Novel MRI technique for the quantification of biochemical deterioration in steroid-induce osteonecrosis of femoral head: a prospective diagnostic trial

Abstract

To explore the novel magnetic resonance imaging techniques, IVIM-DWI and IDEAL-IQ in detecting bone marrow fat and microcirculation in steroid-induced osteonecrosis of the femoral head (SIONFH). In this prospective study, 49 patients (80 hips) with SIONFH taking glucocorticoids and 24 healthy volunteers (48 hips) were recruited and assessed by T1WI, T2WI/fs, IDEAL-IQ and IVIM-DWI. The affected hips, contralateral asymptomatic hips and normal hips, as well as normal, penumbra and necrotic areas in the affected hips, were classified and evaluated. Imaging results were compared with histologic bone sections obtained from SIONFH patients undergoing surgery. The fat fraction (FF) and perfusion fraction (f) differences between groups were analyzed using analysis of variance, the LSD t-test, Pearson correlation analysis and ROC curve analysis. Our results demonstrate that IDEAL-IQ (FF) and IVIM-DWI (f) enable the classification of SIONFH at different ARCO stages. The FF was positively associated with the progression of the disease (r = 0.72), in contrast to f (r = −0.17). The FF and f were significantly different among the necrotic, penumbra and normal areas, and they were negatively correlated with each other (r = −0.37). The diagnostic sensitivity and specificity of IDEAL-IQ were 96.9% and 86.7%, and those of IVIM-DWI were 72.34% and 58.33%, respectively. The FF in contralateral asymptomatic hips was significantly higher than in normal hips, but no difference was found for f. IDEAL-IQ, and not IVIM-DWI, was identified to successfully detect bone marrow fat, which is beneficial to the diagnosis of the severity of SIONFH.

INTRODUCTION

Steroid-induced osteonecrosis of the femoral head (SIONFH) is a chronic and devastating bone disease caused by prolonged and excessive glucocorticoid administration [1]. Glucocorticoid treatment leads to biochemical deterioration in the femoral head, including bone marrow fat deposition and poor perfusion of microcirculation, which is detected by histopathology [2]. Conventional morphological magnetic resonance imaging (MRI) is non-invasive and shows high accuracy in the detection of bone marrow osteonecrosis; however, it lacks the ability to detect biochemical deterioration of the femoral head in SIONFH [3]. It has been reported that 50–70% of cases of osteonecrosis of the femoral head (ONFH) have bilateral hip lesions [4–7], whereas the secondary hip is usually asymptomatic and shows no pathological signs in conventional MRI before the emergence of necrotic signs, possibly due to different susceptibilities of the two hips [8, 9]. Thus, even without osteonecrosis being detected, it is hypothesized that glucocorticoid induces biochemical deterioration in the asymptomatic hip. Because of the limitation of current MRI technology, such patients cannot be distinguished and undergo suitable treatments in advance [1, 10]. This poses great challenges with respect to the exploration of novel imaging techniques for the detection of biochemical substances in the femoral head.

In this prospective diagnostic trial, we used iterative decomposition of water and fat with echo asymmetry and least square estimation–iron quantification (IDEAL-IQ) and intravoxel incoherent motion–diffusion-weighted imaging (IVIM-DWI) as complementary techniques to assess the biochemical deterioration in SIONFH. IDEAL-IQ provides data of bone marrow fat content through detecting ‘in-phase’ and ‘out-phase’ images of water–fat signals [11]. Previous imaging studies revealed that IDEAL-IQ enables the quantitative analysis of the fat deposition in the bone marrow of different bone sites, such as the lumbar vertebral body, the ilium and the intertrochanteric region of the femur [11, 12]. IVIM-DWI accurately and non-invasively characterizes the microcirculation by detecting the diffusion and perfusion of water molecules in tissues [13]. Recent studies have demonstrated that IVIM-DWI performs excellently in the evaluation of bone marrow diffusion in multiple diseases, e.g. myeloma lesions and hepatocellular carcinoma [13–15]. Thus, both techniques may have the potential to be applied in osteonecrosis patients to examine the changes in biochemical composition of the bone marrow in the femoral head, particularly if no morphological features are observed.

