Published Online First: 25 May 2007. doi:10.1136/ard.2006.066878
Annals of the Rheumatic Diseases 2008;67:150-153
Copyright ? 2008 BMJ Publishing Group Ltd & European League Against Rheumatism


EXTENDED REPORTS

Histopathological prevalence of subchondral insufficiency fracture of the femoral head

T Yamamoto , Y Iwamoto , R Schneider , P G Bullough

Departments of Orthopaedic Pathology and Radiology, Hospital for Special Surgery, 535 East 70th Street, New York, NY 10021, USA

Correspondence to:
Dr Peter G Bullough, Department of Laboratory Medicine, Hospital for Special Surgery, 535 East 70th Street, New York, NY 10021, USA; bulloughp{at}hss.edu

Accepted 18 May 2007


*    ABSTRACT
 
Objective: Subchondral insufficiency fracture of the femoral head (SIF) is a recently recognised cause of acute onset arthritis mostly in older women, which previously had been commonly considered either as osteonecrosis or osteoarthritis. The purpose of this study is to report the histopathological incidence of SIF using surgically removed femoral heads.

Methods: We reviewed 7718 consecutive femoral heads from 7286 patients removed over a 4-year period (2001?2004). There were 4211 women and 3507 men. The age range was from 13 to 96, average age was 60. There were 7349 hips with a preoperative clinical diagnosis of osteoarthritis and 369 with a preoperative clinical diagnosis of osteonecrosis.

Results: SIF was diagnosed histologically as the primary process in 501 of 7718 resected femoral heads (6.5%). The age range in these patients was from 20 to 93, with an average age of 68, in which 79% (394 hips) were over 60. They were 305 hips in women and 196 in men. The affected side was the right one in 253 hips and left in 248. The prevalence of SIF in cases with a preoperative diagnosis of osteoarthritis was 6.3% (460 of 7349), and with osteonecrosis was 11.1% (41 of 369). In all cases, callus and granulation tissue were observed histologically along the fracture line.

Conclusions: In this large series of total hip replacements SIF as the cause of disease was diagnosed histologically in 6.5% of the surgically removed femoral heads.


Hip fracture is an important public health problem in older people with osteoporosis, and it has been estimated that more than 500 000 cases will occur annually by the year 2030 in the United States.1 The most commonly encountered fractures are through the femoral neck, either subcapital, intertrochanteric or subtrochanteric.

Subchondral insufficiency fracture of the femoral head (SIF) is a recently recognised condition and several clinical characteristic appearances have been reported. The patients are mostly older women with osteoporosis; however few cases have been seen in renal transplantation cases.2?4 Shortly after the onset of pain, radiographic changes are unremarkable; however, magnetic resonance imaging (MRI) has been reported to show a pattern of bone marrow oedema associated with an irregular low intensity band paralleling the articular surface. MRI may thus be considered useful for the diagnosis of SIF.2 3 The concept of subchondral insufficiency fracture has now been expanded to include the knee and shoulder joint.5 6

As subchondral collapse is commonly observed in patients with symptoms of osteonecrosis in any joints, previous reports of SIF have stressed the importance of its differentiation from osteonecrosis by describing its characteristic clinical and anatomical appearances.1?6

In this study, we have investigated the prevalence of SIF in a series of surgical specimens obtained at the time of total hip replacement.


*    MATERIALS AND METHODS
 
Patients
We retrospectively reviewed all femoral heads removed surgically in our hospital that had a clinical diagnosis of either osteoarthritis or osteonecrosis during a 4-year period from January 2001 to December 2004. Cases of rheumatoid arthritis or other form of inflammatory arthritis were excluded from the study, as were cases of obvious metabolic diseases. During this period, 7718 femoral heads from 7286 patients fulfilling the clinical diagnostic criteria of osteoarthritis7 and osteonecrosis8 were examined in our laboratory. (The clinical imaging diagnosis of subchondral insufficiency fracture had not been made during this period, but was made retrospectively following pathology based upon the re-evaluation of the imaging appearances, including radiographs and MRI.)

The age range was from 13 to 96, with an average age of 60. They were 4211 women and 3507 men (F:M; 1.20:1.0). The reviewed materials included gross photographs, specimen radiographs, microscopic sections in each case.

Among the 7718 hips, 7349 femoral heads had a preoperative diagnosis of osteoarthritis. The age range was from 13 to 96 (average: 61) and 4026 were women and 3323 men (F:M; 1.21:1.0). There were 369 cases that had a preoperative diagnosis of osteonecrosis, in which the age range was from 13 to 85 (average: 41) and 185 were women and 184 men (F:M; 1.01:1.0).

