Nontraumatic Osteonecrosis of The Femoral Head: Ten Years Later

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COPYRIGHT © 2006 BY THE JOURNAL OF BONE AND JOINT SURGERY, INCORPORATED
Current Concepts Review

Nontraumatic Osteonecrosis of
the Femoral Head: Ten Years Later
BY MICHAEL A. MONT, MD, LYNNE C. JONES, PHD, AND DAVID S. HUNGERFORD, MD
Investigation performed at the Center for Joint Preservation and Reconstruction, Rubin Institute for Advanced Orthopedics,
Sinai Hospital of Baltimore, and the Department of Orthopaedic Surgery,
The Johns Hopkins University School of Medicine, Good Samaritan Hospital, Baltimore, Maryland
➤ The etiology of osteonecrosis of the hip may have a genetic basis. The interaction between certain risk factors
and a genetic predisposition may determine whether this disease will develop in a particular individual.
➤ The rationale for use of joint-sparing procedures in the treatment of this disease is based on radiographic mea-
surements and findings with other imaging modalities.
➤ Early diagnosis and intervention prior to collapse of the femoral head is key to a successful outcome of joint-
preserving procedures.
➤ The results of joint-preserving procedures are less satisfactory than the results of total hip arthroplasty for fem-
oral heads that have already collapsed.
➤ New pharmacological measures as well as the use of growth and differentiation factors for the prevention and
treatment of this disease may eventually alter our treatment approach, but it is necessary to await results of
clinical research with long-term follow-up of these patients.
It has been ten years since our previous Current Concepts Re- Etiology, Pathogenesis, and Pathology
view on osteonecrosis of the femoral head was published1. The pathophysiology of osteonecrosis of the femoral head has
Despite recent outstanding reviews on the subject2-4, there not been completely elucidated. Whereas some cases of the dis-
continues to be a lack of consensus concerning the pathogene- ease clearly have a direct cause (trauma, radiation, or Caisson
sis and treatment of this disease. Even the name osteonecrosis is disease), the pathophysiology is uncertain for most cases. Multi-
now more accepted and more commonly used than the previ- ple investigators have postulated vascular impairment, altered
ous name, avascular necrosis. In this review, we will update bone-cell physiology, and other theories1-4,7,39. In addition, sev-
concepts concerning etiologies and nonoperative and opera- eral comorbidities have been linked to this disease1-4,7,40-43.
tive treatment methods that were discussed in the previous re- One of the most common risk factors for osteonecrosis
views. This article is based almost exclusively on peer-reviewed of the femoral head is use of corticosteroids41,44-61, but the ex-
studies published from 1995 to the present, and it is intended to tent of use that constitutes a risk is still under debate. Al-
provide background for an evidence-based approach to treat- though many patients receiving corticosteroids have at least
ment of this disease. one other confounding factor, multivariate analysis has sug-
Over the past ten years, multiple studies have demon- gested that corticosteroid use, especially in high doses, is an
strated excellent rates of success of total hip arthroplasties in pa- independent variable. Dosages typically considered to be asso-
tients with osteonecrosis5-38. The indications for joint-preserving ciated with the disease are >2 g of prednisone, or its equiva-
procedures seem less clear as justification for their use requires lent, within a period of two to three months. Lower dosages
further evidence of positive results from clinical studies. For are not typically related to osteonecrosis of the femoral head,
patients in whom joint-preserving procedures are indicated, and reports of an association with such doses are often anec-
early diagnosis is essential. For the purpose of this review, the dotal and involve patients with multiple risk factors, such as
lesions will be broadly described as precollapse or postcollapse alcohol use or smoking45,60,62-64. Inoue et al.41 reported that os-
with occasional references to the size of the lesion, amount of teonecrosis of the femoral head developed in eighteen of 287
head depression, or acetabular involvement. renal transplant recipients treated orally with ≥25.0 mg/day of
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prednisolone. In a study of twenty-two patients diagnosed creased risk for current smokers (relative odds = 4.7); however,
with osteonecrosis of the femoral head, Koo et al.51 found that a cumulative effect of smoking was evident only in association
the total dose of corticosteroids used until osteonecrosis was with twenty pack-years or more. Matsuo et al.63 also found an
detected with magnetic resonance imaging ranged from 1800 increased risk for current smokers (relative risk = 3.9). Various
to 15,505 mg (mean, 5928 mg) of prednisolone or its equi- studies have demonstrated that smoking inhibits osteogenesis
valent. Various reports have described a corticosteroid dose- or fracture-healing64-66.
related risk of osteonecrosis of the femoral head in patients Osteonecrosis of the femoral head is believed to be a mul-
with severe acute respiratory syndrome (SARS)47,50,55. Griffith tifactorial disease that is associated in some cases with both a
et al.47 found that twelve (5%) of 254 patients with SARS had genetic predilection and exposure to certain risk factors. These
evidence of osteonecrosis of the femoral head and that the cu- risk factors include corticosteroid use, alcohol intake, smoking,
mulative prednisolone-equivalent dose was the most impor- and various chronic diseases (renal disease, hematological dis-
tant risk factor, with the risk being 0.6% for patients receiving ease, inflammatory bowel disease, post-organ transplantation,
a dose of <3 g and 13% for those receiving a dose of >3 g. hypertension, and gout)1-4,39-44,52-54,57,58,62,63.