Therefore, the purpose of this study is to explore the efficiency of IVIM-DWI and IDEAL-IQ in the evaluation of the bone marrow fat content and microcirculation in SIONFH, respectively. It is hypothesized that IVIM-DWI and IDEAL-IQ can help to detect the increased fat deposition and reduced perfusion in bone tissue and provide an early diagnosis of SIONFH.

MATERIALS AND METHODS Participants

In total, 73 participants (41% male and 59% female; median age, 61 years; range, 45–79 years) were recruited from our institution between September 2017 and November 2018, i.e. (i) 49 participants (80 hips) who were diagnosed according to the Chinese Guideline for the Diagnosis and Treatment of Osteonecrosis of the Femoral Head in Adults [16] and evaluated using the ARCO classification (defined by conventional MRI prior to formal tests) (Supplementary Table SI) [17] and (ii) 24 healthy volunteers (48 hips). The characteristics of the participants are summarized in Supplementary Table SII. All SIONFH patients had received glucocorticoid treatment for more than 3 months (>2000 mg), were no excessive alcohol drinkers (alcohol addicts with a drinking history of at least 10 years) and had no hip trauma. Participants with ARCO Stage IV ONFH were excluded due to the mixed MRI signals in the femoral head, leading to possible misdiagnosis. Participants who had undergone surgical procedures for hip treatment prior to our research were also excluded. SIONFH individuals were identified within the institution from multiple referring specialties. This diagnostic prospective study was approved by the institutional review board in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) (Supplementary Table SIII). Written informed consent was obtained from each subject.

Three analysis strategies were used in our study. (i) The affected hips in the bilateral and unilateral cases were classified according to ARCO stage and compared with hips of the healthy volunteers. (ii) Affected hips were divided into three areas, i.e. the normal, penumbral and necrotic areas. (iii) The necrotic areas of the affected hips in the bilateral and unilateral cases were defined as the exposed group, the contralateral asymptomatic hips in the unilateral cases (in the absence of necrotic MRI signals) were defined as the risk group, and the hips of healthy volunteers were defined as the control group.

MRI protocols

All individuals underwent MRI scanning of bilateral hip joints in the supine position using HDxt 3.0T magnetic resonance (Discovery MR750 3T, GE Healthcare, Milwaukee, WI, USA) equipped with a phase array coil (Philips Healthcare, The Netherlands). The lower extremities of the participants were fixed as hip extension and neutral rotation. In the sagittal position, the line of MRI acquisition was parallel to the femoral neck and passed through the center of the femoral head. Scans of both hips were obtained simultaneously. The scan line was set between the anterior-superior iliac spine and the pubic symphysis. The scanning sequences included sagittal and coronal T1-weighted imaging (T1WI), coronal fat-suppressed T2-weighted imaging (T2WI/fs), sagittal IDEAL-IQ and sagittal IVIM-DWI. The imaging parameters are presented in Table I.

Table I.

MRI protocol for IDEAL-IQ and IVIM-DWI

MRI protocol .  . MRI sequence . T1WI . T2WI/fs . IDEAL-IQ . IVIM-DWI . Position Sagittal/Coronal Sagittal Sagittal Sagittal TR (ms) 617 2900 4.8 5200 TE (ms) 16 1.3 1.5 68 FOV (mm × mm) 260 × 260 310 × 310 320 × 320 320 × 300 Matrix 512 × 288 288 × 224 384 × 512 320 × 300 Slice thickness (mm) 4 3 3 3 Slice gap (mm) 0.5 0.6 0.5 0.5 b-values (s/mm2) / / / 10, 20, 30, 50, 80, 100, 200, 400, 800, 1000 Total scan time 11 min 15 s 4 min 6 s 2 min 34 s 3 min 12 s MRI protocol .  . MRI sequence . T1WI . T2WI/fs . IDEAL-IQ . IVIM-DWI . Position Sagittal/Coronal Sagittal Sagittal Sagittal TR (ms) 617 2900 4.8 5200 TE (ms) 16 1.3 1.5 68 FOV (mm × mm) 260 × 260 310 × 310 320 × 320 320 × 300 Matrix 512 × 288 288 × 224 384 × 512 320 × 300 Slice thickness (mm) 4 3 3 3 Slice gap (mm) 0.5 0.6 0.5 0.5 b-values (s/mm2) / / / 10, 20, 30, 50, 80, 100, 200, 400, 800, 1000 Total scan time 11 min 15 s 4 min 6 s 2 min 34 s 3 min 12 s Table I.

