Radiologic Measurements Associated With the Prognosis and Need for Surgery in Patients With Subchondral Insufficiency Fractures of the Femoral Head

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1 Musculoskeletal Imaging Original Research Iwasaki et al. Measurement of Femoral Fractures Musculoskeletal Imaging Original Research Kenyu Iwasaki 1 Takuaki Yamamoto Goro Motomura Satoshi Ikemura Ryosuke Yamaguchi Yukihide Iwamoto Iwasaki K, Yamamoto T, Motomura G, Ikemura S, Yamaguchi R, Iwamoto Y Keywords: acetabular coverage, MRI, prognosis, subchondral insufficiency fracture of the femoral head DOI: /JR Received July 6, 2012; accepted after revision October 28, Supported in part by a grant-in-aid in scientific research ( ) from the Japanese Society for the Promotion of Science, a research grant from the Osteoporosis Foundation, and a grant-in-aid from the Japanese Society for the Promotion of Science Fellows ( ). 1 ll authors: Department of Orthopaedic Surgery, Graduate School of Medical Sciences, Kyushu University, Maidashi, Higashi-ku, Fukuoka , Japan. ddress correspondence to T. Yamamoto (yamataku@ortho.med.kyushu-u.ac.jp). WE This is a web exclusive article. JR 2013; 201:W97 W X/13/2011 W97 merican Roentgen Ray Society Radiologic Measurements ssociated With the Prognosis and Need for Surgery in Patients With Subchondral Insufficiency Fractures of the Femoral Head OJECTIVE. The objective of this study was to identify the risk factors associated with the prognosis and need for surgery of patients with subchondral insufficiency fractures of the femoral head. MTERILS ND METHODS. Twenty-nine consecutively registered patients with subchondral insufficiency fractures of the femoral head were divided into the two groups: a nonprogression of group, which included patients who had no or 2 mm or less of of the femoral head and whose symptoms resolved (14 patients), and a progression of group, which included patients who had more than 2 mm of, for which surgery was indicated (15 patients). oth groups received the same conservative therapy. The following radiographic measurements were obtained: Sharp angle, center edge angle, acetabular roof angle, and acetabular head index. On MR images, band length, defined as the length of a lowsignal-intensity band in the coronal plane, and band length ratio, defined as the proportion of the band length relative to the weight bearing portion, were assessed for each patient. one mineral density measurements (T score) were available for 17 patients. RESULTS. In the univariate analyses, T score, Sharp angle, center edge angle, acetabular roof angle, acetabular head index, band length, and band length ratio were found to be significant prognostic factors. Multivariate analyses of T score, acetabular head index, and band length ratio showed that both acetabular head index and band length ratio were significant predictors. CONCLUSION. oth acetabular head index and band length ratio are important prognostic factors in the care of patients with subchondral insufficiency fractures of the femoral head. S ubchondral insufficiency fractures of the femoral head often occur in elderly persons with osteoporosis [1 9]. These patients usually have acute hip pain without any obvious antecedent trauma. t the onset of hip pain, radiographs generally show no abnormalities [4, 5, 10], but T1-weighted MR images show bands of very low signal intensity in the subchondral area of the femoral head that tend to be irregular, disconnected, and parallel to the articular surface [2, 4, 5, 7, 9, 11]. These low-intensity bands have been proved histologically to correspond to fracture lines associated with repair tissue [5, 9]. Some cases of subchondral insufficiency fractures of the femoral head resolve after conservative treatment [5, 10 14]. Others entail further of the femoral head that necessitates surgical treatment [4 10, 15]. The prognosis of patients with these fractures remains unknown. In a 2012 MRI study [16], we proposed that band length seems to be a prognostic factor for subchondral insufficiency fractures of the femoral head. That analysis was based on MRI evaluation only and excluded radiographic factors. Ishihara et al. [17], however, reported that acetabular coverage was inadequate in comparison with that observed in a control group, in which the prognosis of the fractures was not evaluated. We therefore believe that more detailed analysis that includes clinical data, radiographs, and MR images is necessary for evaluating prognosis. The purpose of this study was to investigate the risk factors that influence the prognosis of subchondral insufficiency fractures of the femoral head, including clinical data, adequacy of acetabular coverage, and band length on MR images. Materials and Methods Our institutional review board approved this retrospective study. JR:201, July 2013 W97