The risk period for the development of osteonecrosis of Patients with inherited coagulation disorders may be at
the femoral head following corticosteroid therapy has been risk for the development of osteonecrosis of the femoral head.
more exactly defined. Using magnetic resonance imaging, Studies have shown an association with thrombophilia (an in-
Sakamoto et al.56 prospectively evaluated the femoral heads in creased likelihood of blood clots) and hypofibrinolysis (a de-
forty-eight patients (ninety-six hips) receiving high-dose cor- creased ability to lyse blood clots)3,4,39,40,42,43,67-80. We analyzed
ticosteroids for various autoimmune-related disorders. Ab- nine coagulation factors and found at least one coagulation
normalities were found in thirty-one hips (32%). The initial factor abnormality in thirty-seven (82%) of forty-five pa-
necrotic changes were seen as well-demarcated, band-like tients with osteonecrosis of the femoral head compared with
zones at a mean of 3.6 months (maximum, twelve months) af- 30% of controls (p < 0.0001)74. Two or more abnormalities
ter initiation of the corticosteroid treatment. Fink et al.59, in a were identified in twenty-one patients (47%) compared with
prospective study of forty-three patients receiving corticoste- 2.5% of controls (p < 0.0001). Glueck et al.70 found a high
roids while undergoing renal transplantation, observed that prevalence of plasminogen activator inhibitor-1 coagulation
osteonecrosis of the femoral head occurred in six hip joints of abnormalities in a study of fifty-nine patients with osteone-
four patients (9%) within three months after the transplanta- crosis of the femoral head. Because some of these coagulation
tion. Magnetic resonance imaging performed twelve months alterations may be the result of autosomal dominant disor-
after transplantation revealed no additional lesions. Koo et ders, it may be possible to screen individuals at risk.
al.51 found the period from the start of corticosteroid treat- Liu et al.81 identified three families with an autosomal
ment to the diagnosis of osteonecrosis to range from one to dominant inheritance of osteonecrosis of the femoral head
sixteen months (mean, 5.3 months), with twenty-one of and mapped the chromosomal position of a collagen type-II
twenty-two patients diagnosed within twelve months. Thus, gene (COL2A1 gene) mutation. Osteonecrosis of the femoral
for the majority of patients receiving corticosteroids, the risk head has also been associated with certain genetic polymor-
period for the development of osteonecrosis of the femoral phisms such as alcohol-metabolizing enzymes and the drug-
head is twelve months or less. transport protein P-glycoprotein48,78,82-86. The importance of
Alcohol use is another important risk factor44,62,63. In a these findings is that genetic screening of families with os-
retrospective study comparing 118 patients with noncorticos- teonecrosis of the femoral head could be used to identify car-
teroid-associated osteonecrosis of the femoral head with 236 riers before the onset of clinical symptoms. This might allow
control patients, Hirota et al.62 found a higher risk of osteone- the initiation of measures that could delay disease progression
crosis of the femoral head developing in occasional drinkers and may have implications for pharmacological treatment. In
(<8 mL of alcohol once a week, but not daily) (relative odds = addition, the pathological condition associated with the defect
3.2) and in regular drinkers (≥8 mL of alcohol daily) (relative could be treated, thereby possibly eliminating the risk factor.
odds = 13.1) than in controls. They also found a significant For example, a patient with familial hyperlipidemia could be
dose-response relationship (p < 0.001), with the relative odds treated with lipid-lowering agents and be regularly screened
for current drinkers being 2.8, 9.4, and 14.8 in association with magnetic resonance imaging to enable an early diagnosis,
with ethanol intakes of <320, 320 to 799, and ≥800 g/wk, re- which could lead to the most optimal treatment.
spectively. Matsuo et al.63 compared 112 patients with osteone- Corticosteroids and alcohol may also have an effect on
crosis of the femoral head with 168 control patients and found osteoblast differentiation48,49,84,87. While laboratory studies by
an elevated risk for regular drinkers (>8 mL of alcohol every Wang et al.57,58 showed that corticosteroids may direct bone-
day) (relative risk = 7.8). They also reported a clear dose-re- marrow stromal cells into the adipocytic pathway as opposed
sponse relationship, with relative risks of 3.3, 9.8, and 17.9 for to the osteoblastic pathway, a clinical study has also shown de-
current drinkers consuming <400, 400 to 1000, and ≥1000 creased osteogenic differentiation in cells harvested from pa-
mL/wk of alcohol, respectively. tients with corticosteroid or alcohol-associated osteonecrosis
Smoking has been implicated as a risk factor for os- of the femoral head87.
teonecrosis of the femoral head62-64. Hirota et al.62 found an in- Patients infected with human immunodeficiency virus
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(HIV) are at increased risk for the development of osteonecrosis

of the femoral head88-96. It is unclear whether the virus itself is re-
sponsible or the treatments (with antiretroviral drugs such as
protease inhibitors, corticosteroids, or other chemotherapeutic
agents) are the pathogenic agents. In a study of eight patients
with HIV infection, Blacksin et al.88 found that osteonecrosis of
the femoral head did not appear to be directly related to HIV,
but rather to the use of corticosteroid treatment. Miller et al.94
found osteonecrosis of the femoral head in fifteen (4.4%) of 339
HIV-infected adults and no hip lesions in 118 age and gender-
matched HIV-negative volunteers. The hip lesions occurred
more frequently in individuals who used corticosteroids, lipid-
lowering agents, or testosterone. Several studies have impli-
cated antiretroviral therapy as the most important pathogenic
agent89,91,92,95. In contradistinction to these studies, Ries et al.96
identified four patients with HIV and osteonecrosis of the fem-
oral head who had no other known risk factors, a finding that
suggests that HIV infection itself may be a unique risk factor.
Although osteonecrosis of the femoral head is a rare
complication of pregnancy, several cases have been docu-
mented in the literature97-100. These patients typically have no
other risk factors. Montella et al.98 reported on thirteen pa-
tients (seventeen hips) in whom osteonecrosis of the femoral
head developed during pregnancy or in the first postpartum
month. The patients were mostly primigravid (eleven of thir-
teen patients), with “a small body frame and a relatively large
weight gain.” Many of these cases were initially misdiagnosed
as transient osteoporosis of the hip.
Factors Affecting Treatment Fig. 1

Radiographic Staging A: Sagittal radiograph of a femoral head, delineating a cres-
Treatment algorithms for osteonecrosis of the femoral head are cent sign (arrows) that is the result of a subchondral fracture
based on staging of the lesion. Numerous staging systems have and indicates biomechanical compromise. B: Sagittally sliced
been utilized to describe the radiographic extent of the disease. gross section of a femoral head obtained at surgery, delineat-
Each system has limitations, and no single system has been uni- ing a crescent sign (arrows).
versally accepted for use alone as a guide to treatment.