MRI protocol for IDEAL-IQ and IVIM-DWI

MRI protocol .  . MRI sequence . T1WI . T2WI/fs . IDEAL-IQ . IVIM-DWI . Position Sagittal/Coronal Sagittal Sagittal Sagittal TR (ms) 617 2900 4.8 5200 TE (ms) 16 1.3 1.5 68 FOV (mm × mm) 260 × 260 310 × 310 320 × 320 320 × 300 Matrix 512 × 288 288 × 224 384 × 512 320 × 300 Slice thickness (mm) 4 3 3 3 Slice gap (mm) 0.5 0.6 0.5 0.5 b-values (s/mm2) / / / 10, 20, 30, 50, 80, 100, 200, 400, 800, 1000 Total scan time 11 min 15 s 4 min 6 s 2 min 34 s 3 min 12 s MRI protocol .  . MRI sequence . T1WI . T2WI/fs . IDEAL-IQ . IVIM-DWI . Position Sagittal/Coronal Sagittal Sagittal Sagittal TR (ms) 617 2900 4.8 5200 TE (ms) 16 1.3 1.5 68 FOV (mm × mm) 260 × 260 310 × 310 320 × 320 320 × 300 Matrix 512 × 288 288 × 224 384 × 512 320 × 300 Slice thickness (mm) 4 3 3 3 Slice gap (mm) 0.5 0.6 0.5 0.5 b-values (s/mm2) / / / 10, 20, 30, 50, 80, 100, 200, 400, 800, 1000 Total scan time 11 min 15 s 4 min 6 s 2 min 34 s 3 min 12 s 

Imaging data of IDEAL-IQ and IVIM-DWI were post-processed using an AW4.5 workstation. In IDEAL-IQ, the pseudo-color image corresponding to the fat content was generated. Then we defined the region of interest (ROI) and calculated the fat fraction (FF) by the following formula: FF = (SIIP–SIOP)/(2SIIP). IVIM-DWI was performed using an MADC kit. The pseudo-color images were generated for matching the corresponding b-values (10–200 s/mm2), and then f, indicating perfusion of microcirculation, was obtained. The bone marrow FF and the microcirculation (f) were measured in each strategy. A center-weight-bearing line (parallel to the B0 line through the center of the femoral head) was set and ROIs were defined within the area ranging from −30° to +30° around the line. IDEAL-IQ and IVIM-DWI values were obtained and measured at the −30° line, the centerline and the +30° line in each area (Fig. 1a). ROIs were allowed to be adjusted no more than 5° if the necrotic or penumbra area was not big enough. This line drawing was also applied in the normal and risk groups (Fig. 1b and c). Each test was performed in triplicate and we recorded the averages as the final results. In order to ensure consistency between the tests, all of the steps were independently completed by two radiologists (X.R.H and Y.G., with 10 and 20 years of experience, respectively).

Fig. 1.

Division of the femoral head in T1WI images and ROI selection. The ROIs were used to divide the IDEAL-IQ and IVIM-DWI images of the femoral head into radial sections. (a) For the normal hips and contralateral asymptomatic hips, the center was confirmed using a concentric circle in the femoral head and a center line parallel to B0 that passed through the center of the femoral head (white circle: normal area selection). (b1) In SIONFH, the femoral head is divided into three parts, i.e. the normal area (β), penumbra area (white arrow, presenting as a low signal band) and necrotic area (α, presenting as a high signal). (b2) ROIs were allowed to be adjusted no more than 5° if the necrotic or penumbra area was not big enough (green circle: necrotic area selection; orange circle: penumbra area selection; white circle: normal area selection).

