Osteonecrosis of the knee: differences among idiopathic and secondary types

J. Narváez, J. A. Narváez1, J. Rodriguez-Moreno and D. Roig-Escofet1

Department of Rheumatology, Hospital Príncipes de España, Ciudad Sanitaria y Universitaria de Bellvitge and
1 Department of Computed Tomography and Magnetic Resonance Imaging, Institut de Diagnostic per la Imatge, Hospital Duran i Reynals, Ciudad Sanitaria y Universitaria de Bellvitge, Barcelona, Spain


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Objective. To describe the clinical and imaging features of patients with osteonecrosis of the knee, emphasizing the differences among idiopathic and secondary types.

Methods. A retrospective chart review of 37 consecutive patients (41 knees) with osteonecrosis of the knee confirmed by bone scintigraphy and/or magnetic resonance imaging (MRI), and a comparison of idiopathic and secondary types of osteonecrosis.

Results. Twenty-four patients had idiopathic osteonecrosis, and in 13 patients one or more predisposing factors were identified (secondary osteonecrosis). Idiopathic osteonecrosis of the knee was typically a disease of the elderly, characterized by severe knee pain of sudden onset, unilateral involvement, and restriction of the lesions generally to one femoral condyle or tibial plateau, with predilection for the medial compartment of the joint. Secondary osteonecrosis generally occurred in younger patients and frequently had an insidious onset with mild or vague pain, the lateral compartment of the knee was often involved, and the lesions were generally larger than lesions arising spontaneously; in the great majority of cases they involved the femoral condyles and/or tibial plateaus. Bilateral distribution and multifocal involvement was also seen in these forms. Magnetic resonance imaging was helpful in confirming the suspected diagnosis when conventional radiographs were normal or equivocal, and demonstrated different patterns of abnormalities in idiopathic and secondary types.

Conclusion. There are significant differences between idiopathic and secondary osteonecrosis, especially in regard to clinical presentation and the location, extent and MRI appearance of the lesions. These differences are probably due to a difference in the pathogenetic mechanism.

KEY WORDS: Osteonecrosis of the knee, Idiopathic osteonecrosis, Secondary osteonecrosis, Magnetic resonance imaging


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Osteonecrosis (ON) is a relatively common condition that usually results from circulatory impairment of an area of bone, leading to the ischaemic death of the cellular constituents of the bone and marrow. There are a few specific areas of the skeleton for which this condition seems to have a predilection. These include the femoral and humeral heads, the femoral condyles, the proximal tibia and some of the small bones of the foot and ankle and of the wrist. The area most commonly affected is the femoral head, followed by the humeral head and the knee. In the knee, it may involve either the distal femur or the proximal tibia, and one or both condyles or plateaus. There seem to be two distinct forms of this condition: the idiopathic, primary or spontaneous ON (ION) of the knee, which appears in patients without risk factors for osteonecrosis, and secondary ON (SON), caused by a number of well-recognized predisposing factors, often acting alone but at times acting in concert. The first of these forms has been characterized as a distinct entity since its first description by Ahlbäck et al. in 1968 [19]. The second form is poorly documented; few reports have been devoted to SON of the knee [1013], in contrast with the great number of published papers that have focused on SON of the hip.

To describe the clinical and imaging features of patients with ION and SON of the knee, we present a clinical review of a series of 37 patients (41 knees), emphasizing the differences among the two types of osteonecrosis.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Our study was a retrospective chart analysis of 37 patients (41 knees) with ON of the knee, confirmed by bone scintigraphy and/or magnetic resonance imaging (MRI). The patients comprised 25 women and 12 men and the mean age at diagnosis was 60 ± 13 yr (range 19–85 yr). According to the presence of risk factors for osteonecrosis, the patients were grouped into two categories: ION (24 cases) and SON (13 cases). Four patients with SON had bilateral involvement.

The medical charts of all patients were reviewed comprehensively to obtain clinical, laboratory, imaging and disease evolution data. Symptoms were usually described carefully and adequately in the medical records. All patients had conventional radiographs of the knees taken at the initial visit and at follow-ups. The necrotic lesion was staged according to the classification of Aglietti et al. [6]: stage 1 = normal; stage 2 = flattening of the affected weight-bearing part of the condyle; stage 3 = a subchondral lesion comprising an area of radiolucency of variable size and depth surrounded proximally and distally by some sclerosis; stage 4 = the radiolucent area is surrounded by a sclerotic halo and the subchondral bone has collapsed and is visible as a calcified plate; stage 5 = secondary degenerative changes with osteophyte formation and subchondral sclerosis on both femur and tibia, and some erosion. The degree of osteoarthritis was graded radiologically as follows: none = no visible changes; minimal = spurring of the tibial spine, mild joint space narrowing, some flattening of the femoral condyles, and small marginal osteophytes; moderate = appreciable joint space narrowing, subchondral sclerosis and larger osteophytes; severe = joint space obliteration with deformity or even destruction of the articular surface, and occasionally lateral subluxation. Radiographs were reviewed to establish the degree of ON and osteoarthritis in a blinded manner by the first two authors (J.N. and J.A.N.); in cases of disagreement a consensus opinion was obtained.