Tissue preparation
In our department, all femoral heads removed at surgery are photographed intact and then fixed in 10% formalin solution. In each case, a 5 mm thick mid coronal section is obtained using a band saw, and is first photographed and then radiographed using low voltage x-rays (Faxitron, Buffalo Grove, IL, USA) and fine-grain films (Kodak, Rochester, NY, USA). After decalcification in 5% nitric acid solution, the sections are processed, embedded in paraffin and 5-?m thick glass mounted sections are prepared, which are routinely stained with haematoxylin and eosin.

Histopathological criteria of subchondral fracture
The morphological criteria for diagnosis of subchondral fracture were based on the previously published criteria.9 10 On gross examination, a linear narrow and irregular whitish grey zone in the bone marrow space paralleling the subchondral bone endplate is generally seen. Microscopically, this area consists of irregularly arranged fracture callus, reactive cartilage and granulation tissue. It should be noted that as all fracture leads to some bone and bone marrow necrosis on either side of the fracture line, small segments of necrotic bone trabeculae may be observed.11 12 However, such necrotic regions will be observed only around the fracture line and there will be no evidence of antecedent bone infarction or its zonal pattern. (Localised microfractures often observed in the superficial subarticular bone in osteoarthritis are not considered as SIF. In osteoarthritis, fractured bone trabeculae are generally thick, while those in SIF are thin and sparse.)


*    RESULTS
 
Prevalence of subchondral insufficiency fracture and clinical appearances
Subchondral insufficiency fracture was observed histologically in 6.5% of the resected femoral heads (501 of 7718). They were 305 women and 196 men (F:M; 1.56:1.0). The age range of SIF cases was from 20 to 93, with an average of 68 (table 1). Age distribution is described in fig 1a,b; six cases (1.2%) were in their third decades, 11 in their fourth (2.2%), 24 in fifth (4.8%), 66 in sixth (13.2%), 129 in seventh (25.7%), 195 in eighth (38.9%), 68 in ninth (13.6%) and two in their 10th decade (0.4%). The majority of the SIF cases (78%: 394 of 501) were over 60, which showed different distribution as compared with osteonecrosis, but similar with that in osteoarthritis (fig 2a,b). The affected side was the right one in 253 hips and left in 248. Bilateral involvement of SIF was observed in 14 cases (2.7%), in which the age range was from 46 to 75 (average 65). They were nine women and five men.

 


Figure 01
 
Figure 1 (a) Age and gender distribution in subchondral insufficiency fracture of the femoral head (SIF). There are 305 women and 196 men (F:M; 1.56:1.0). The age range is from 20 to 93, with an average of 68. (b) Age distribution in SIF. Six cases (1.2%) are in the third decade, 11 in the fourth (2.2%), 24 in the fifth (4.8%), 66 in the sixth (13.2%), 129 in the seventh (25.7%), 195 in the eighth (38.9%), 68 in the ninth (13.6%) and two in the 10th (0.4%). The majority of the SIF cases (394 of 501; 78%) are in the over 60s group.

 


Figure 02
 
Figure 2 (a) Age and gender distribution in osteonecrosis. A total of 369 cases had a preoperative diagnosis of osteonecrosis, in which the age range is from 13 to 85 (average: 41) and the female the male ratio is 1.01:1.0. (b) Age and gender distribution in osteoarthritis. A total of 7349 femoral heads had a preoperative diagnosis of osteoarthritis. The age range is from 13 to 96 (average: 61) and the female the male ratio is 1.21:1.0.

 


The prevalence of SIF in cases with a preoperative clinical diagnosis of osteoarthritis was 6.3% (460 of 7349), while in osteonecrosis it was 11.1% (41 of 369).

The prevalence of osteoarthritis, osteonecrosis and SIF in each decade is described in fig 3. From the third to seventh decades, the prevalence of SIF was about 3?6%, while that in the eight and ninth decades was about 8?9%.

 


Figure 03
 
Figure 3 Distribution of diseases in every decade. From the third to seventh decades, the prevalence of subchondral insufficiency fracture of the femoral head is about 3?6%, while that in the eighth and ninth decades is about 8?9%.

 
In 41 cases of SIF with the age of 20?49, the preoperative diagnosis was osteonecrosis in 17 cases and osteoarthritis in 24 cases. In these 24 cases of SIF with the preoperative diagnosis of osteoarthritis, secondary osteoarthritis was seen in two cases (developmental dysplasia of the hip and Legg?Calve?Perthes).

