August 2020, VOLUME 215
NUMBER 2

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August 2020, Volume 215, Number 2

Musculoskeletal Imaging

Original Research

Distribution of Femoral Head Subchondral Fracture Site Relates to Contact Pressures, Age, and Acetabular Structure

+ Affiliations:
1Department of Orthopaedic Surgery, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan.

2Department of Anatomy and Cell Biology, RWTH Aachen University, Aachen, Germany.

Citation: American Journal of Roentgenology. 2020;215: 448-457. 10.2214/AJR.19.21895

ABSTRACT
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OBJECTIVE. Nontraumatic subchondral fracture of the femoral head (FH) is often seen in elderly patients with osteoporosis and acetabular dysplasia. Although this injury can also occur in young people, even those without osteoporosis, it remains unclear who is at risk. We examined the acetabular structure and sites of subchondral fracture of the FH in young patients compared with those in middle-aged and older patients.

MATERIALS AND METHODS. Forty-eight hips with nontraumatic subchondral fracture of the FH were divided into two groups according to patient age: young (< 40 years) and middle-aged and older (≥ 40 years). Dysplasia and retroversion were defined as a lateral center-edge angle of < 20° and crossover sign on anterosuperior radiographs, respectively. Locations and extents of fracture were evaluated by measuring the edge location of low-signal-intensity bands on coronal T1-weighted MR images. Stress distribution on subchondral bone in young patients was evaluated in contralateral unaffected hips with the same acetabular structure using finite element modeling based on CT.

RESULTS. Twelve hips were in young patients and 36 were in middle-aged and older patients. Hips in young patients showed retroversion in 41.7%, whereas those in middle-aged and older patients had dysplasia in 38.9%. Young patients had larger mediolateral fractures; fractures in middle-aged and older patients were laterally located. Anterosuperior fractures were seen in both groups. Contact stress in patients with retroversion was mainly distributed on the mediolateral and superior sides but was concentrated laterally and superiorly in one patient with dysplasia.

CONCLUSION. Mediolateral and anterosuperior fractures and stress distribution by retroversion were commonly observed in young patients, suggesting partial involvement of retroversion in the mechanism of injury of nontraumatic subchondral fractures of the FH in young patients.

Keywords: acetabular dysplasia, acetabular retroversion, finite element modeling, MRI, subchondral fracture of the femoral head

Subchondral fracture of the femoral head (FH) reportedly occurs without antecedent trauma; it is seen in elderly people with osteoporosis as an insufficiency fracture [1, 2]. In 1997, Visuri [3] reported that subchondral fracture of the FH also occurred as a fatigue fracture in 10 young military recruits. Later reports have described this injury in young patients with osteoporosis and in healthy young people even without evidence of overuse or general osteoporosis [46]. Because of the small number of reported cases, the causes of this fracture in young people remain unclear.

Several studies of elderly people with osteoporosis have reported a high prevalence of acetabular dysplasia, which suggests that ace-tabular structure may play a part in the occurrence of subchondral fracture of the FH [79]. Iwasaki et al. [10] suggested that insufficient acetabular coverage in patients with acetabular dysplasia can cause contact stress between the acetabulum edge and the lateral location of the FH, leading to lateral subchondral fracture.

To our knowledge, no previous study has investigated the effect of acetabular structure or location of subchondral fracture of the FH in young patients. We hypothesized that radiologic features of acetabular structure and fracture site in young patients would differ from those in middle-aged and older patients, which could shed light on causes of subchondral fracture of the FH in young patients. Therefore, the purpose of our study was to examine acetabular structure and fracture site of nontraumatic subchondral fracture of the FH in young patients compared with those in middle-aged and older patients.