Most authors have reported routinely utilizing four essen-
tial radiographic findings when formulating a treatment plan. fined. These lesions can be detected only with magnetic reso-
These findings, which have been corroborated in peer-reviewed nance imaging (Fig. 2). Steinberg et al.111 described a method
studies of outcomes of various treatment methods3,4,74,101-111, in- for assessing the amount of femoral head involvement by
clude (1) evidence that the lesion is either precollapse or post- these lesions with magnetic resonance imaging. Cherian et
collapse, (2) the size of the necrotic segment, (3) the amount of al.113 used radiographs and magnetic resonance imaging to
femoral head depression, and (4) acetabular involvement with evaluate thirty-nine hips in twenty-five patients who had
signs of osteoarthritis. Stage-I or II disease according to the grading system of the As-
Integrity of femoral head: Collapse of the femoral head is sociation Research Circulation Osseous (ARCO). They found
a consequence of mechanical failure. While large areas of col- that various methods for measuring the sizes of lesions (calcu-
lapse can be recognized as a change in the contour of the fem- lation of an index of necrotic extent and estimation of the per-
oral head, the so-called crescent sign is an earlier indicator of cent involvement) could be used with confidence as they were
this failure (Fig. 1). When collapse is present, it is probable highly reliable and reproducible. Their analysis of the grades
that the patient will eventually require a total hip replacement. assigned independently on two separate occasions by three
Size of lesion: Many studies have shown that the size of observers with different medical specialty backgrounds and
the lesion, regardless of the treatment method, is predictive of experience resulted in correlation coefficients that demon-
outcome101. The size of a radiographically evident lesion can strated substantial agreement for all sizes of lesions.
be estimated on the basis of combined necrotic angle mea- Femoral head depression: A change in the femoral head
surements112. When a patient has early disease, the lesion is not contour of >2 mm has been shown to confer a worse progno-
radiographically evident or the margins may be poorly de- sis. In a cross-sectional study of fifty-two patients (sixty-eight
1120
Fig. 2
T1-weighted magnetic resonance images showing a small (A) and a large (B) osteone-
crotic lesion of the femoral head. The arrows denote the lesions.
hips) who had had a core decompression for the treatment of would be more appropriate. Arthroscopy can also be utilized
Ficat and Arlet Stage-III disease114 and had been followed for a to evaluate lesions120-124. Ruch et al. used arthroscopy to study
mean of twelve years (range, four to eighteen years)109, eigh- fifty-two hips in forty-six patients with osteonecrosis of the
teen (41%) of forty-four hips with Steinberg Stage-III dis- femoral head that had been staged prospectively with radio-
ease111 (no head depression and the presence of a crescent sign) graphs and magnetic resonance imaging123. In eighteen hips in
required a total hip replacement whereas twenty-two (92%) of which loss of integrity of the femoral head had been noted on
twenty-four hips with Steinberg Stage-IV disease (head de- plain radiographs, arthroscopy of the hip revealed osteochon-
pression) underwent arthroplasty. Soucacos et al.115 reported dral degeneration not detected by magnetic resonance imag-
that, in a study of 184 hips (152 patients) followed for one to ing. McCarthy et al. used arthroscopy to study seven patients
ten years (mean, 4.7 years) after vascularized fibular grafting, and concluded that this procedure could enhance the accuracy
the best results were found in hips with Steinberg Stage-II dis- of staging122.
ease (no head depression), 95% of which had remained stable. Sometimes procedures (core decompression and bone-
In contrast, only 39% of the hips with femoral head depres- grafting) are performed without assessment of the femoral
sion had remained stable. head cartilage intraoperatively. Other tests might be consid-
Acetabular involvement: It is important to recognize ace- ered for further evaluation of such cases. For example, if one is
tabular involvement, as treatments directed at saving the fem- considering core decompression for what is believed to be a
oral head will be unsuccessful when the disease has progressed precollapse lesion, a computed tomography scan or tomo-
to involve the acetabular socket1,2,116-118. Moreover, there may be gram could be used to determine whether there is actually
evidence of degeneration of the acetabulum even when radio- femoral head collapse125.
graphs show normal findings and joint-space narrowing is
absent119. Patient-Specific Factors
It is essential to consider patient age, activity level, general
Intraoperative Assessment health, comorbidities, and life expectancy when planning treat-
Although most procedures used for the early treatment of os- ment. Physical examination assessing the amount of pain, limp,
teonecrosis of the femoral head are selected on the basis of and limitation of hip motion may also be utilized to determine
preoperative assessment, intraoperative findings are valuable the severity of joint involvement. Systemic disease or a short life
for confirming staging and they may play a role in treatment expectancy may preclude a major surgical procedure. Similar le-
choice. For example, one might have planned a bone-grafting sions may not be treated in the same way in two patients with
procedure on the basis of the radiographic findings, but an in- different ages and activity levels. For example, a hip with femo-
traoperative finding of substantial damage to the cartilage of ral head collapse and no acetabular involvement might be best
the femoral head would indicate that a total hip replacement treated with a bone graft in a healthy twenty-one-year-old but
1121
the same pathological condition would be best treated with a that are radiographically occult or not obvious on radiographs
total hip replacement in a seventy-six-year-old. Patients who are as it has been found to be 99% sensitive and 98% specific for
medically compromised may be more appropriately treated this disease128-134. Protocols have allowed rapid screening to re-
with one definitive procedure (total hip replacement) rather duce the cost and time of magnetic resonance imaging, making
than with procedures that may be only temporizing. It might be sequential, temporal screenings feasible. When limited, rapidly
intuitive to think that patients with certain diagnoses and risk performed magnetic resonance imaging and full screening with
factors (corticosteroid treatment or systemic lupus erythemato- magnetic resonance imaging were both used to diagnose lesions
sus, for example) would have worse outcomes of treatment. and to determine their size, the two studies showed agreement
However, treatment success rates have been more closely corre- for 177 (98.9%) of 179 hips132. May and Disler134 found that the
lated with the structural integrity of the femoral head than with results of a rapid screening protocol (an imaging time of less
demographic factors. than one minute) were similar to those of the routine protocol
The duration of symptoms has been found to influence the (an imaging time of more than seven minutes) for patients who
outcomes of preservative treatment. In a previous study of forty- had had findings suspicious for radiographically occult os-
five Ficat and Arlet Stage-I and II hips in which core decompress- teonecrosis of the femoral head.