Confirmatory [99mTc]methylene diphosphonate bone scintigraphy was performed in 19 patients. MRI examination was carried out in 34 patients, four of whom had bilateral involvement, and a total of 38 knees were studied. MRI images were reviewed in a blinded manner by one radiologist (J.A.N.), who did not know if the patient was classified as having ION or SON (he described only the appearance of the lesion without classifying the patients as having ION or SON). The diagnosis of osteonecrosis by the use of MRI was based mainly on two patterns: (i) a focal subcortical loss of signal intensity on T1- and T2-weighted images (Fig. 1Go), and (ii) a focal lesion of variable signal intensity surrounded by a demarcation rim. This demarcation rim appears as a low signal margin on T1-weighted images, and a double halo (high-signal inner border inside a low-signal peripheral rim) on T2-weighted images (Fig. 2Go). These two patterns may be associated with bone marrow oedema. MRI images were also assessed for the presence of focal deformities of the cartilage and subchondral cortical bone, tearing or degeneration of the menisci, and joint effusion.



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FIG. 1. (A) Sagittal T1-weighted MRI showing a low-signal subchondral lesion (arrows) of linear morphology. This lesion is associated with ill-defined bone marrow oedema. (B) On T2-weighted sequences the subchondral lesion also shows a low signal (arrowheads) and the ill-defined bone marrow oedema shows a high signal. Joint effusion (arrows) is also well demonstrated, with a homogeneous high signal.

 


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FIG. 2. (A) Sagittal T1-weighted MRI demonstrating a large subchondral lesion (arrowheads) isointense with normal fatty marrow and surrounded by a serpiginous low-signal band. (B) On T2-weighted sequences this lesion (arrows) is demarcated by a band of high signal intensity inside a hypointense margin—the double halo sign.

 
Twenty-five patients had a minimum follow-up of 6 months after the initial diagnosis was made; the remaining 12 were lost to follow-up. In these patients, the evolution of ON was monitored with periodical conventional radiographs and clinical examinations. Follow-up MRI examination was performed in only four patients.

Statistical analysis
Continuous data were described as mean ± S.D. and categorical variables as percentages. Patients were classified in idiopathic and secondary groups and their clinical manifestations were compared. Comparisons were made using Student's t-test for independent continuous variables or the Mann–Whitney U-test when the assumption of normality was not realized. To analyse categorical data, we performed the {chi}2 test with Yates’ correction or Fisher's exact test when the expected values were less than 5. Statistical significance was defined as P <= 0.05.

We also calculated the {phi}{rho} coefficient as a measure of the magnitude of the association and the relative risk (RR) between groups for some variables, together with the 95% confidence interval (CI).


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Results are summarized in Table 1Go.


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TABLE 1. Clinical features of 37 patients with ON of the knee

 
Aetiology
ION was observed in 24 (64.9%) of the 37 patients studied; in 13 (35.1%) of them one or more aetiological factors were identified: alcoholism (two cases), renal transplantation (two cases were receiving treatment with cyclosporin A and 5 mg prednisone per day), connective tissue disorders (two cases of systemic lupus erythematosus and two cases of rheumatoid arthritis, all of them treated with low doses of glucocorticosteroids), thalassaemia (one case), leukaemia (one case treated with chemotherapy and allogeneic bone marrow transplantation), and systemic steroid administration (one case of myasthenia gravis, one case of giant cell arteritis and one case of eosinophilic fasciitis).

Location and extent of the lesions
In 33 (89.2%) patients the lesions were unilateral (the right knee was affected in 13 cases and the left knee in 20); the remaining four patients (10.8%), all of them with secondary forms, had bilateral disease.

The most frequent location was the medial femoral condyle, which was affected, alone or in combination with involvement of the lateral condyle and/or the proximal tibial, in 36/41 (87.8%) knees (Table 2Go). With regard to the aetiology and extent (Table 3Go), all the ION were unilateral, with lesions restricted to one condyle or tibial plateau in 23/24 (95.8%) cases. The medial side of the joint was most commonly involved, with predilection for the weight-bearing surface of the femoral condyle (20/24 cases).