Materials and Methods
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Patients

The institutional review board of Kyushu University approved this retrospective study. All subjects were informed that the data would be submitted and gave their consent. Fifty-one consecutive hips in 48 patients with nontraumatic subchondral fracture of the FH underwent MRI from January 2006 to March 2016. Of them, three hips had already shown severe osteoarthritic changes classified as Kellgren-Lawrence grade 4 on initial radiographs; these patients were excluded. We thus finally examined 48 hips in 45 patients with non-traumatic subchondral fracture of the FH, including 13 men (15 hips) and 32 women (33 hips) with a mean age of 56 years (range, 16–85 years). Using 40 years as the beginning of middle age, we divided subjects into two groups: patients younger than 40 years old (young) and patients 40 years or older (middle-aged and older). Body mass index (BMI), presence of osteoporosis on dual-energy x-ray absorptiometry (DEXA), history of regular strenuous physical activity, treatment of nontraumatic subchondral fracture of the FH, and time from pain onset to surgery were recorded for the two groups.

Diagnosis

Nontraumatic subchondral fracture of the FH was diagnosed in patients who fulfilled the following inclusion criteria: hip pain without any antecedent trauma; radiographs that showed collapse of the FH, linear patchy sclerotic areas in the FH, or both; bone marrow edema–like signal intensity in the FH, neck, or both on MRI; and a subchondral low-signal-intensity band on T1-weighted MRI that was serpentine or parallel to the articular surface [2, 11]. In addition, the histopathologic evidence of a subchondral fracture in patients treated surgically was confirmed by examining the completely resected FH or an intraoperative biopsy of the collapsed lesion [1, 2]. A curvilinear fracture with a whitish-gray appearance paralleling the subchondral bone endplate was macroscopically observed, and a whitish-gray area was microscopically observed, including an irregularly arranged fracture callus, reactive cartilage, and granulation tissue. Although necrotic lesions were not seen around the fracture, small necrotic lesions can be observed in association with a nontraumatic subchondral fracture of the FH. These lesions are confined to the area around the fracture line, with no evidence of an antecedent bone infarction. Gadolinium-enhanced MRI was performed in seven hips to differentiate nontraumatic subchondral fracture from osteonecrosis of the FH [12, 13]. On enhanced MRI, the proximal portion of the FH tends to show high signal intensity in nontraumatic subchondral fracture, whereas this portion is not enhanced in osteonecrosis [11]. Bone marrow edema–like signal intensity on MRI without FH collapse or a subchondral fracture was distinguished from nontraumatic subchondral fracture of the FH [14].

Treatment

All patients with subchondral fracture of the FH initially underwent nonoperative treatment consisting of rest and avoidance of weight-bearing activity for 6–8 weeks. Total hip arthroplasty (THA) was indicated for patients with osteoarthritic changes or progressive collapse on radiographs. Osteotomy was indicated for patients younger than 50 years old if one-third or more of the posterior region of the FH was intact [15].

Radiologic Assessment

Anteroposterior radiographs of the pelvis were obtained with the subject supine. The central axis of the beam radiated through the midpoint of the superior margin of the symphysis pubis and a line connecting the anterosuperior iliac spine. The rotation of lower limbs was standardized by positioning both patellas in an exact frontal position. Pelvic inclination was determined using the method described by Siebenrock et al. [16]. They measured the distance between the symphysis and the middle of the sacrococcygeal joint to evaluate pelvic tilt on anteroposterior radiographs, reporting that this distance significantly correlated with pelvic inclination. The normal distance between the symphysis pubis and the sacrococcygeal joint is 20–40 mm in men and 40–60 mm in women; these values were used to decrease measurement errors of the hip parameters according to the pelvic tilt.

MRI was performed with a 1.5- or 3-T system (Achieva, Philips Healthcare). Coronal and axial T1-weighted images (TR/TE, 400–748/8–20; FOV, 36 × 36 cm; slice thickness, 3–5 mm; inter-slice gap, 1 mm) were available for all patients.