ion was done by drilling multiple times with a percutaneous Bone-scanning has been reported to be insensitive for the
small-diameter pin, one of us (M.A.M.) and colleagues126 re- diagnosis of osteonecrosis of the femoral head135-140. Scheiber et
ported a mean preoperative duration of symptoms of six months al.139 compared planar three-phase bone scans that had been
for patients who had a successful outcome compared with eleven made with a high-resolution parallel-hole collimator with mag-
months for those who had a poor outcome. Beaule et al.127 ob- netic resonance images of 120 patients with nontraumatic hip
served a better prognosis for patients who had experienced symp- pain and twenty-three individuals in a control group. All pa-
toms for less than twelve months before treatment with limited tients had undergone the magnetic resonance imaging scan
femoral head resurfacing than for patients who had had symp- within two months of the bone scan. Of thirty hips with a nor-
toms for more than twelve months before such treatment. mal appearing scan, twenty-two were found to have osteone-
crosis of the femoral head on the magnetic resonance image.
Diagnostic Methods The authors concluded that bone-scanning is not indicated for
If standard anteroposterior and frog-leg lateral radiographs the diagnosis of possible involvement of the contralateral hip in
show obvious osteonecrosis of the femoral head, it is not neces- patients with osteonecrosis of the femoral head. Figure 3 illus-
sary to perform magnetic resonance imaging. However, mag- trates the lack of sensitivity of bone-scanning for diagnosing os-
netic resonance imaging is the best diagnostic method for cases teonecrosis of the femoral head.
Fig. 3
Bone-scanning lacks sensitivity for diagnosing osteonecrotic lesions of the femoral head. A: Early signs of an
osteonecrotic lesion (arrow) are shown on the plain radiograph. B: A normal or “cold” bone scan of both hips.
C: Evidence of a subchondral osteonecrotic lesion (arrow) is seen on the magnetic resonance image.
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Nonoperative Treatment studies by Wang et al.57,58, who analyzed the ability of lovastatin
Most methods of nonoperative treatment have involved re- to prevent corticosteroid-induced adipogenesis in vitro as well
stricted weight-bearing (with various modalities such as a as its effects on adipogenesis and osteonecrosis of the femoral
cane, crutch, walker, or two crutches) on the basis of the belief head in vivo in chickens. These studies suggested that, in pa-
that this slows the progression of the disease so that ultimately, tients with systemic lupus erythematosus, osteonecrosis of the
femoral head-preserving procedures can be performed. How- femoral head may develop as a result of a physiological diver-
ever, >80% of affected hips progress to femoral head collapse sion of mesenchymal stem cells toward an adipocytic as op-
and arthritis by four years after the diagnosis141. Disease diag- posed to an osteoblastic lineage. Consequently, treatment with
nosed in the early stages (before femoral head collapse) may lovastatin may prevent osteonecrosis by preventing the effects
be amenable to newer nonoperative treatment modalities, but of the disease on the diversion of normal osteoblastic cellular
the exact stages at which specific interventions may be suc- differentiation. Pritchett reported that, at a mean of 7.5 years
cessful have not been established. (minimum, five years), osteonecrosis of the femoral head had
Published reports now appear to justify nonoperative developed in only three (1%) of 284 patients who were taking
treatment of small precollapse lesions that are asymptomatic, high-dose corticosteroids as well as various statin drugs (lipid-
which may have a better natural history142-146. These lesions are clearing agents that dramatically reduce lipid levels)148. That
often diagnosed in the contralateral hip after evaluation of a prevalence is much lower than the 3% to 20% prevalence re-
symptomatic hip. Jergesen and Khan found that fourteen of ported for patients receiving high-dose corticosteroids with-
nineteen asymptomatic hips with untreated osteonecrosis of out statins3,43,44. Thus, statins might offer protection against
the femoral head had progression of the disease; nine had it this disease when corticosteroid treatment is necessary.
within five years and five, more than five years after the Glueck et al.71 used the anabolic steroid stanozolol (6
diagnosis143. In a prospective study of forty asymptomatic hips mg/day) to treat four patients who had hypofibrinolysis asso-
with a small early-stage lesion that was not treated, Hernigou ciated with a high level of plasminogen activator activity and
et al.144 reported that thirty-five (88%) became symptomatic one patient who had a high level of lipoprotein in the serum.
and twenty-nine (73%) demonstrated collapse at a minimum All five patients showed a decrease of symptoms at one year
of ten years (mean, eleven years) after the diagnosis. following treatment. In another study, Glueck et al.72 used
There is evidence that certain small lesions may sponta- enoxaparin (60 mg/day for twelve weeks) to treat patients who
neously heal. Cheng et al.147 prospectively studied thirty hips had thrombophilic or hypofibrinolytic disorders and early
and found that three had spontaneous resolution. Factors that stages of osteonecrosis of the femoral head. At two years,
appeared to be related to resolution were early, asymptomatic thirty-one (89%) of thirty-five hips had not required surgery
disease and a small lesion. In a study by Yoshida et al.61, and still had Ficat and Arlet Stage-I or Stage-II disease as as-
twenty-four asymptomatic, radiographically normal hips that sessed radiographically.