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TABLE 2. Extent of the ON lesions

 

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TABLE 3. Aetiology and extent of the lesions

 
SON was unilateral in nine (69.2%) patients and bilateral in four (30.8%). Generally, the SON lesions were of greater size than the idiopathic ones, involving at least one femoral condyle and tibial plateau or both femoral condyles (with or without concomitant involvement of tibial plateaus) in 15/17 (88.2%) knees. Only in 2/17 (11.8%) knees were the lesions restricted to one femoral condyle. Involvement of the lateral femoral condyle occurred in up to 75% of knees, alone or in combination with changes in the medial femoral condyle and/or tibial plateaus. The four patients with bilateral disease had diffuse involvement of both femoral condyles and tibial plateaus in each knee; in all of them, the symptoms began simultaneously.

Four patients (10.81%), all of them with secondary forms, had polytopic ON at the time of diagnosis, with simultaneous involvement of the right humeral head in patient 4, both femoral heads in patients 5 and 8, and both hips and both shoulders in patient 22.

Clinical features
The disease was more frequent in women (25 women and 12 men). The mean age at onset in the group with ION was 66 ± 8 yr, whereas in the group with SON it was 49 ± 14 yr. The interval between the onset of symptoms and diagnosis was 105 ± 120 days (range 3–365 days).

Pain was the dominant symptom in all cases. It appeared suddenly in 27/37 (73%) patients (22 remembered the exact moment it occurred) and gradually in 10/37 (27%). None of the patients had a history of minor knee trauma. In the ION group, the onset of symptoms was acute in 22/24 (91.6%) patients and gradual in 2/24 (8.4%). Pain was usually severe and localized, occurring predominantly on active motion or weight-bearing and causing significant functional impairment in all cases; pain at rest was seen in 58% of patients. In the SON group, the typical history of sudden onset of well-localized severe pain occurred in only 5/13 (38.5%) patients; in the remaining eight patients (61.5%) the onset of symptoms was gradual, with mild and diffuse pain (Table 4Go). These differences may explain the longer delay until diagnosis observed in the group with SON (121 ± 123 versus 96 ± 116 days). In the cases of steroid-related ON, the interval between steroid intake and the appearance of symptoms ranged from 9 months to 2 yr.


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TABLE 4. Differences between ION and SON

 
Physical examination showed tenderness over the involved area in 100% of patients, small or moderate effusion in 80.5% of knees (the synovial fluid was examined in 18 patients and was non-inflammatory in all of them) and flexion contracture or mild restricted motion in 20%.

Imaging modalities
Radiography.
The mean duration from the onset of symptoms to the first radiographic examination was 15 ± 17 weeks. Initially, plain roentgenograms showed evidence of ON in only 20 (48.8%) of the 41 knees, and were normal in the remaining 21 (51.2%). Aglietti's stage II was observed in nine knees (22%), stage III in six (14.6%), stage IV in two (4.9%) and stage V in three (7.3%). The initial radiographs were normal in 19 knees (46.3%), minimal changes were seen in 12 (29.3%), moderate changes in six (14.6%) and severe changes in four (9.8%). Radiological evidence of osteoarthritis was more frequent in the ION group. In these patients, the initial radiographs revealed arthrosis in 19/24 (79.1%) knees: 11/24 (45.8%) presented minimal changes, 6/24 (25%) moderate changes and 2/24 (8.3%) severe changes. In SON, the initial radiographs revealed osteoarthritis in only 3/17 (17.6%) knees: in one knee (5.8%) there were minimal changes and in two (11.7%) there were severe changes.

At the follow-up examination, the Aglietti stage had not changed in 16 of the 20 knees, but had increased in four despite the conservative treatment. None of the patients with initial normal radiographs developed osteonecrotic changes.

Scintigraphy.
Confirmatory bone scintigraphy was carried out in 19 patients. It was very useful in confirming the suspected diagnosis in patients without radiological evidence of ON at the time of presentation, and in detecting multiple ON in patients with polytopic involvement. We did not find differences in the bone scan pattern between ION and SON.