Division of the femoral head in T1WI images and ROI selection. The ROIs were used to divide the IDEAL-IQ and IVIM-DWI images of the femoral head into radial sections. (a) For the normal hips and contralateral asymptomatic hips, the center was confirmed using a concentric circle in the femoral head and a center line parallel to B0 that passed through the center of the femoral head (white circle: normal area selection). (b1) In SIONFH, the femoral head is divided into three parts, i.e. the normal area (⁠β⁠), penumbra area (white arrow, presenting as a low signal band) and necrotic area (⁠α⁠, presenting as a high signal). (b2) ROIs were allowed to be adjusted no more than 5° if the necrotic or penumbra area was not big enough (green circle: necrotic area selection; orange circle: penumbra area selection; white circle: normal area selection).

Fig. 1.

Division of the femoral head in T1WI images and ROI selection. The ROIs were used to divide the IDEAL-IQ and IVIM-DWI images of the femoral head into radial sections. (a) For the normal hips and contralateral asymptomatic hips, the center was confirmed using a concentric circle in the femoral head and a center line parallel to B0 that passed through the center of the femoral head (white circle: normal area selection). (b1) In SIONFH, the femoral head is divided into three parts, i.e. the normal area (β), penumbra area (white arrow, presenting as a low signal band) and necrotic area (α, presenting as a high signal). (b2) ROIs were allowed to be adjusted no more than 5° if the necrotic or penumbra area was not big enough (green circle: necrotic area selection; orange circle: penumbra area selection; white circle: normal area selection).

Division of the femoral head in T1WI images and ROI selection. The ROIs were used to divide the IDEAL-IQ and IVIM-DWI images of the femoral head into radial sections. (a) For the normal hips and contralateral asymptomatic hips, the center was confirmed using a concentric circle in the femoral head and a center line parallel to B0 that passed through the center of the femoral head (white circle: normal area selection). (b1) In SIONFH, the femoral head is divided into three parts, i.e. the normal area (⁠β⁠), penumbra area (white arrow, presenting as a low signal band) and necrotic area (⁠α⁠, presenting as a high signal). (b2) ROIs were allowed to be adjusted no more than 5° if the necrotic or penumbra area was not big enough (green circle: necrotic area selection; orange circle: penumbra area selection; white circle: normal area selection).

Histologic evaluation and immunohistochemistry assay

Due to the indications of total hip arthroplasty for SIONFH, only patients at ARCO Stage III underwent surgery in our study (performed by Z.Q.C.). The necrotic femoral heads were collected for hematoxylin and eosin (H&E) staining and immunohistochemistry assay. Specifically, bone cubes were punched down from the normal, penumbral and necrotic areas of the isolated femoral head. Then the cubes were fixed, decalcified and embedded, and the created slices were stained using H&E. For immunohistochemistry, the slices were deparaffinized, rehydrated and incubated with anti-VEGF and a secondary antibody (Thermo Fisher Scientific, Waltham, MA, USA) (performed by G.J.H.).

Statistical analysis

Statistical analyses were conducted using SPSS Statistics 22.0 (Chicago, IL, USA), except for the receiver operating characteristic (ROC) comparison, which was conducted using MedCalc (Ostend, Belgium). Both continuous and discrete variables are expressed as mean ± standard deviation (SD). The FF and f were compared between areas (normal, penumbra and necrotic areas) and groups (normal, exposed and risk groups) by analysis of variance (ANOVA). The LSD t-test was used for further multiple comparisons. The diagnostic sensitivity and specificity of the FF and f detected in the necrotic area were evaluated by ROC curve analysis.

RESULTS Demographic characteristics

This study included 31 bilateral SIONFH cases (18 males and 13 females; median age, 43 years; range, 16–58 years) and 18 unilateral SIONFH cases (12 males and 6 females; median age, 42 years; range, 19–60 years). A total of 24 healthy volunteers without ONFH or any other hip joint disease were enrolled (14 males and 10 females; median age, 36; range, 19–47 years).