were found to have osteonecrosis of the femoral head on mag- The effects of the prostacyclin derivative iloprost, used
netic resonance imaging in thirteen patients with systemic lu- as a vasodilator, have been studied in patients with osteo-
pus erythematosus were followed with magnetic resonance necrosis of the femoral head and bone marrow edema syn-
imaging for twelve to ninety-five months (mean, fifty-one drome149,150. Seventeen patients with early-stage osteonecrosis
months). Fifteen hips improved (>15% reduction in the vol- of the femoral head all had clinical and radiographic improve-
ume of necrosis) during the observation period, and all hips ments at one year after treatment with this agent.
in which the volume of the necrotic area had been <25% Bisphosphonates have shown promise in small case
showed a time-dependent decrease in the size of the lesion. series151-154. These agents, which inhibit osteoclast activity and
A meta-analysis of the outcomes of protected weight- thus curtail bone resorption, could theoretically slow progres-
bearing in 819 patients demonstrated a failure rate of >80% at sion of the disease on the basis of the hypothesis that increased
a mean of thirty-four months141. As the majority of patients re- resorption contributes to collapse of the femoral head. Three
quired a total hip replacement in a short period of time, the recent studies of rats155, canines156, and pigs157 have shown a re-
authors concluded that conservative treatment of osteonecro- duction in the prevalence of femoral head collapse after treat-
sis of the femoral head is not appropriate. ment with bisphosphonates. Recent clinical reports have
The use of pharmacological agents for the treatment of suggested that alendronate can be potentially beneficial for
osteonecrosis of the femoral head has received considerable patients with osteonecrosis of the femoral head. At an average
attention in recent years. The aim of these agents, which in- of one year (range, three months to five years) after treatment
clude lipid-lowering drugs, anticoagulants, vasodilators, and of sixty patients (100 hips) with this agent (10 mg/day), Agar-
bisphosphonates, is to address specific physiological risk fac- wala et al.151 found clinical improvement, with a reduction in
tors for osteonecrosis such as lipid emboli, adipocyte hyper- patient disability scores and only six patients (ten hips) requir-
trophy, venous thrombosis, increased intraosseous pressure, ing surgery. Similar findings were recently reported by Lai et
and resorption of bone. al.154, in a study of forty patients with Steinberg Stage-II or III
Patients with systemic lupus erythematosus and high se- osteonecrosis of the femoral head who were either treated
rum cholesterol and lipid levels have been treated with lipid- with alendronate (70 mg/day for twenty-five weeks) or as-
lowering agents46,148. This treatment is based on laboratory signed to a control group. At a minimum of twenty-four
1123
months, only two of the twenty-nine hips in the alendronate and for twenty-four (80%) of thirty Ficat and Arlet Stage-I
group had loss of femoral head integrity compared with nine- hips. The procedure was technically straightforward, and
teen of the twenty-five hips in the control group (p < 0.001). there were no operative complications. The technique was
One hip in the alendronate group and sixteen hips in the con- based on previous work by Kim et al., who reported a lower
trol group underwent total hip arthroplasty (p < 0.001). rate of radiographically determined femoral head collapse
Various external, biophysical, nonoperative modalities (14.3%) at three years compared with the rate following tradi-
have been utilized to treat osteonecrosis of the femoral head. tional core decompression techniques (45%; p = 0.03)172.
These include electromagnetic stimulation, extracorporeal Scully et al.184 compared core decompression (ninety-
shock-wave therapy158-160, and hyperbaric oxygen161-164. The ef- eight hips; seventy-two patients) with vascularized fibular
fectiveness of electromagnetic stimulation for treatment of os- grafting (614 hips; 480 patients). None of the eleven hips that
teonecrosis of the femoral head was evaluated in the 1980s and had Ficat and Arlet Stage-I disease needed a total hip replace-
1990s, with some studies showing early promising results114,165; ment after being treated with either regimen, whereas 65%
however, the evidence was not conclusive enough for approval (twenty-eight) of forty-three Stage-II hips treated with core
by the Food and Drug Administration. Extracorporeal shock- decompression and 89% (ninety-nine) of 111 Stage-II hips
wave therapy has been utilized in Europe for treatment of treated with vascularized fibular grafting had survived at fifty
early-stage disease. Wang et al.160 compared the results of such months. The rate of survival of the hips with Ficat and Arlet
therapy in twenty-three patients (twenty-nine hips) with the Stage-III disease was superior following vascularized fibular
results in a group treated with nonvascularized fibular graft- grafting (p < 0.0001). The authors concluded that the in-
ing. At a mean of twenty-five months, 79% of the shock-wave creased morbidity associated with vascularized fibular graft-
group had improved Harris hip scores compared with 29% of ing is justified by the associated delay in, or prevention of,
the group treated with nonvascularized fibular grafting. The articular collapse in hips that have large Ficat and Arlet Stage-
use of hyperbaric oxygen has had mixed results and is associ- II lesions or Stage-III disease. Since the results of the two pro-
ated with high cost and an extensive time commitment for pa- cedures were similar for the hips with Stage-I or early Stage-II
tients. In one study, hyperbaric oxygen prevented femoral disease, core decompression, which is technically easy and as-
head collapse in a vascular deprivation-induced osteonecrosis sociated with low morbidity, might be preferable at those
model in rats161. In another study, by Reis et al.162, sixteen hips stages. In summary, core decompression has the best results in
in twelve patients who had early-stage osteonecrosis of the hips with a small or medium-sized lesion, regardless of associ-
femoral head were treated with hyperbaric oxygen for 100 ated risk factors. For an excellent review of core decompres-
days. Thirteen of the sixteen hips had disappearance of abnor- sion, readers are referred to the recent report by Lieberman191.
malities on magnetic resonance imaging.