MRI.
The mean interval from the onset of symptoms to MRI examination was 5.6 ± 4 months. In patients with ION, the most frequent MRI pattern was a subcortical focal loss of signal, which was observed in 95.6% of knees on T1-weighted images and in 69.5% of knees on T2-weighted images (Fig. 1Go). The demarcation rim (double-halo sign) was not seen in any patient. Additional frequent findings in ION patients were homolateral meniscal lesion (degeneration an/r tearing), which was observed in all knees but one (95.6%), and focal deformity of the subchondral plate, which was seen in 65% of cases. On the contrary, in patients with SON the demarcation rim was observed in 73.3% of knees (Fig. 2Go). Homolateral meniscal lesion was found in 33% of cases, and focal deformity of the subchondral bone plate was seen in 20% of knees. The extent of bone necrosis measured on MRI scans at presentation was significantly greater in SON than in ION. Evidence of an osteochondral defect at presentation was infrequent in both groups (6.6% of cases with ION and 4.3% of cases with SON), and was observed only in cases with longer diagnostic delay. Joint effusion was seen in 80.5% of knees.

Outcome
Twelve patients were lost to follow-up. In the remaining 25 patients (four with bilateral involvement), the average follow-up period was 18 ± 13 months (range 6–60 months) after the initial examination. Initially, surgical treatment (arthroplasty) was performed in four patients with Aglietti's stage IV or V; an operation was recommended for other knee but it was refused by the patient. In addition, one case with steroid-related ON was treated with core decompression. The remaining 18 patients (22 knees) were managed conservatively (limitation of weight-bearing, and analgesics). Progression of the symptoms/disease led to a knee arthroplasty in six of these 22 knees within 2 yr. In the other patients symptoms resolved or improved.

At the time of last follow-up, 6/24 (25%) knees in the ION group and 4/17 (23.5%) in the SON group required arthroplasty, although two of the patients with SON also had severe articular damage at presentation due to erosive rheumatoid arthritis.


    Discussion
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Whereas ION of the knee is an accepted entity, it has become clear that a similar condition can develop in patients with well-recognized risk factors for ischaemic necrosis of bone (SON of the knee); however, its clinical and imaging features are not yet fully understood, mainly because of the limited number of reports devoted to this condition [1013].

Despite the comparatively small number of patients included in our study, which may not have been large enough to detect minor differences, we found significant differences between the idiopathic and secondary forms of osteonecrosis, especially with regard to its clinical presentation and the location and extent of the lesions (Table 4Go) and their MRI appearance. These results indicate that two distinct forms of the disease can be identified.

ION occurs in older individuals, usually after the sixth decade of life [1, 48]. Women are affected three times more frequently than men [1, 4, 6, 8]. The pain is usually characterized by sudden onset (frequently the patient could remember the exact moment or the activity during which the symptoms started) and is initially severe, causing significant functional impairment; pain is frequently present at rest [1, 38]. Unilateral involvement predominates over bilateral involvement. The condition is generally restricted to one femoral condyle or tibial plateau. The medial side of the joint is the side that is most commonly involved, and the lesion occurs more often in the femoral condyle than in the tibial plateau [4, 68]. Less frequently, the lateral condyle is affected [68]. In SON, the age and sex distribution is dependent upon the primary disease, although it generally affects a younger age group. The onset of symptoms is gradual in more than 60% of patients, and often mild or vague pain occurs only with active motion or weight-bearing. Generally, the lesions of SON are larger than those of ION; fewer than 15% of cases show changes of a limited extent. Both knees are affected in 30–80% of patients [6, 10, 12, 13] and involvement of the lateral femoral condyle occurs in up to 60% of patients [6, 10, 12], alone or in combination with simultaneous involvement of the medial femoral condyle [10, 12]. Proximal tibial involvement is less common. This is contrast to the almost invariably unilateral distribution of ION and its predilection for the weight-bearing segment of the medial femoral condyle. The simultaneous presence of ON in other locations (hips and shoulders) is not rare [10, 12].

Our results were similar to those reported in other studies. However, contrary to the earlier series of ION, in which there were appreciable radiographic osteonecrotic changes in 76–100% of patients at the time of diagnosis [4, 6, 7, 14], we found a higher proportion of necrotic lesions in the early stages, with normal initial radiographs in more than half of our patients. This difference could be explained by the fact that scintigraphy and MRI allowed us to make an early diagnosis, before the development of radiographic abnormalities.

We also observed different patterns of MRI abnormalities in ION and SON. It is remarkable that the demarcation rim, which is considered specific and pathognomonic for avascular ON [15], was observed in most of the patients with SON but in none of those with ION. The demarcation rim or reactive interface separates necrotic bone and marrow from adjacent viable tissue, and shows a low signal intensity on T1-weighted images and a double-halo appearance on T2-weighted images. The double halo consists of a high-signal inner border inside a low-signal rim surrounding the lesion. Histological studies have demonstrated that the low-signal outer rim corresponds to sclerotic bone, whereas the high-intensity inner border probably consists of hypervascular granulation tissue resulting from a hyperaemic response adjacent to thickened trabeculae [16]. In contrast, the most common MRI pattern observed in ION was a focal subcortical area of low signal intensity on both T1- and T2-weighted images. To date, there have been few reports on the use of MRI in ON of the knee [1719]. Of interest, similar observations have been reported increasingly in ION of the knee [18, 20, 21]. Among the few reports of MRI in SON, Chancelier et al. [19] described MRI signal alterations similar to those we saw in a series of patients receiving long-term corticosteroid therapy. The cause of these apparent differences among idiopathic and secondary types is not clear, although they may be ascribable to a difference in the underlying pathogenesis.