The structure of the acetabular rim was evaluated by measuring the lateral center-edge angle (LCEA) on anteroposterior radiographs, and ace-tabular dysplasia was defined as the presence of an LCEA of less than 20° [17, 18] (Fig. 1). Acetabular retroversion was defined as the presence of a crossover sign (COS) on anteroposterior radiographs [19, 20] (Fig. 1). The Sharp angle (formed by a line connecting the lateral and inferior edges of the acetabulum and a horizontal line) and acetabular roof obliquity (formed by a line connecting the medial edge of the sourcil, the lateral edge of the acetabulum, and a horizontal line) were also measured on anteroposterior radiographs [17, 21, 22]. The acetabular anteversion angle was measured on an axial slice of the MRI examination using the method described by Anda et al. [23] (Fig. 1). In dysplastic hips, hip osteoarthritis was evaluated on antero-posterior radiographs using the Kellgren-Lawrence grading system [24]. Presence or absence of bone marrow edema–like signal intensity in the acetabulum was investigated in these patients using coronal T1-weighted MR images.

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Fig. 1A —Methods of measuring radiologic features of acetabulum.

A, Lateral center-edge angle (LCEA) is measured as angle formed by line connecting center of femoral head and lateral edge of acetabulum with sagittal line on coronal plane passing through center of femoral head.

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Fig. 1B —Methods of measuring radiologic features of acetabulum.

B, Crossover sign (COS) is created by anterior aspect of acetabular rim (solid line) being more lateral than posterior aspect (dotted line) in proximal portion of acetabulum.

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Fig. 1C —Methods of measuring radiologic features of acetabulum.

C, Acetabular anteversion angle is measured as angle formed by line connecting anterior and posterior edges of acetabulum and with sagittal line passing through center of femoral head on mid axial MR image.

Regarding sites of nontraumatic subchondral fracture of the FH, both mediolateral and antero-posterior locations and the extent of the subchondral fracture were evaluated by measuring the location of each edge (medial, lateral, anterior, and posterior) of subchondral low-signal-intensity bands on all coronal T1-weighted MR images (Fig. 2). Using the mediolateral and anteroposterior locations of the low-signal-intensity bands, the distribution of fractures was illustrated in the two groups.

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Fig. 2A —Location and extent of subchondral fracture of femoral head.

A, Extent of band is evaluated on coronal T1-weighted MR images (3- to 5-mm slice thickness) showing extent of subchondral low-signal-intensity bands.

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Fig. 2B —Location and extent of subchondral fracture of femoral head.

B, Illustrations show examples of bands on integrated images of coronal slices. Using extent of subchondral low-signal-intensity band on each slice, location of mediolateral edges of fracture and extent of fracture (B) are determined. Location of anteroposterior edges and extent of subchondral fracture (C) are determined according to location of each coronal slice with subchondral low-signal-intensity band.

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Fig. 2C —Location and extent of subchondral fracture of femoral head.

C, Illustrations show examples of bands on integrated images of coronal slices. Using extent of subchondral low-signal-intensity band on each slice, location of mediolateral edges of fracture and extent of fracture (B) are determined. Location of anteroposterior edges and extent of subchondral fracture (C) are determined according to location of each coronal slice with subchondral low-signal-intensity band.

All of the radiologic parameters, except for the COS, were measured using ImageJ software (National Institutes of Health).

Finite Element Modeling

The distribution of contact stress on the subchondral bone of the FH with acetabular retroversion in the young patient group on mid coronal and mid sagittal slices was separately evaluated using finite element models (FEMs). FEMs were generated for patients who had undergone CT. To remove the influence of the subchondral fracture of the FH, FEMs of each patient were generated in the contralateral unaffected hip with same acetabular structure. As a control, stress distribution of one contralateral dysplastic hip in the middle-aged and older patient group was also evaluated. CT data included both hip and knee joints in the helical mode in a 512 × 512 matrix, with a slice thickness of 2 mm or less (Aquilion, Toshiba). During the scan, patients were placed supine with their lower legs secured to the table using a below-knee splint to fix rotational position. FEMs were generated from DICOM CT data using Mechanical Finder software (version 7.0, Research Center for Computational Mechanics).