2 Iwasaki et al. Patients We retrospectively reviewed the records of 29 consecutively registered patients who received the diagnosis of subchondral insufficiency fractures of the femoral head at our institution between 2002 and 2009 and underwent follow-up for at least 2 years. The diagnosis of subchondral insufficiency fracture of the femoral head was based on the following published criteria [4, 5, 10]: hip pain that began without an apparent history of trauma; normal radiographic findings or radiographs showing of the femoral head or linear patchy sclerotic areas in the superior portion of the femoral head, or both, and MR images showing bone marrow edema patterns in the femoral head or neck; and subchondral bands of low signal intensity on T1-weighted MR images that were serpiginous or paralleled the articular surface. The study included eight men and 21 women (age range, years; mean, 57.5 years). Patients with a history of any previous surgery (one patient), trauma (one patient), infection of the hip joint (one patient), or Perthes disease (two patients) had been excluded. To clarify that none of the patients had either osteonecrosis or metabolic bone disease, both hematologic and histopathologic examinations were performed on the patients who underwent surgery. That is, either bone biopsy or resected femoral head specimens were histopathologically evaluated. ll patients initially underwent conservative treatment, which consisted of rest and avoidance of weight bearing activities for 6 8 weeks. To evaluate the progression of of the femoral head, all patients underwent both clinical assessment and follow-up radiography 1, 2, 4, 6, and 12 months after the start of treatment. If progressed, surgical treatment was indicated. In the patients who did not undergo surgery, follow-up MR images were obtained approximately 6 or 12 months after the first evaluation. In these patients, no abnormal findings were found on the follow-up MR images. flowchart of outcome of the 29 patients is shown in Figure 1. t the first evaluation, seven patients had no of the femoral head, 16 patients had slight ( 2 mm), and six patients had severe (> 2 mm). The 29 patients with injured hips were divided into two groups: those without progression of and those with progression of of the femoral head. Seven patients without of the femoral head at first evaluation had no at the end of the follow-up (2 years). Of the 16 patients with slight ( 2 mm) at the first evaluation, eight had no progression by the end of follow-up. Less than 1-mm progression was considered nonprogression. The 15 patients who had no t first evaluation t the end of follow-up No (n = 7) No (n = 7) Cure No progression group (n = 15) or no progression of were the nonprogression group (Fig. 1). Eight of the 16 patients who had slight of the femoral head at the first evaluation had progression of, which necessitated surgery. ll six patients who had severe at first evaluation had progression of, also necessitating surgery. More than 1-mm progression was considered progression of. Fourteen patients were in the progression group (Fig. 1). ll of the patients who had resolution of symptoms after conservative treatment were included in the nonprogression group, and all of the patients who underwent surgical treatment after undergoing similar conservative treatment were included in the nonprogression group. In our experience, more than 2-mm in any followup period usually results in arthritis. Therefore, surgical treatment was suggested to patients who continued to have intractable pain and had more than 2-mm while undergoing conservative treatment. The cutoff point in this study was when the symptoms and all abnormal MRI findings disappeared (nonprogression group) or when surgery was performed (progression group). The mean time span from first visit to surgery was 3.9 months 29 Patients with SIF Slight 20 mm (n = 16) No progression of (n = 8) Progression of (n = 8) Surgery Progression group (n = 14) Severe > 20 mm (n = 6) Progression of (n = 6) Fig. 1 Flowchart shows outcome for all 29 patients with subchondral insufficiency fractures of the femoral head (SIF). More than 1-mm additional was considered progression of. In seven patients who did not have at first evaluation, fractures resolved after conservative therapy. Eight of 16 patients who had slight ( 2 mm) at first evaluation had progression of during conservative therapy, which necessitated surgery. Other eight patients did not have progression of. In six patients with severe (> 2 mm), progressed, necessitating surgery. (range, months). Three patients younger than 30 years who had an intact area in the posterior portion of the femoral head underwent anterior rotational osteotomy. The other 11 patients in the progression group underwent hip arthroplasty. ody mass index (MI; weight in kilograms divided by the square of height in meters) [18] and the length of the follow-up period were documented for each patient. Four of the 29 patients had known diagnoses of osteoporosis (three patients used bisphosphonates), three had a history of corticosteroid therapy, and one had chronic renal failure. one mineral density measurements of the proximal femur were obtained for 17 patients by dual-energy x-ray absorptiometry. Radiologic Measurements of Inadequate cetabular Coverage Radiographs were obtained throughout the study period with the same technique consisting of anteroposterior hip and frog leg lateral views. t the first evaluation, the presence of was assessed on anteroposterior radiographs. The following radiographic measurements were recorded on radiographs obtained at the first evaluation: Sharp angle [19], center edge angle, acetabular roof angle [20], and acetabular head index (HI) [21] (Fig. 2). W98 JR:201, July 2013