Imaging of IDEAL-IQ and IVIM-DWI analysis

The pseudo-color images of IDEAL-IQ and IVIM-DWI were colonized through the spatial distributions of FF and f, both of which represent the dynamic changes of biochemical substances in the femoral head. When considering the IDEAL-IQ image, as shown in Fig. 2(a4), the femoral heads of healthy volunteers exhibited morphologic integrity, with a smooth articular surface and uniform green color gradation. In SIONFH ARCO Stages I and II, pseudo-color images containing unexpected yellow or red spots (necrotic area) and blue bands (penumbral area) were observed [Fig. 2(b4–c4)]. In SIONFH ARCO Stage III, these signs in the necrotic area progressively aggravated, presenting as fading or confused colors. Additionally, a large blue band was the main characteristic of the pseudo-color image of the penumbral area at this stage [Fig. 2(d4)]. The location of the necrotic area identified in T1WI and T2WI/fs images [Fig. 2(1–3)] was approximately consistent with the enhanced IDEAL-IQ signal, which was demonstrated by the positive correlation coefficient of 0.72 (P = 0.000) between the FF and ARCO stages (Fig. 3a). In the necrotic area of the femoral head, the FF at ARCO Stages I–III gradually increased (increases of 28.63%, 47.66% and 83.37%, respectively, compared with normal hips; Table II); the statistical significance of these increases was confirmed by the LSD t-test (Table III). In IVIM-DWI, the observation of diffuse and mixed colors (green–yellow–red) in the femoral head indicated poor perfusion and ischemic injury. The area of patchy-like mixed colors was enlarged with the progression of the ARCO stage [Fig. 2(a5–d5)]. Although the level of microcirculation perfusion was negatively correlated with the fat deposition, as demonstrated by IDEAL-IQ (the correlation coefficient was −0.37, P = 0.048; Fig. 3b), The locations of ischemic lesions [Fig. 2(a5–d5)] did not completely coincide with those of osteonecrosis shown in T1WI and T2WI/fs [Fig. 2(1–3)]. In the IVIM-DWI pseudo-color images, f decreased with the progression of the disease from Stages I to III [decreases of 17.54%, 21.44% and 45.6%, respectively (Table II)] and their correlation coefficient was −0.17 (P = 0.390) (Fig. 3a). In the LSD t-test, the mean f of necrotic areas varied at each stage, but no significant difference was found between Stage I and Stage II (Table III).

Fig. 2.

The progression of ARCO stage and signal changes in sagittal/coronal T1WI, sagittal T2WI/fs, sagittal IDEAL-IQ and sagittal IVIM-DWI sequences. (a1–a5) A 52-year-old female participant without SIONFH exhibited an even color gradation of the femoral head and clear boundaries at imaging. (b1–b5) A 53-year-old male ARCO Stage I patient showed a small blue band and a green color spot in the IDEAL-IQ and IVIM-DWI images, respectively. (c1–c5) A 61-year-old female ARCO Stage II patient exhibited mixed-color bands in both techniques. (d1–d5) A 41-year-old male ARCO Stage III patient showed a blue band indicating the penumbra area in IDEAL-IQ and diffuse and mixed colors (green–yellow–red) in IVIM-DWI.

The progression of ARCO stage and signal changes in sagittal/coronal T1WI, sagittal T2WI/fs, sagittal IDEAL-IQ and sagittal IVIM-DWI sequences. (a1–a5) A 52-year-old female participant without SIONFH exhibited an even color gradation of the femoral head and clear boundaries at imaging. (b1–b5) A 53-year-old male ARCO Stage I patient showed a small blue band and a green color spot in the IDEAL-IQ and IVIM-DWI images, respectively. (c1–c5) A 61-year-old female ARCO Stage II patient exhibited mixed-color bands in both techniques. (d1–d5) A 41-year-old male ARCO Stage III patient showed a blue band indicating the penumbra area in IDEAL-IQ and diffuse and mixed colors (green–yellow–red) in IVIM-DWI.

Fig. 2.

The progression of ARCO stage and signal changes in sagittal/coronal T1WI, sagittal T2WI/fs, sagittal IDEAL-IQ and sagittal IVIM-DWI sequences. (a1–a5) A 52-year-old female participant without SIONFH exhibited an even color gradation of the femoral head and clear boundaries at imaging. (b1–b5) A 53-year-old male ARCO Stage I patient showed a small blue band and a green color spot in the IDEAL-IQ and IVIM-DWI images, respectively. (c1–c5) A 61-year-old female ARCO Stage II patient exhibited mixed-color bands in both techniques. (d1–d5) A 41-year-old male ARCO Stage III patient showed a blue band indicating the penumbra area in IDEAL-IQ and diffuse and mixed colors (green–yellow–red) in IVIM-DWI.