FEMs consisted of pelvises, articular cartilage, and femurs, which together represented unilateral hip joints. The structures were assumed to be completely bonded. FEMs had 2-mm tetrahedral elements for trabecular bones and 3-point shell elements with a thickness of 0.4 mm for the outer surface of cortical bones. Articular cartilage was modeled as homogeneous isotropic material, and the elastic modulus of bone was determined from CT attenuation values [25]. The attenuation in each element was calculated by the mean CT value in 17 points of a tetrahedral element using Mechanical Finder software. Subsequently, the bone mineral density (BMD) (in g/cm3) was determined according to these attenuation values, using a calibration equation described in previous studies [25, 26]. For attenuation values of of −1 HU or less, BMD was 0.0 g/cm3. For attenuation values above −1 HU,

where HU is the attenuation value. The elastic modulus (E) of each element was determined from the BMD value using equations described by Keyak et al. [26]. The Poisson ratio of pelvis and femur was 0.30 [27]. The elastic modulus and the Poisson ratio of articular cartilage were 10.35 and 0.40, respectively [25]. A load of 900 N was vertically applied to pelvis, and the distal part of femoral shaft was fully restrained [25, 28]. Finally, we compared the distribution of Drucker-Prager equivalent stress, a widely used method that treats the bone as a brittle material [29], on mid coronal and mid sagittal slices (which showed contact stress) of examinations of the FH.

Statistical Analysis

BMI, time from pain onset to surgery, and radiologic measurements were compared between the two groups using t statistics. LCEA less than 20° and COS were compared using the Pearson chi-square test. The relationship between time from pain onset to surgery and the extent of the mediolateral subchondral fracture of the FH was evaluated using the Pearson correlation coefficient. A single author measured all of the radiologic parameters twice 1 month apart. Two observers also measured them independently. Intra- and interobserver reliabilities were assessed using an intraclass correlation coefficient. Intraclass correlation was defined as almost perfect when a value exceeded 0.80. A value of p < 0.05 indicated statistical significance. All statistical analyses were conducted using JMP Pro software (version 11, SAS Institute).

Results
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Fracture was seen in 12 hips (11 in men, one in a woman) of 10 patients in the young patient group and in 36 hips (four in men, 32 in women) of 35 patients in the middle-aged and older patient group. The mean BMI in the young patient group was significantly lower than that in the middle-aged and older patient group (p < 0.01). Three of 11 hips (27%) in the young patients who underwent DEXA and 24 of 27 hips (89%) in the middle-aged and older patients who underwent DEXA showed osteoporosis. Of the 12 hips in the young patient group, seven (58%) were in patients whose occupation involved intense physical activity, including six hips in military personnel or police trainees. The patients with the remaining 41 hips reported no intense physical activity in daily life. For treatment of nontraumatic subchondral fracture of the FH, 12 hips in the young patient group and one hip in the middle-aged and older patient group underwent osteotomy, and 15 hips in the middle-aged and older patient group underwent THA. Conservative therapy was used to treat the remaining 20 hips in the middle-aged and older patient group. Mean time from pain onset to surgery in the young patient group was significantly shorter than that in the middle-aged and older patient group (p < 0.05). Table 1 summarizes the clinical data of the two groups.

TABLE 1: Demographic Characteristics of the Patients With Subchondral Fracture of the Femoral Head

For acetabular dysplasia, an LCEA of less than 20° was seen significantly more often in the middle-aged and older patient group (38.9%) than in the young patient group (0%) (p < 0.05). Significant differences were also seen in mean LCEA, sharp angle, and acetabular roof obliquity between the young patient group and the middle-aged and older patient group (p < 0.01, p < 0.01, and p < 0.001, respectively) (Table 2). Mild or moderate hip osteoarthritis classified as Kellgren-Lawrence grade 2 or 3 was seen in 12 of 14 dysplastic hips. These 12 hips had osteophytes and bone marrow edema–like signal intensity in the lateral side of the acetabulum a mean 1.3 months after the appearance of acute hip pain; similar findings were not seen in the acetabulum of the remaining two dysplastic hips.