3 Measurement of Femoral Fractures b Two authors independently investigated the radiographs of all of the patients. They determined all markings and reference points, including femoral head center, lateral acetabular margin, and the distal point of the teardrop, on the radiographs. fter this process was completed, one of the investigators made the measurements. To test the reproducibility of the findings, one author measured all of the radiographs two times with an interval of 2 weeks separating the measurements. The values were averaged and statistically analyzed. Fig. 3 and length and band length ratio. a = band length, b = weight bearing portion of femoral head, defined as area lateral to midvertical line through acetabular edge and teardrop bottom. and length ratio is a/b., Diagram shows method used to measure length of low-signal-intensity band and band length ratio on T1-weighted MR images., 53-year-old woman with right hip pain. T1- weighted MR image (TR/TE, 413/11) shows lowsignal-intensity band just beneath articular cartilage. a α γ 3. MRI Evaluations of the Size and Location of the Low-Signal-Intensity ands Twenty patients underwent MRI with a 1.5-T system (Magnetom Symphony or Vision, Siemens Healthcare, or chieva, Philips Healthcare), and nine patients underwent MRI with a 3-T system (chieva). T1-weighted images (TR/TE, 400 cetabular edge and b a β Teardrop bottom Fig. 2 Radiographic measurements., Drawing shows radiographic indexes used for evaluation of hip. 1 = horizontal line between pelvic teardrops, 2 = line between lateral edge of acetabular roof and inferior tip of pelvic teardrop, 3 = line between lateral edge of acetabular roof and center of femoral head, 4 = line between lateral edge of acetabular roof and intersection of horizontal and vertical components of acetabulum, α = Sharp angle, β = center edge angle, γ = acetabular roof angle., Drawing shows measurements for acetabular head index, which is calculated as a/b 100, where a is distance between medial tip of femoral head and lateral edge of acetabular roof and b is size of femoral head. 600/8 19; FOV, 62 cm 2 ; matrix, ; slice thickness, 3 5 mm) and T2-weighted images (TR/TE, /81 108; FOV, 62 cm 2 ; matrix, ; slice thickness, 3 5 mm) in the coronal and axial planes (or oblique axial plane paralleling the femoral neck axis) were available for all of the patients. and lengths and band length ratios were evaluated with previously reported methods [16]. The band lengths and band length ratios were measured on the coronal T1-weighted MR images. and length was measured in the slice in which the longest band was detected. and length ratio was measured in the slice through the center of the femoral head. The weight bearing portion of the femoral head was defined as the area lateral to the midvertical line through the acetabular edge and the bottom of the teardrop. The band length ratio represents the band length relative to the weight bearing portion (Fig. 3). Three authors assessed all of the MR images blinded and independently estimated the values. We calculated the mean of the three values. To test the reproducibility of the findings, one author measured all of the values two times with an interval of 2 weeks separating the measurements. The values were averaged and statistically analyzed. ll of the measurements on the MR images were JR:201, July 2013 W99

4 Iwasaki et al. analyzed with image analysis software programs (CIS-Image Viewer, IM; Image J, National Institutes of Health; and Synapse, Fujifilm). Fig year-old woman with severe right hip pain., Radiograph obtained at first evaluation shows no abnormalities. Sharp angle, 43.4 ; center edge angle, 27.7 ; acetabular roof angle, 17.1 ; acetabular head index, 77.3., T1-weighted MR image (TR/TE, 400/15) shows low-signal-intensity band (arrows) immediately beneath articular cartilage. and length, 8.8 mm; band length ratio, 27.7%. C, Radiograph obtained 24 months after and shows no progression of in femoral head. Statistical nalysis Differences in age, MI, length of follow-up period, Sharp angle, center edge angle, acetabular roof angle, HI, band length, and band length ratio in the nonprogression and progression groups were analyzed by unpaired Student t test. The Fisher exact test was used to analyze the sex proportions. Differences with p < 0.05 were considered statistically significant. We conducted multivariate analyses using stepwise discriminant analysis after selecting the variables that were significant in the univariate analysis. Using these variables, we also performed a multivariate analysis adjusted for age, sex, and MI. The cutoff points for these radiographic variables were calculated with receiver operating characteristic (ROC) curves. The area under the ROC curve (UC) was used to test the useful prognostic factors. n area of 1 represented a perfect test, and an area of 0.5 represented a worthless test. The survivorship data were calculated by Kaplan-Meier analyses, and the survival curves of the two groups were compared by use of a log-rank test. To evaluate the intraobserver and interobserver