Osteotomy
Operative Treatment Osteotomies are used to move the segment of necrotic bone
Core Decompression away from the weight-bearing region. There are two general
In a meta-analysis of the outcomes of core decompression in types of osteotomies: angular intertrochanteric (varus and
1206 hips treated in twenty-four studies published prior to valgus) and rotational transtrochanteric20,108,192-214. Rotational
1995, the best results were observed following the treatment of osteotomies allow large degrees of translation of the osteone-
early-stage lesions141: 84% of patients with Ficat and Arlet Stage- crotic segment, as vthey employ a rotational femoral bone
I disease and 65% of patients with Stage-II disease had a suc- flap based on a vascular pedicle (the medial femoral circum-
cessful result. Similar results for precollapse disease were found flex artery). While rotational osteotomies may have a role in
in studies published since 1996 (see Appendix)103,105,107,109,126,165-191. the management of selected patients, they can be difficult to
In 2000, Castro and Barrack identified twenty-two studies of perform and they have a high potential for morbidity, includ-
core decompressions and compared them with eight studies in ing nonunion. Total hip replacements performed after an os-
which the patients had been treated nonoperatively167. Chi- teotomy are often technically more difficult than those done
square analysis showed the success rate of core decompression in patients with osteonecrosis of the femoral head who have
to be significantly higher than that of conservative treatment for never had an osteotomy. Several reports have described in-
hips with early-stage disease (p < 0.05). The authors concluded creased operative time, increased blood loss, technical diffi-
that large, multicenter, prospective, double-blinded studies of culties, and high infection rates in association with hip
patients randomized to either treatment method and then strat- replacements after osteotomy193,215,216.
ified by the stage, cause, and bilaterality of the disease were The results of seven studies of angular osteotomies,
needed. published since 1995, are summarized in the Appendix. Ancil-
One of us (M.A.M.) and colleagues described a core lary bone-grafting was also used in some of the studies198,208,217.
technique that involves drilling multiple times with a small Results were variable, with success rates ranging from 40% to
(3.2-mm-diameter) pin126. At a mean of two years (range, 96% at three to twenty-six years postoperatively. The angular
twenty to thirty-nine months) postoperatively, the clinical osteotomies usually had the best results in young active pa-
outcome was successful (a Harris hip score of >80 points and tients who were not taking corticosteroids, had unilateral in-
no additional surgery) for thirty-two (71%) of forty-five hips volvement with a good preoperative range of hip motion, and
1124
had a small lesion without femoral head collapse. through a core track in fifteen patients (seventeen hips). At a
The results of nine studies of rotational osteotomies are mean of fifty-three months (range, twenty-six to ninety-four
also summarized in the Appendix. These procedures are tech- months), fourteen hips showed a clinically successful result,
nically more demanding than angular osteotomies. For excel- with a Harris hip score of >80 points and no patient requiring
lent reviews of the indications, techniques, and results of conversion to a total hip replacement.
osteotomies, readers are referred to recent reports by one of us
(D.S.H.)116 as well as by Shannon and Trousdale193. Vascularized Bone-Grafting
The rationale for vascularized bone-grafting is that it allows de-
Nonvascularized Bone-Grafting compression, provides structural support, and restores a vascu-
Nonvascularized bone-grafting has numerous theoretical ad- lar supply that had been deficient or nonexistent for a long
vantages for the treatment of precollapse and early postcollapse period of time. There have been multiple published reports on
lesions when the articular cartilage is relatively undamaged. The the use of vascularized fibular and iliac grafts106,113,171,184,198,200,208,226,229-251.
procedure provides decompression of the femoral head, re- The results of these procedures are summarized in the Appendix.
moval of necrotic bone, and structural support and scaffolding Urbaniak et al.246 treated 103 osteonecrotic hips with a
to allow repair and remodeling of subchondral bone176,217-228. vascularized fibular graft and followed them for a minimum
Presently, there are three distinct approaches for introducing of five years. The best results were seen after the treatment of
bone graft: (1) placement of cortical graft through a core track small and medium precollapse lesions. Of seventy-five pa-
made in the femoral neck and head; (2) grafting performed tients who responded to a questionnaire, 81% expressed satis-
through a so-called trapdoor220-222 made through the articular faction with the result of the procedure. Eleven percent (two)
cartilage of the femoral head (the trapdoor exposes the underly- of nineteen hips with a precollapse lesion, 23% (five) of
ing lesion, necrotic bone is removed, and the cavity is filled with twenty-two hips with a postcollapse lesion without depres-
cancellous and/or cortical bone graft); and (3) grafting through sion, and 39% (twenty-four) of sixty-two hips with a more ad-
a window made in the femoral neck at the base of the head (the vanced lesion were converted to a total hip replacement.
necrotic area is removed, and bone graft is placed in the defect). Berend et al.101 analyzed 224 collapsed osteonecrotic hips
The results of these bone-grafting techniques are sum- (in 188 patients) treated with vascularized fibular grafts and
marized in the Appendix. In well-selected patients, success found a survival rate of 64.5% at a mean of 4.3 years (range,
rates have ranged from 24% to 100% at two to fifteen years two to twelve years). They reported that an increased relative
postoperatively. Rosenwasser et al.228 described a “light bulb” risk of conversion to total hip replacement was associated with
procedure in which diseased bone was curetted out through a an increased lesion size and the amount of collapse.
trapdoor in the femoral neck and was replaced by cancellous In summary, vascularized bone-grafting can lead to ex-
autograft. The authors found an 87% rate of successful results cellent results in hips with early-stage disease. The procedure
in a study of fifteen hips at a mean of twelve years. One of us may be effective, compared with core decompression, for
(M.A.M.) and colleagues223 performed a similar procedure in larger lesions just before head collapse. Once the head has col-
twenty-one hips (nineteen patients), with diseased bone re- lapsed, the results are less predictable. For an excellent review
placed by a bone-graft substitute (a combination of deminer- of the indications, techniques, and results of vascularized fibu-
alized bone matrix, processed allograft bone chips, and a lar grafting, readers are referred to the report of Urbaniak and
thermoplastic carrier). At a mean of four years (range, three to Harvey247.