TABLE 2: Radiologic Parameters of Acetabula in the Two Age Groups With Subchondral Fracture of the Femoral Head

For patients with acetabular retroversion, COS was seen significantly more often in the young patient group (41.7%) than in middle-aged and older patients (11.1%) (odds ratio, 5.71; 95% CI, 1.30–25.4; p < 0.05). In addition, the mean acetabular anteversion angle in the young patient group was significantly smaller than that in the middle-aged and older patient group (p < 0.0001) (Table 2).

Table 3 describes the characteristics of the young patient group. Acetabular retroversion was observed in only one of seven hips in young patients with a history of strenuous daily physical activity, whereas it was seen in four of five hips in young patients with no history of regular intense physical activity.

TABLE 3: Characteristics of Nontraumatic Subchondral Fracture of the Femoral Head in the Young Patient Group

With regard to mediolateral location, the medial edge of fractures in the young patient group was located more medially than that in the middle-aged and older patient group (p < 0.0001), but no significant difference was seen in the location of the lateral edge of fractures between the two groups (p = 0.45). The mediolateral extent of fractures in the young patient group was significantly larger than that in the middle-aged and older patient group (p < 0.0001) (Figs. 3 and 4).

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Fig. 3A —Comparison of location and extent of fractures in nontraumatic subchondral fracture of femoral head in young (< 40 years old; n = 12 hips) and middle-aged and older (≥ 40 years old; n = 36 hips) patients.

A, Graphs show mediolateral location and extent of fractures in young (A) and middle-aged and older (B) patients. Location of mediolateral edges of fractures was calculated as distance from femoral head center to mediolateral edges of bands divided by diameter of femoral head and multiplied by 100 to yield percentages shown. Mediolateral extent of fractures was calculated as distance from medial edges of bands to lateral edges of bands divided by diameter of femoral head and multiplied by 100 to yield percentages shown.

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Fig. 3B —Comparison of location and extent of fractures in nontraumatic subchondral fracture of femoral head in young (< 40 years old; n = 12 hips) and middle-aged and older (≥ 40 years old; n = 36 hips) patients.

B, Graphs show mediolateral location and extent of fractures in young (A) and middle-aged and older (B) patients. Location of mediolateral edges of fractures was calculated as distance from femoral head center to mediolateral edges of bands divided by diameter of femoral head and multiplied by 100 to yield percentages shown. Mediolateral extent of fractures was calculated as distance from medial edges of bands to lateral edges of bands divided by diameter of femoral head and multiplied by 100 to yield percentages shown.

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Fig. 3C —Comparison of location and extent of fractures in nontraumatic subchondral fracture of femoral head in young (< 40 years old; n = 12 hips) and middle-aged and older (≥ 40 years old; n = 36 hips) patients.

C, Graphs show anteroposterior location and extent of fractures in young (C) and middle-aged and older (D) patients. Location of anteroposterior edges of fractures was calculated as distance from femoral head center to anteroposterior edges of bands divided by diameter of femoral head and multiplied by 100 to yield percentages shown. Anteroposterior extent of fractures was calculated as distance from anterior edges of bands to posterior edges of bands divided by diameter of femoral head and multiplied by 100 to yield percentages shown.

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Fig. 3D —Comparison of location and extent of fractures in nontraumatic subchondral fracture of femoral head in young (< 40 years old; n = 12 hips) and middle-aged and older (≥ 40 years old; n = 36 hips) patients.

D, Graphs show anteroposterior location and extent of fractures in young (C) and middle-aged and older (D) patients. Location of anteroposterior edges of fractures was calculated as distance from femoral head center to anteroposterior edges of bands divided by diameter of femoral head and multiplied by 100 to yield percentages shown. Anteroposterior extent of fractures was calculated as distance from anterior edges of bands to posterior edges of bands divided by diameter of femoral head and multiplied by 100 to yield percentages shown.

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Fig. 4A —Subchondral fracture of femoral head (FH) and acetabular retroversion or dysplasia.

A, 21-year-old woman with subchondral fracture of FH and acetabular retroversion in left hip. Anteroposterior radiograph (A) shows crossover sign, and coronal T1-weighted MR image (B) shows mediolateral fracture (arrows).

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Fig. 4B —Subchondral fracture of femoral head (FH) and acetabular retroversion or dysplasia.