reproducibility of the measurements obtained from the radiographs, we evaluated the reliability of the measurements using Spearman correlation coefficient. Values greater than 0.7 were considered to be in good agreement. ll of the statistical analyses were performed with the JMP software program (version 9.0.1, SS Institute). Results Clinical Data ll of the patients had unilateral fractures. The follow-up periods ranged from 2.2 to 6.0 years (mean, 3.4 years). The group without progression of of the femoral head included 15 patients, and the progression group included 14 patients (Figs. 4 and 5). The clinical data are summarized in Table 1. No sig- Fig year-old woman with severe right hip pain., Radiograph obtained at first evaluation shows slight of femoral head and slightly inadequate acetabular coverage. Sharp angle, 45.5 ; center edge angle, 24.8 ; acetabular roof angle, 19.5 ; acetabular head index, 71.4., T1-weighted MR image (TR/TE, 470/15) shows low-signal-intensity band (arrows) immediately beneath articular cartilage. and length, 17.0 mm; band length ratio, 52.7%. C, Radiograph obtained only 3 months after and shows progression of of femoral head. C C W100 JR:201, July 2013

5 Measurement of Femoral Fractures nificant differences were observed in sex, age, MI, or length of follow-up period. Radiographic Findings The radiologic measurements are summarized in Table 1. one mineral density measurements were available for 17 patients and indicated either osteopenia (T score between 1.0 and 2.5) or osteoporosis (T score less than 2.5) in 12 patients [22]. The mean bone mineral density of the patients in the progression group was significantly less than that of the patients in the nonprogression group. oth mean Sharp angle and mean TLE 1: Characteristics of 29 Study Participants and Radiologic Measurements Characteristic Nonprogression Group (n = 15) Progression Group (n = 14) p Sex (no.) Men 5 3 Women ge (y) 60.4 ± ± ody mass index 23.2 ± ± Follow-up period (y) 3.4 ± ± one mineral density (T score) 1.26 ± 0.41 a 2.13 ± 0.63 b Sharp angle ( ) 40.1 ± ± Center edge angle ( ) 30.3 ± ± cetabular roof angle ( ) 14.8 ± ± cetabular head index 79.9 ± ± and length (mm) 13.2 ± ± and length ratio (%) 38.2 ± ± Note Except for sex, values are mean ± SD. a n = 9. b n = 8. TLE 2: Results of Multivariate nalyses With Logistic nalysis Measurement Chi Square p a p b and length ratio < cetabular head index < one mineral density (T score) a Obtained from three parameters (T score, acetabular head index, and band length ratio). b Obtained from respective analyses adjusted for age, sex, and body mass index. TLE 3: Receiver Operating Characteristic Curves Measurement Sensitivity (%) Specificity (%) Cutoff rea Under Curve cetabular head index and length ratio % TLE 4: Linear Correlations etween Measurements (Spearman Correlation Coefficient) Measurement Intraobserver Reproducibility Interobserver Reproducibility Sharp angle Center edge angle cetabular roof angle cetabular head index and length and length ratio acetabular roof angle in the patients in the progression group were significantly greater than those of the patients in the nonprogression group, but both mean center edge angle and mean HI of the patients in the progression group were significantly less than those of the patients in the nonprogression group. That is, the patients in the progression group had a tendency toward inadequate acetabular coverage in all four values compared with that observed in the patients in the nonprogression group. MRI Evaluations oth the mean band length and mean band length ratio of the patients in the progression group were significantly greater than those of the patients in the nonprogression group (Table 1). Multivariate nalysis T score, HI, and band length ratio were selected from the results of the univariate analyses for the multivariate analysis. multivariate analysis including T score, HI, and band length ratio revealed significant differences in mean HI and mean band length ratio between the nonprogression group and the progression group. multivariate analysis adjusted for age, sex, and MI showed significant differences in T score, HI, and band length ratio (Table 2). Receiver Operating Characteristic Curves and Kaplan-Meier Survivorship nalysis The ROC curves established the cutoff points for HI and band length ratio (Table 3). In the ROC tests, all UCs for HI and band length ratio showed good results (> 0.8). In the Kaplan-Meier survivorship analysis, these cutoff points were used to predict 2-year survival rates for HI and band length ratio. Significant differences between the two groups were found with the log-rank test (Fig. 6). Interobserver and Intraobserver Variability The interobserver and intraobserver coefficients of variability for Sharp angle, center edge angle, acetabular roof angle, HI, band length, and band length ratio are summarized in Table 4. The linear correlations between the measurements (Spearman correlation coefficient) were considered to be in good agreement (> 0.7) for all of the measurements. Discussion The results of this study showed that the adequacy of acetabular coverage (HI) and band length ratio may be useful for predict- JR:201, July 2013 W101