4.5 years), eighteen (86%) of the twenty-one hips showed a
clinically successful result (a Harris hip score of >80 points Other Operative Methods for
and no additional procedures). Treating Stage-III and IV Disease
Rijnen et al.227 used a lateral approach, as is employed in a Multipotential stem cells: The augmentation of various treat-
traditional core decompression, to remove osteonecrotic bone ment methods with mesenchymal cells may be of benefit for pa-
from femoral head lesions and impacted allogeneic and autoge- tients with osteonecrosis of the femoral head252-255. Gangji et al.
nous cancellous bone grafts to regain femoral head sphericity. randomized thirteen patients (eighteen hips) with precollapse
Of twenty-eight consecutive hips (twenty-seven patients) with disease to be treated with either a 3-mm core decompression or
extensive lesions that were prospectively followed for a mean of a core decompression with implantation of autologous bone-
forty-two months (range, twenty-four to 119 months), eight marrow mononuclear cells252. After twenty-four months, the
(29%) were converted to a total hip replacement. Of the twenty group treated with the bone-marrow graft had a significant re-
reconstructed hips that survived, eighteen (90%) had a clini- duction in pain (p = 0.021) and joint symptoms compared with
cally successful result (minimal or no pain) and 70% showed no the other group. Five of the eight hips treated with core de-
signs of progression radiographically. compression only had radiographic evidence of deterioration,
Lieberman et al. reported on the use of bone morphoge- whereas only one of the ten hips treated with the bone-marrow
netic proteins for the treatment of osteonecrosis of the femo- graft had such deterioration (p = 0.016). Hernigou and
ral head176. Partially purified human bone morphogenetic Beaujean followed 189 hips in 116 patients for five to ten years
protein was combined with allogeneic antigen-extracted auto- after core decompression and grafting combined with implanta-
lyzed human bone and was introduced into the femoral head tion of autologous bone marrow obtained from the iliac crest254.
1125
TABLE I Decision-Making Hierarchy for the Treatment of Patients with Osteonecrosis of the Femoral Head
Stage Treatment
I (no radiographic changes) Core decompression, percutaneous drilling
II (precollapse) Core decompression, percutaneous drilling, bone-grafting, osteotomies
III (crescent sign [subchondral fracture collapse]) Bone-grafting, hemiresurfacing, total hip arthroplasty
IV (joint deformity, acetabular involvement) Total hip arthroplasty, possibly metal-on-metal total hip resurfacing arthroplasty
Success (avoidance of total hip replacement) was achieved in the resurfacing group had persistent groin pain (20% [six
136 (94%) of 145 hips that had been operated on before col- hips] compared with 7% [two hips] in the other group). In a
lapse but in only nineteen (43%) of forty-four hips that had study of thirty-seven hips followed for a mean of 6.5 years
been operated on after collapse. (range, two to eighteen years), Beaule et al. reported a good or
Cementation of the femoral head256-260: Treatment by re- excellent result (according to the Harris hip score) in 79% and
moving the dead bone from the femoral head (sequestrec- 62% of the hips at five and ten years, respectively127.
tomy) and replacing it with bone cement was first reported in Various studies on limited femoral resurfacing pub-
1993 by Hernigou et al., who studied the results in patients lished since 1995 have demonstrated satisfactory results for up
with sickle cell anemia256. Sixteen hips were injected with ce- to ten years and beyond127,261,264,270-273. Recently, a few studies
ment to elevate the cartilage and allow immediate full weight- showed less predictable outcomes of these procedures. In a re-
bearing. At a mean of five years (range, three to seven years), view of the results of twenty-nine consecutive femoral head
fourteen of the sixteen hips were stabilized (i.e., they had min- resurfacing procedures in twenty-eight patients261, Adili and
imum pain and no radiographic signs of progression). Wood Trousdale reported that seventeen patients (eighteen hips,
et al. treated nineteen patients (twenty hips) with open reduc- 62%) stated that they felt better than they had before the sur-
tion augmented with methylmethacrylate cement and fol- gery. The overall hip survivorship was 75.9% at three years,
lowed them for six months to two years258. Three patients had and eight hips (27.6%) were converted to a total hip replace-
a conversion to a total hip replacement. The long-term results
of this procedure are unknown.
TABLE II Recommendations for Treatment for Osteonecrosis
Joint Arthroplasty of the Femoral Head
Total joint replacement: Total hip replacement is indicated Grade of
once the femoral head has collapsed and the hip joint has de- Recommendation*
generated such that the articulation is compromised. Total Nonoperative
joint replacement will not be addressed in this paper, as it is
Lipid-lowering agents I
too extensive a topic and deserves a separate review. Large pre-
Anticoagulants I
collapse lesions and postcollapse disease pose a difficult prob-
Iloprost I
lem. Procedures aimed at joint preservation do not have
Bisphosphonates I
predictable results in hips with such lesions; however, because
Shock-wave therapy I
patients with osteonecrosis of the femoral head are generally
Hyperbaric oxygen I
young, total hip arthroplasty is often an unfavorable option.
Surgical alternatives for these patients may include limited Pulsed electromagnetic fields I
femoral resurfacing and bipolar hemiarthroplasty. Operative
Limited femoral resurfacing arthroplasty: In this proce- Core decompression (early-stage disease) A
dure, the damaged cartilage on the femoral side is removed Osteotomy B
and bone stock is preserved127,261-274. The viable acetabular carti- Nonvascularized bone-grafting B
lage is retained. The potential advantages of resurfacing over Vascularized bone-grafting A
total hip replacement are lower dislocation rates, preservation Multipotential stem cells I
of bone stock, and the ability to perform conversion to total Cementation I
hip arthroplasty if necessary. A study of hips treated for post- Limited femoral resurfacing B
collapse disease showed that, at a mean of seven years, overall
survivorship after hemiresurfacing (twenty-seven of thirty *A = good evidence (Level-I studies with consistent findings) for
hips) was similar to that after standard total hip replacement or against recommending intervention, B = fair evidence (Level-II
(twenty-eight of thirty hips)271. A higher percentage of patients or III studies with consistent findings) for or against recommend-
ing intervention, C = poor-quality evidence (Level-IV or V studies
treated with resurfacing maintained a high activity level (60% with consistent findings) for or against recommending interven-
[eighteen hips] compared with 27% [eight hips] in the group tion, and I = insufficient evidence to make a recommendation.
treated with total hip replacement). However, more patients in
1126
ing implantation of twenty-nine uncemented press-fit bipolar

TABLE III Methods Not Recommended for Treatment of
Osteonecrosis of the Femoral Head
endoprostheses, Yamano et al.281 found femoral loosening in six
hips, acetabular protrusio in five, and osteolysis in eleven. Bipo-
Grade of lar hemiarthroplasty has a high failure and complication rate
Recommendation and is associated with a high prevalence of polyethylene wear279-281.