B, 21-year-old woman with subchondral fracture of FH and acetabular retroversion in left hip. Anteroposterior radiograph (A) shows crossover sign, and coronal T1-weighted MR image (B) shows mediolateral fracture (arrows).

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Fig. 4C —Subchondral fracture of femoral head (FH) and acetabular retroversion or dysplasia.

C, 52-year-old woman with subchondral fracture of FH and acetabular dysplasia in right hip. Anteroposterior radiograph (C) shows lateral center-edge angle of 17°, and coronal T1-weighted MR image (D) shows mediolateral fracture (arrows).

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Fig. 4D —Subchondral fracture of femoral head (FH) and acetabular retroversion or dysplasia.

D, 52-year-old woman with subchondral fracture of FH and acetabular dysplasia in right hip. Anteroposterior radiograph (C) shows lateral center-edge angle of 17°, and coronal T1-weighted MR image (D) shows mediolateral fracture (arrows).

For anteroposterior location, the anterior edge of fractures in the young patient group was located more anteriorly than that in the middle-aged and older patient group (p < 0.05), whereas there was no significant difference in the location of the posterior edge of fractures between the two groups (p = 0.56). Additionally, there was no significant difference in the anteroposterior extent of fractures between the two groups (p = 0.25) (Fig. 3).

The extent of the mediolateral subchondral fracture showed a moderate negative correlation with the time from pain onset to operation (r = −0.66; 95% CI, −0.83 to −0.37; p < 0.001) (Fig. 5).

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Fig. 5 —Graph shows correlation between time from pain onset to surgery and extent of mediolateral subchondral fracture (r = −0.66, p < 0.001).

The approximate distribution of fractures revealed that they were located from side to side in the mediolateral FH and on the anterior side in the young patient group but at the lateral and anterior sides of the FH in middle-aged and older patients (Fig. 6).

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Fig. 6A —Distribution of subchondral fractures of femoral head. Gray shows mean distribution area of fractures on integrated images of coronal slices.

A, Graph shows distribution of fractures in 12 hips in 10 young patients (< 40 years old).

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Fig. 6B —Distribution of subchondral fractures of femoral head. Gray shows mean distribution area of fractures on integrated images of coronal slices.

B, Graph shows distribution of fractures in 36 hips in 35 middle-aged and older patients (≥ 40 years old).

FEM analysis of the acetabulum showed four unaffected contralateral hips had radiologic parameters similar to those in the affected side (Table 4). Based on the results of this analysis, the mediolateral contact stress in three of four hips with retroversion was widely distributed from the lateral edge of the acetabular rim to the medial region. In the remaining hip (patient 3), it was laterally distributed. Conversely, mediolateral contact stress in dysplasia was concentrated around the lateral edge of the acetabular rim. The anteroposterior contact stress in all hips with retroversion and dysplasia was distributed from anterior to superior portions; in patient 3, it was posteriorly distributed (Fig. 7).

TABLE 4: Radiologic Parameters of Contralateral Unaffected Hips in the Young Patient Group
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Fig. 7 —Comparison of stress distribution and site of subchondral fracture of femoral head. Stress distribution on coronal (top row) and sagittal (middle row) slices created using finite element modeling in contralateral unaffected hips with same acetabular structure is shown, including four hips with acetabular retroversion in patients listed in Tables 3 and 4 (patient 1 in left hip [first column from left], patient 2 in right hip [second column from left], patient 3 in left hip [middle column], and patient 8 in right hip [second column from right]), and one hip with dysplasia in middle-aged and older patient group as control [first column from right]. Bottom row shows fracture site. Arrows indicate stress concentration on subchondral bone. Amount of contact stress is indicated by color bar. Med = medial, Lat = lateral, Post = posterior, Ant = anterior.

Intraobserver reliability of radiologic measurements was almost perfect (range, 0.868–0.989). Interobserver reliabilities of radiologic measurements for the two independent observers were also almost perfect (0.842–0.976 and 0.823–0.922).