Histopathological findings
Gross examination of the resected femoral heads showed relatively spherical femoral heads with thinning of the articular cartilage or partially detached flaps of articular cartilage (about 0.5?2.5 cm in the greatest dimension) on the superolateral articular surfaces. On the examination of mid-coronal cut sections, a notched linear shaped zone of white and grey tissue, usually paralleling the subchondral bone endplate, was observed and consisted of fracture callus, reactive cartilage, and granulation tissue. In the surrounding tissue there was focal resorption of bone by active osteoclasts and replacement by vascular granulation tissue. Thin disconnected bone trabeculae indicative of osteopenia were observed in the remaining area of some of the femoral heads. Histology of the articular cartilage overlying the fractured region showed fibrillation or mild thinning; however, the articular cartilage was viable.

On the specimen radiograph, there was patchy osteosclerosis, which was microscopically confirmed as microcallus.

A representative case is shown in fig 4.

 


Figure 04
 
Figure 4 A 68-year-old woman with a preoperative diagnosis of osteonecrosis. (A) Radiograph shows patchy osteosclerotic area beneath the articular cartilage (arrows). (B) T1 weighted magnetic resonance image shows diffuse low signal intensity and there is also an irregular shaped low intensity band beneath the articular cartilage (arrow). This band corresponds histologically to the fracture line and associated repair tissue. (C) Cut section of the resected femoral head shows a whitish linear shaped area beneath the articular cartilage (arrow). (D) Specimen radiograph shows linear sclerosis. (E) Histology of the linear sclerotic area shows fracture callus formation and granulation tissue. (Haematoxylin and eosin x100.)

 

*    DISCUSSION
 
The prevalence of SIF in cases with a preoperative diagnosis of osteonecrosis was higher (11.1%) than that in osteoarthritis (6.3%). As a subchondral collapse is commonly observed in cases of osteonecrosis, radiographic evidence of subchondral fracture has in the past generally been considered as being associated with osteonecrosis.4 In previously reported cases of SIF, differentiation from osteonecrosis by imaging has been mainly based on MRI, as the radiographic differentiation between osteonecrosis and SIF appears to be somewhat confusing.4 10 One of the characteristic findings on MRI in SIF has been reported as the shape of the low intensity band on the T1-weighted images, which is generally irregular, serpiginous, paralleling the articular surface, and often discontinuous.2?4 8?10 13 On T2 weighted images, in SIF, both the low intensity band and the portion between the band and the articular surface tend to show a high intensity especially in the early phase of the fracture.

Patients with SIF clinically have generally been reported to be mostly older patients with osteopenia.2?4 However, in this study rare cases of SIF were observed in younger adults about 20?40.14

In those cases with a preoperative diagnosis of osteoarthritis, the clinical diagnosis was probably based on the clinical symptoms and radiographically by early disappearance of the joint space; however, some cases of SIF have been reported to undergo rapid joint space narrowing subsequently resulting in a rapid joint destruction.15 16

Before the concept of SIF had been introduced in 2000,9 the majority of the SIF cases reported here would have been diagnosed histologically as osteonecrosis, presumably based on the small foci of necrosis caused by the fracture. Histopathologically, the most characteristic finding of SIF is the presence of fracture callus and granulation tissue along both edges of the fracture line. Although small segments of necrotic bone trabeculae may be observed around the fracture in SIF, such necrotic regions are observed only around the fracture line and there is no evidence of antecedent bone infarction or its zonal pattern.9

In the majority of cases with osteoarthritis, isolated microfractures are often observed in the superficial eburnated lesion. However, such lesions can be distinguished from SIF based on the lack of a linear fracture line and the presence in osteoarthritis of sclerotic bony changes, loss of cartilage in the subchondral area, cysts osteophytes, etc.

Some cases of SIF have been reported to undergo collapse necessitating surgery, while other cases of SIF radiographically have been reported to heal after conservative therapy.2 3 17 The prognosis of SIF may depend on a number of variables, including the degree of osteopenia, activity, weight and the extent of fracture, as well as the initial treatment. The appropriate initial treatment of an insufficiency fracture may alter the prognosis.

The chief limitation of this study was the lack of clinical and radiographical information available to us; however, our main purpose is to document the histopathological prevalence of SIF based on a review of the surgical specimens. The significance of clinically recognising its prevalence appears to us to lie in its early recognition and management.

 

 


*    FOOTNOTES
 
Funding: This work is supported in part by a Grant-in-Aid in Scientific Research (No. 18591665) from JSPS and a grant from Daiwa Securities Health Foundation.

Competing interests: None.

Published Online First 25 May 2007


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