Against Use
of Treatment* As a consequence, there has been an overall decrease in the utili-
zation of these devices.
Nonoperative
Non-weight-bearing A
Treatment Recommendations
Restricted weight-bearing A
and Future Methods
Operative A decision-making hierarchy that we used for the treatment of
Core decompression (late-stage disease) A patients with osteonecrosis of the femoral head is presented in
Bipolar arthroplasty B Table I. It is based on radiographic findings and the philoso-
Rotational osteotomy (United States) A phy of performing the least invasive treatment appropriate for
the extent of the disease. This hierarchy is necessary because
*A = good evidence (Level-I studies with consistent findings)
the surgeon can use an extensive procedure such as a total hip
for or against recommending intervention, B = fair evidence
(Level-II or III studies with consistent findings) for or against
replacement for any stage. The table should serve as a guide,
recommending intervention, C = poor-quality evidence (Level-IV and it is subject to surgeon interpretation.
or V studies with consistent findings) for or against recom- The use of biological agents (bone morphogenetic pro-
mending intervention, and I = insufficient evidence to make a teins and vascular growth factors) to preserve the femoral
recommendation. head and avoid joint replacement is currently under investiga-
tion282-285. In the future, these agents might be used to augment
some of the femoral head-preserving procedures mentioned
ment. In a study of fifty-nine patients (fifty-nine hips) fol- in this paper. Future treatment of osteonecrosis of the femoral
lowed for a mean of 4.5 years266, Cuckler et al. reported head appears promising as recombinant factors become more
eighteen failures—i.e., conversion to total hip replacement or available to enhance bone and cartilage healing.
considerable groin pain requiring medication. Tables II and III present treatments recommended and
We recommend the following criteria for choosing not recommended for osteonecrosis of the femoral head on
candidates for limited femoral head resurfacing: (1) Ficat the basis of the quality (level of evidence) of studies of those
and Arlet Stage-III disease, (2) a combined necrotic angle treatments.
of >200° or >30% involvement, (3) femoral head collapse
of >2 mm, and (4) no evidence of damage to the acetabular Appendix
cartilage. Tables showing the results of core decompression, an-
Bipolar hemiarthroplasty: Bipolar hemiarthroplasty has gular and rotational osteotomy, nonvascularized bone-
the same indications as hemiresurfacing arthroplasty. The pro- grafting, and vascularized bone-grafting, as reported in the
cedure has yielded variable success rates in the treatment of os- literature, are available with the electronic versions of this arti-
teonecrosis of the femoral head13,275-281. In a series of twenty-two cle, on our web site at jbjs.org (go to the article citation and
patients, Grevitt and Spencer276 reported a good or excellent click on “Supplementary Material”) and on our quarterly CD-
clinical outcome (defined as no need for total hip replacement) ROM (call our subscription department, at 781-449-9780, to
in twenty-one patients at a mean of forty months (range, order the CD-ROM).
twenty-four to seventy-one months). Chan and Shih13 com-
pared the outcomes of cementless total hip replacement with NOTE: The authors thank Dr. German Marulanda and Dr. Thorsten Seyler for their help with re-
search background material.
those of hemiarthroplasty in a series of twenty-eight patients
with bilateral disease. At a mean of 6.4 years (range, four to
twelve years), a satisfactory outcome (defined as no need for ad-
ditional surgery) was found in twenty-four of the twenty-eight
Michael A. Mont, MD
hips treated with the hemiarthroplasty compared with twenty- Center for Joint Preservation and Reconstruction, Rubin Institute
three of the twenty-eight hips treated with the standard total hip for Advanced Orthopedics, Sinai Hospital of Baltimore, 2401
replacement. Other studies have shown high complication rates West Belvedere Avenue, Baltimore, MD 21215. E-mail address:
following bipolar hemiarthroplasties in patients with osteone- [email protected]
crosis of the femoral head. Sanjay and Moreau279 reported sev-
enteen complications in twenty-one patients at a mean of 4.6 Lynne C. Jones, PhD
David S. Hungerford, MD
years (range, 2.1 to seven years) postoperatively. Takaoka et al.280 Division of Arthritis Surgery, Department of Orthopaedic Surgery, The
found a 42% rate of radiographic failure and/or acetabular de- Johns Hopkins University School of Medicine, Good Samaritan Hospital,
generation in forty-7eight hips (thirty-five patients) at a mean Professional Office Building, Suite G-1, 5601 Loch Raven Boulevard, Bal-
of 11.4 years postoperatively. At a mean of twelve years follow- timore, MD 21239
1127
The authors did not receive grants or outside funding in support of ble or nonprofit organization with which the authors are affiliated or
their research for or preparation of this manuscript. They did not associated.
receive payments or other benefits or a commitment or agreement
to provide such benefits from a commercial entity. No commercial
entity paid or directed, or agreed to pay or direct, any benefits to any
research fund, foundation, educational institution, or other charita- doi:10.2106/JBJS.E.01041
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Current Concepts Review

(HIV) are at increased risk for the development of osteonecrosis

Factors Affecting Treatment Fig. 1

II (precollapse) Core decompression, percutaneous drilling, bone-grafting, osteotomies

ing implantation of twenty-nine uncemented press-fit bipolar

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