The progression of ARCO stage and signal changes in sagittal/coronal T1WI, sagittal T2WI/fs, sagittal IDEAL-IQ and sagittal IVIM-DWI sequences. (a1–a5) A 52-year-old female participant without SIONFH exhibited an even color gradation of the femoral head and clear boundaries at imaging. (b1–b5) A 53-year-old male ARCO Stage I patient showed a small blue band and a green color spot in the IDEAL-IQ and IVIM-DWI images, respectively. (c1–c5) A 61-year-old female ARCO Stage II patient exhibited mixed-color bands in both techniques. (d1–d5) A 41-year-old male ARCO Stage III patient showed a blue band indicating the penumbra area in IDEAL-IQ and diffuse and mixed colors (green–yellow–red) in IVIM-DWI.

Fig. 3.

Relationships among IDEAL-IQ and IVIM-DWI and ARCO stage. (a) A positive correlation was observed between IDEAL-IQ and ARCO stage (r = 0.72, P = 0.000). IVIM-DWI and ARCO stage were negatively correlated (r = −0.17, P = 0.390). (b) IDEAL-IQ was negatively correlated with the IVIM-DWI (r = −0.37, P = 0.048).

Relationships among IDEAL-IQ and IVIM-DWI and ARCO stage. (a) A positive correlation was observed between IDEAL-IQ and ARCO stage (r = 0.72, P = 0.000). IVIM-DWI and ARCO stage were negatively correlated (r = −0.17, P = 0.390). (b) IDEAL-IQ was negatively correlated with the IVIM-DWI (r = −0.37, P = 0.048).

Fig. 3.

Relationships among IDEAL-IQ and IVIM-DWI and ARCO stage. (a) A positive correlation was observed between IDEAL-IQ and ARCO stage (r = 0.72, P = 0.000). IVIM-DWI and ARCO stage were negatively correlated (r = −0.17, P = 0.390). (b) IDEAL-IQ was negatively correlated with the IVIM-DWI (r = −0.37, P = 0.048).

Relationships among IDEAL-IQ and IVIM-DWI and ARCO stage. (a) A positive correlation was observed between IDEAL-IQ and ARCO stage (r = 0.72, P = 0.000). IVIM-DWI and ARCO stage were negatively correlated (r = −0.17, P = 0.390). (b) IDEAL-IQ was negatively correlated with the IVIM-DWI (r = −0.37, P = 0.048).

Table II.

IDEAL-IQ and IVIM-DWI in each stage of the femoral head

. ARCO stage . F value . P-value . Normal (n = 48) . I (n = 12) . II (n = 28) . III (n = 40) . FF (%) 57.80 ± 6.85 74.35 ± 4.21 85.35 ± 6.42 105.99 ± 0.05 59.02 0.000 F 0.57 ± 0.06 0.47 ± 0.03 0.37 ± 0.02 0.31 ± 0.07 37.07 0.000  . ARCO stage . F value . P-value . Normal (n = 48) . I (n = 12) . II (n = 28) . III (n = 40) . FF (%) 57.80 ± 6.85 74.35 ± 4.21 85.35 ± 6.42 105.99 ± 0.05 59.02 0.000 F 0.57 ± 0.06 0.47 ± 0.03 0.37 ± 0.02 0.31 ± 0.07 37.07 0.000 Table II.

IDEAL-IQ and IVIM-DWI in each stage of the femoral head

. ARCO stage . F value . P-value . Normal (n = 48) . I (n = 12) . II (n = 28) . III (n = 40) . FF (%) 57.80 ± 6.85 74.35 ± 4.21 85.35 ± 6.42 105.99 ± 0.05 59.02 0.000 F 0.57 ± 0.06 0.47 ± 0.03 0.37 ± 0.02 0.31 ± 0.07 37.07 0.000  . ARCO stage . F value . P-value . Normal (n = 48) . I (n = 12) . II (n = 28) . III (n = 40) . FF (%) 57.80 ± 6.85 74.35 ± 4.21 85.35 ± 6.42 105.99 ± 0.05 59.02 0.000 F 0.57 ± 0.06 0.47 ± 0.03 0.37 ± 0.02 0.31 ± 0.07 37.07 0.000 
Table III.