6 Iwasaki et al. Survival Rate p < Survival Time (y) ing the progression of and need for surgery in patients with subchondral insufficiency fractures of the femoral head. Regarding the occurrence of these fractures, Ishihara et al. [17] reported that the fractures were associated with inadequate acetabular coverage compared with that observed in a control group. Those authors suggested that excessive stress on the acetabular edge might be associated with the fractures. In this study we also found that inadequate acetabular coverage represented by measurements of Sharp angle, center edge angle, acetabular roof angle, and HI seems to be a prognostic factor in the treatment of subchondral insufficiency fractures of the femoral head. Previous studies [23, 24] showed that joint contact pressure associated with inadequate acetabular coverage is concentrated on the lateral edge of the acetabulum. In subchondral insufficiency fractures of the femoral head, which are associated with inadequate acetabular coverage, increased joint contact pressure on the lateral edge adds mechanical stress to the area of the subchondral fracture. This increased pressure may cause further and result in incongruity of the femoral head. The shape of the very-low-signal-intensity band on T1-weighted MR images is a characteristic finding of subchondral insufficiency fractures of the femoral head. This band is generally irregular, serpiginous, and convex to the articular surface and is often discontinuous [2, 4, 5, 7, 9, 11]. Histopathologically, the bands observed in these insufficiency fractures represent fracture lines associated with repair tissue [4, 5, 10]. ecause the bands correspond to fracture lines, HI > 76.8 HI p < Fig. 6 Kaplan-Meier survival curve shows survival rate. Endpoint is time when operation was performed., Two-year survival rate in higher acetabular head index (HI) group is 86.2% and in lower HI group is 8.3%., Two-year survival rate in lower band length ratio group is 82.5% and in higher band length group is zero. Survival Rate Survival Time (y) and length ratio 57.9 and length ratio > band length represents the length of the subchondral fracture, and the band length ratio represents the proportion of the subchondral fracture relative to the weight bearing portion of the femoral head. s found in this study, band length and band length ratio both are important for prognosis in the care of patients with subchondral insufficiency fractures of the femoral head. These results are consistent with those of a previous MRI study showing that both band length and band length ratio are important prognostic factors [16]. ecause the previous study analyzed only MR images, in this study we evaluated both MR images and radiographs, making it possible to make a more precise prognostic prediction. Subchondral fractures of the femoral head have been observed in young military trainees, but such cases are considered fatigue stress fractures [25 27]. In this study, eight patients were younger than 50 years, and three patients were younger than 30 years. Only one patient had participated in sports (badminton in high school), and no patient had a history of overexertion. ecause three patients younger than 30 years had progression of necessitating surgery (anterior rotational osteotomy), we performed biopsy on these three patients. The histologic examinations showed thin, disconnected bone trabeculae, indicating the presence of osteopenia, and hematologic studies showed no evidence of bone metabolic disease. On the basis of these clinical and histologic findings, we made the diagnosis of insufficiency fracture and thus ruled out fatigue fracture in these young patients. In the current study, the indication for surgery was based on the degree of and hip pain. That is, surgical treatment was suggested to patients with more than 2-mm and who had intractable hip pain. The main limitations of this study were small sample size and the retrospective observational design. ecause subchondral insufficiency fracture of the femoral head is a newly proposed concept, further large prospective studies are necessary. In addition, in this study bone mineral density (T score) was found in univariate analysis to be a significant risk factor. However, the multivariate analysis that included three parameters (T score, HI, and band length ratio) showed that a patient s T score was not a significant factor. ecause the number of patients who underwent bone mineral density measurement was small (17 patients), further investigation is needed to clarify the association between bone mineral density and the prognosis of subchondral insufficiency fractures of the femoral head. In this study, the prognoses among patients with subchondral insufficiency fractures of the femoral head varied, even though all of the patients initially underwent similar conservative treatment. dequacy of acetabular coverage and band length ratio seem to be useful for predicting progression of and the need for surgery in patients with these fractures. References 1. angil M, Soubrier M, Dubost JJ, et al. Subchondral insufficiency fracture of the femoral head. Rev Rhum Engl Ed 1996; 63: Rafii M, Mitnick H, Klug J, et al. 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