The aetiopathogenesis of ION of the knee remains unclear. Two main theories have been proposed: primary vascular insufficiency leading to infarction of bone [6, 22], and a minor, unrecognized traumatic insult producing microfractures in the subchondral bone and subsequent osteonecrosis [3, 7, 9, 21, 22]. The usual sudden onset of symptoms that characterizes ION, its occurrence in middle-aged and elderly patients, in whom osteoporosis is frequent, and its characteristic predilection for the area of maximum weight-bearing of the medial femoral condyle or tibial plateau, strongly suggest a traumatic lesion as the most likely underlying cause of ION. In this respect, more authors [3, 7, 21] are of the opinion that the initial insult may be stress microfractures occurring within the weak subchondral bone plate, caused by the repeated impact of the articular surfaces. Additional support for this assertion comes from the similarity in MRI appearance between ION and stress fractures, which appear as band-like areas of low signal intensity in the intramedullary space on T1- and T2-weighted images [24, 25].

Moreover, meniscal tears have been reported in association with this condition, and a prominent role of meniscal injury in the pathogenesis of ION has also been proposed [26]. It is well established that the injured meniscus has a diminished load-bearing capacity. The repeated impact of the articular surface against a fragmented meniscus during everyday activity could result in microfractures and subsequent vascular insufficiency of the subchondral bone. The appearance of ION about the knee after meniscal surgery also supports this pathogenetic relationship [27]. The high rate of medial meniscus lesion (95.6%) observed in our patients with ION is in agreement with this hypothesis. However, this cannot be the only factor involved in its pathogenesis, because some patients with ION had no evidence of a torn meniscus. In this sense, it has been suggested that the presence of osteoarthritis an/r osteoporosis may also be a significant contributing factor in the development of subchondral plate microfractures [3, 9, 21]. It is commonly recognized that osteoporosis and osteoarthritis (as a result of violent impact between osseous surfaces not protected by articular cartilage) can weaken the load-bearing capacity of bone such that fracture can result from normal activity. The exact temporal and causal relationship between ON and osteoarthritis remains controversial, because is difficult to establish whether ON is simply a predisposing factor for osteoarthritis or whether the presence of moderate to severe osteoarthritis predisposes to spontaneous osteonecrosis of bone [7]. In our series, radiological evidence of osteoarthritis at the time of diagnosis was more frequent in the group with ION (79%) than in the group with SON (17%), although this difference could be explained by the older age of the ION patients. In initial radiographs, only 33% of patients with ION were found to have moderate to severe osteoarthritis in the compartment where osteonecrosis developed subsequently.

By contrast, the pathophysiology of SON of the knee seems to be comparable with that which occurs in the femoral head [7]. In SON of the knee, several aetiological factors have been identified, all of them causing, by different mechanisms (embolization, thrombosis, vessel wall injury, marrow encroachment or venous occlusion) [15], an interruption of the blood supply. Interruption of the vascular supply to the subchondral bone then leads to death of bone and marrow cells over a larger volume than is observed in ION [7]. This similar pathogenesis can explain the similar MRI appearance of the two conditions, with evidence of the demarcation rim in up to 80% of cases of avascular necrosis of the hip [28] and in 73% of our cases of SON of the knee; this value agrees with the results of other authors [19].

In summary, although the number of patients included is not large, this study does indicate a sharp contrast between two different types of ON of the knee, which presumably have different underlying pathogenetic mechanisms. The more extensive lesions in patients with the secondary form of disease and the facts that they occur in the lateral compartment and that other joints may be affected argue for a generalized ‘metabolic’ aetiology as opposed to some more local ‘mechanical’ cause in the idiopathic type, which may or may not be related to pre-existing degenerative changes an/r meniscal injury.


    Notes
 
Correspondence to: F. J. Narváez Garcia, C/Llobregat, no. 5. 3° 1a, Hospitalet de Llobregat 08904, Barcelona, Spain. Back


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

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Submitted 7 May 1999; revised version accepted 3 March 2000.



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