LSD t-test for IDEAL-IQ and IVIM-DWI of multiple comparisons between ARCO stages

. ARCO stage . X ± s . P-value . 95% CI . FF (%) Normal I –16.55 ± 5.57 0.00 0.02, 0.18 II –27.55 ± 3.84 0.00 0.04, 0.15 III –48.20 ± 3.74 0.00 0.20, 0.31 I Normal 16.55 ± 5.57 0.00 –0.18, –0.02 II –11.00 ± 5.21 0.04 –0.08, 0.07 III –31.65 ± 5.13 0.00 0.08, 0.23 II Normal 27.55 ± 3.84 0.00 –0.15, –0.04 I 11.00 ± 5.21 0.04 –0.07, 0.08 III –20.64 ± 3.18 0.00 0.11, 0.20 III Normal 48.20 ± 3.74 0.00 –0.31, –0.20 I 31.65 ± 5.13 0.00 –0.23, –0.08 II 20.64 ± 3.18 0.00 –0.20, –0.11 F Normal I 0.10 ± 0.04 0.02 –27.90, –5.21 II 0.10 ± 0.03 0.00 –35.37, 19.73 III 0.25 ± 0.03 0.00 –55.81, –40.59 I Normal –0.10 ± 0.04 0.02 5.21, 27.9 II –0.00 ± 0.04 0.96 –21.61, –0.39 III 0.16 ± 0.04 0.00 –42.10, –21.19 II Normal –0.10 ± 0.03 0.00 19.73, 35.37 I 0.00 ± 0.04 0.96 0.39, 21.61 III 0.16 ± 0.02 0.00 40.59, –14.18 III Normal –0.25 ± 0.03 0.00 40.59, 55.81 I –0.16 ± 0.04 0.00 21.19, 42.1 II –0.16 ± 0.02 0.00 14.18, 27.11  . ARCO stage . X ± s . P-value . 95% CI . FF (%) Normal I –16.55 ± 5.57 0.00 0.02, 0.18 II –27.55 ± 3.84 0.00 0.04, 0.15 III –48.20 ± 3.74 0.00 0.20, 0.31 I Normal 16.55 ± 5.57 0.00 –0.18, –0.02 II –11.00 ± 5.21 0.04 –0.08, 0.07 III –31.65 ± 5.13 0.00 0.08, 0.23 II Normal 27.55 ± 3.84 0.00 –0.15, –0.04 I 11.00 ± 5.21 0.04 –0.07, 0.08 III –20.64 ± 3.18 0.00 0.11, 0.20 III Normal 48.20 ± 3.74 0.00 –0.31, –0.20 I 31.65 ± 5.13 0.00 –0.23, –0.08 II 20.64 ± 3.18 0.00 –0.20, –0.11 F Normal I 0.10 ± 0.04 0.02 –27.90, –5.21 II 0.10 ± 0.03 0.00 –35.37, 19.73 III 0.25 ± 0.03 0.00 –55.81, –40.59 I Normal –0.10 ± 0.04 0.02 5.21, 27.9 II –0.00 ± 0.04 0.96 –21.61, –0.39 III 0.16 ± 0.04 0.00 –42.10, –21.19 II Normal –0.10 ± 0.03 0.00 19.73, 35.37 I 0.00 ± 0.04 0.96 0.39, 21.61 III 0.16 ± 0.02 0.00 40.59, –14.18 III Normal –0.25 ± 0.03 0.00 40.59, 55.81 I –0.16 ± 0.04 0.00 21.19, 42.1 II –0.16 ± 0.02 0.00 14.18, 27.11 Table III.