Discussion
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In this study, acetabular retroversion was observed in 41.7% of young patients with subchondral fracture of the FH. To our knowledge, no previous studies have described the association of acetabular structure with this injury in young adults. Despite young patients having lower BMI and fewer occurrences of osteoporosis, subchondral fractures of the FH in this age group revealed statistically larger mediolateral fractures compared with those in middle-aged and older patients in our study. Song et al. [30] reported cases of subchondral fracture of the FH in young military recruits that showed mediolateral linear low-signal-intensity bands on coronal T1-weighted images. Similarly, in our study, approximately half of large subchondral fractures in young patients may have been caused by excessive stress from strenuous physical occupations. Interestingly, four of the remaining five young patients with no history of regular intense physical activity had acetabular retroversion. Additionally, FEM analysis showed mediolateral stress distribution on the subchondral bone in three of four hips with retroversion in young patients with subchondral fracture of the FH. These findings suggest a possible partial involvement of acetabular retroversion in the mechanism of injury of nontraumatic subchondral fracture of the FH in young people.

Middle-aged and older patients with subchondral fractures of the FH had a high frequency of acetabular dysplasia, which echoes findings in previous reports [810]. In our study, the location of the medial edge of subchondral fractures of the FH in young patients was located medially, unlike what was seen in middle-aged and older patients. FEM study of acetabular structure generally focuses on articular cartilage to evaluate the influence of contact stress on osteoarthritis [27, 31, 32]. Henak et al. [31, 32] reported that the contact pressure pattern on articular cartilage during walking in retroverted hips was localized medially. They also described that lateral loading on articular cartilage of the FH resulted in higher contact stress in dysplastic hips than in normal hips. In contrast, FEM is typically performed for bone when assessing the effect of contact stress on fracture [33]. To our knowledge, no previous reports have investigated the stress distribution on subchondral bone focusing on acetabular structure. Similar to these previous reports, we found that the contact stress on subchondral bone in retroverted hips was widely distributed from the lateral edge of the acetabular rim to the medial region. That in one dysplastic hip was concentrated on the lateral edge of the acetabular rim. These patterns were related to fracture site in young patients and middle-aged and older patients, respectively [31, 32]. Therefore, acetabular structure may affect the site of nontraumatic subchondral fracture of the FH through the contact stress on subchondral bone.

In the current study, the anteroposterior portion of fractures in either young or middle-aged and older patients was located anteriorly despite significant difference in the anterior edges of fractures between the two groups. Subchondral fracture has generally been reported to be localized in the anterior portion of the FH [10]. Our FEM analysis mainly revealed anterior or superior stress distribution in hips with retroversion and dysplasia. A recent biomechanical study using composite femur with a solid cancellous bone density suggested that external load caused subchondral fractures at the anterior FH [34]. However, hip flex position during daily activity causes anterior shift of the contact area and higher loading on the FH, which can be associated with nontraumatic subchondral fracture of the FH [35]. Previous studies using FEM also reported that anteroposterior contact stress on articular cartilage in dysplastic and retroverted hips varied during walking, stair descent, or stair ascent [31, 32, 36]. Therefore, kinetic analysis will be necessary to accurately evaluate anteroposterior stress distributions of subchondral bone in subchondral fracture of the FH.

We also evaluated bone marrow edema–like signal intensity in acetabula with dysplasia on MRI. Neumann et al. [37] reported a correlation of bone marrow edema–like signal intensity with cartilage loss in patients with mechanical symptoms of the hip on MR arthrography, indicating that its appearance may affect the development of hip osteoarthritis. A previous arthroscopic study also suggested that cartilage degeneration of the acetabulum with dysplasia usually preceded that of the FH in a prearthritic stage [38]. In our study, bone marrow edema–like signal intensity was observed in the acetabulum in 12 of 14 dysplastic hips on MR images that had been obtained a mean of 1.3 months after the onset of acute hip pain. Osteophyte formation on the lateral side of the acetabulum was also seen on radiographs. However, in a retrospective series like this one, proving a causal relationship between a fracture and osteoarthritis is difficult because it is unclear whether the osteoarthritic change existed before or after the occurrence of the fracture. Subchondral fracture of the FH has been reported in osteoarthritic hips [39]. Considering that MRI was performed shortly after the onset of acute hip pain, osteoarthritis may have already existed at the time of the fracture in these 12 dysplastic hips. However, subchondral fracture of the FH can lead to rapidly progressive osteoarthritic changes because of the simultaneous occurrence of subchondral fracture in the acetabulum [40]. Therefore, prospective studies are needed to investigate if osteoarthritic patients with hip dysplasia will develop subchondral fracture of the FH.

