Cheng EY, Thongtrangan I, Laorr A, Saleh
KJ. Spontaneous resolution of osteonecrosis of the femoral head. J Bone
Joint Surg Am.2004;86:
2594-9.862594
2004
Stulberg BN, Davis AW, Bauer TW, Levine
M, Easley K. Osteonecrosis of the femoral head. A prospective randomized
treatment protocol. Clin Orthop Relat Res.1991;268:
140-51.268140
1991
[PubMed]
Davidson JL, Coogan PG, Gunneson EE,
Urbaniak JR. The asymptomatic contralateral hip in osteonecrosis of the
femoral head. In: Urbaniak JR, Jones JP, editors. Osteonecrosis:
etiology, diagnosis, and treatment. Rosemont, IL: American Academy of
Orthopaedic Surgeons; 1997. p
231-40.231
1997
Kopecky KK, Braunstein EM, Brandt KD,
Filo RS, Leapman SB, Capello WN, Klatte EC. Apparent avascular necrosis of the
hip: appearance and spontaneous resolution of MR findings in renal allograft
recipients. Radiology.1991;179:
523-7.179523
1991
[PubMed]
Takatori Y, Kokubo T, Ninomiya S,
Nakamura S, Morimoto S, Kusaba I. Avascular necrosis of the femoral head.
Natural history and magnetic resonance imaging. J Bone Joint Surg
Br.1993;75:
217-21.75217
1993
Fordyce MJ, Solomon L. Early detection
of avascular necrosis of the femoral head by MRI. J Bone Joint Surg
Br.1993;75:
365-7.75365
1993
Mulliken BD, Renfrew DL, Brand RA,
Whitten CG. Prevalence of previously undetected osteonecrosis of the femoral
head in renal transplant recipients. Radiology.1994;192:
831-4.192831
1994
[PubMed]
Hernigou P, Lambotte JC. Bilateral hip
osteonecrosis: influence of hip size on outcome. Ann Rheum Dis.2000;59:
817-21.59817
2000
[PubMed][CrossRef]
Hernigou P, Beaujean F. Treatment of
osteonecrosis with autologous bone marrow grafting. Clin Orthop Relat
Res.2002;405:
14-23.40514
2002
[CrossRef]
Mont MA, Carbone JJ, Fairbank AC. Core
decompression versus nonoperative management for osteonecrosis of the hip.
Clin Orthop Relat Res.1996;324:
169-78.324169
1996
[PubMed][CrossRef]
Steinberg ME, Larcom PG, Strafford B,
Hosick WB, Corces A, Bands RE, Hartman KE. Core decompression with bone
grafting for osteonecrosis of the femoral head. Clin Orthop Relat
Res.2001;386:
71-8.38671
2001
[CrossRef]
Sugano N, Nishii T, Shibuya T, Nakata K,
Masuhara K, Takaoka K. Contralateral hip in patients with unilateral
nontraumatic osteonecrosis of the femoral head. Clin Orthop Relat
Res.1997;334:
85-90.33485
1997
Montella BJ, Nunley JA, Urbaniak JR.
Osteonecrosis of the femoral head associated with pregnancy. A preliminary
report. J Bone Joint Surg Am.1999;
81: 790-8.81790
1999
[PubMed][CrossRef]