LSD t-test for IDEAL-IQ and IVIM-DWI of multiple comparisons between ARCO stages

. ARCO stage . X ± s . P-value . 95% CI . FF (%) Normal I –16.55 ± 5.57 0.00 0.02, 0.18 II –27.55 ± 3.84 0.00 0.04, 0.15 III –48.20 ± 3.74 0.00 0.20, 0.31 I Normal 16.55 ± 5.57 0.00 –0.18, –0.02 II –11.00 ± 5.21 0.04 –0.08, 0.07 III –31.65 ± 5.13 0.00 0.08, 0.23 II Normal 27.55 ± 3.84 0.00 –0.15, –0.04 I 11.00 ± 5.21 0.04 –0.07, 0.08 III –20.64 ± 3.18 0.00 0.11, 0.20 III Normal 48.20 ± 3.74 0.00 –0.31, –0.20 I 31.65 ± 5.13 0.00 –0.23, –0.08 II 20.64 ± 3.18 0.00 –0.20, –0.11 F Normal I 0.10 ± 0.04 0.02 –27.90, –5.21 II 0.10 ± 0.03 0.00 –35.37, 19.73 III 0.25 ± 0.03 0.00 –55.81, –40.59 I Normal –0.10 ± 0.04 0.02 5.21, 27.9 II –0.00 ± 0.04 0.96 –21.61, –0.39 III 0.16 ± 0.04 0.00 –42.10, –21.19 II Normal –0.10 ± 0.03 0.00 19.73, 35.37 I 0.00 ± 0.04 0.96 0.39, 21.61 III 0.16 ± 0.02 0.00 40.59, –14.18 III Normal –0.25 ± 0.03 0.00 40.59, 55.81 I –0.16 ± 0.04 0.00 21.19, 42.1 II –0.16 ± 0.02 0.00 14.18, 27.11  . ARCO stage . X ± s . P-value . 95% CI . FF (%) Normal I –16.55 ± 5.57 0.00 0.02, 0.18 II –27.55 ± 3.84 0.00 0.04, 0.15 III –48.20 ± 3.74 0.00 0.20, 0.31 I Normal 16.55 ± 5.57 0.00 –0.18, –0.02 II –11.00 ± 5.21 0.04 –0.08, 0.07 III –31.65 ± 5.13 0.00 0.08, 0.23 II Normal 27.55 ± 3.84 0.00 –0.15, –0.04 I 11.00 ± 5.21 0.04 –0.07, 0.08 III –20.64 ± 3.18 0.00 0.11, 0.20 III Normal 48.20 ± 3.74 0.00 –0.31, –0.20 I 31.65 ± 5.13 0.00 –0.23, –0.08 II 20.64 ± 3.18 0.00 –0.20, –0.11 F Normal I 0.10 ± 0.04 0.02 –27.90, –5.21 II 0.10 ± 0.03 0.00 –35.37, 19.73 III 0.25 ± 0.03 0.00 –55.81, –40.59 I Normal –0.10 ± 0.04 0.02 5.21, 27.9 II –0.00 ± 0.04 0.96 –21.61, –0.39 III 0.16 ± 0.04 0.00 –42.10, –21.19 II Normal –0.10 ± 0.03 0.00 19.73, 35.37 I 0.00 ± 0.04 0.96 0.39, 21.61 III 0.16 ± 0.02 0.00 40.59, –14.18 III Normal –0.25 ± 0.03 0.00 40.59, 55.81 I –0.16 ± 0.04 0.00 21.19, 42.1 II –0.16 ± 0.02 0.00 14.18, 27.11  Comparison of the IDEAL-IQ and IVIM-DWI values among different areas

To distinguish the appearances of different areas of the femoral head, the FF and f were further investigated at the normal, penumbral and necrotic areas in the femoral head of SIONFH patients. The average FF was enhanced by 102.42% at the necrotic area, whereas it was reduced to 38.56% at the penumbral area. The highest obtained value for f at the normal area was 0.4%, and lower values were obtained at the other areas (Tables IV and V).

Table IV.

IDEAL-IQ and IVIM-DWI in each area of the femoral head

. Area of femoral head . F value . P-value . NA (n = 80) . PA (n = 80) . OA (n = 80) . FF (%) 75.24 ± 14.55 38.56 ± 13.04 102.42 ± 36.67 51.76 0.000 F 0.40 ± 0.08 0.34 ± 0.08 0.30 ± 0.07 12.36 0.000  . Area of femoral head . F value . P-value . NA (n = 80) . PA (n = 80) . OA (n = 80) . FF (%) 75.24 ± 14.55 38.56 ± 13.04 102.42 ± 36.67 51.76 0.000 F 0.40 ± 0.08 0.34 ± 0.08 0.30 ± 0.07 12.36 0.000 

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