Recently, Yamaguchi et al. [41] reported a high prevalence of acetabular retroversion in 31 patients with transient osteoporosis of the hip (TOH), which is characterized by bone marrow edema–like signal intensity on MRI and temporary hip pain without antecedent trauma [14, 42]. Sixteen (52%) patients with TOH had acetabular retroversion [41]. The association of acetabular retroversion with subchondral fracture of the FH has yet to be discussed. In our study, some young patients with subchondral fracture of the FH also had acetabular retro-version, which was similar to what Yamaguchi et al. reported. Additionally, subchondral fracture of the FH has been proposed to be partially associated with TOH; Miyanishi et al. [43] reported detecting a subchondral band on hip MRI in 12 hips of 11 patients with TOH in their study, similar to what has been found in young patients with subchondral fracture of the FH [1, 11]. Although TOH is generally observed in middle-aged men or pregnant women, the combination of structural and radiologic findings in TOH may indicate a pathologic condition similar to that in young patients with subchondral fracture of the FH [44, 45].

This study had several limitations. First, the sample size was small because of the rarity of nontraumatic subchondral fracture of the FH in young people. Several studies have suggested that the evaluation of COS determined from anteroposterior radiographs can be influenced by pelvic tilt [46, 47]. In our study, however, posterior pelvic tilt was within the normal range in all patients [16]. In addition, COS was seen at a higher rate in young patients with subchondral fracture of the FH (41.7%) than that reported by Ezoe et al. [48] in normal hips (7%). Second, in our correlation analysis, the more extensive the mediolateral subchondral fracture of the FH, the shorter the time from pain onset to surgery. Additionally, the time in young patients with subchondral fracture of the FH was significantly shorter than that in middle-aged and older patients. Eventually, all young patients in our study underwent osteotomy. Considering that osteotomy needs to be performed as soon as possible before the occurrence of subsequent rapid osteoarthritic changes in the subchondral fracture of the FH, type of surgery may affect patients' pain duration [15]. Third, our FEM analysis assumed that the femur was rigidly connected to the acetabulum through the cartilage. More sophisticated FEM analysis is needed to consider the effects of surrounding muscles or friction between acetabular and FH cartilage. The detailed mechanism causing nontraumatic subchondral fracture of the FH remains unknown. However, the results of our study suggest that acetabular dysplasia and retroversion may affect the fracture site of nontraumatic subchondral fracture of the FH. Further studies to evaluate bone tissues in hips with acetabular abnormality at specific potential fracture sites using the compression test may be needed to elucidate the mechanism of injury of nontraumatic subchondral fracture of the FH.

Conclusion
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Mediolateral and anterosuperior fractures in correspondence with stress distribution by retroversion were commonly observed in young patients with subchondral fracture of the FH; different radiologic features were seen in middle-aged and older patients with subchondral fracture of the FH. Additionally, young patients with subchondral fracture of the FH but no history of regular intense physical activity largely had acetabular retroversion. These results suggest that acetabular retroversion may be partially involved in the mechanism of injury of nontraumatic subchondral fracture of the FH in young patients.

Supported in part by a grant-in-aid in Scientific Research (19K09601) from the Japan Society for the Promotion of Science.

Acknowledgments
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We thank Koichiro Kawano, Mingjian Xu, and Kenji Kitamura (Department of Orthopaedic Surgery, Graduate School of Medical Sciences, Kyushu University) for their assistance in revising the manuscript.

References
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Address correspondence to G. Motomura ().

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