Assessment Of Bone Resorption In ONFH With MR Imaging

doi:10.21203/rs.3.rs-1333313/v1

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Assessment Of Bone Resorption In ONFH With MR Imaging

https://doi.org/10.21203/rs.3.rs-1333313/v1

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The aim of this study was to analyze the image characteristics of bone resorption lesion in Osteonecrosis of the femoral head (ONFH) on MR. 359 cases with ONFH staged as ARCO 2/3 were retrospectively analyzed, and 46 cases were included finally. General information, CT/MR signs of bone resorption, and bone marrow edema were evaluated and compared between two types of T2WI signal group. The sensitivity of MR in detecting bone resorption was 70.6%, and the specificity was 100%. The number, ADC value of bone resorption, BME, and the incidence of bone resorption connected to the subchondral fracture fissure were significantly greater in group 2 than 1. The intensity of bone resorption was significantly lower in group 2 than 1. MR performance good in detection of bone resorption. T2 Type I signal bone resorption lesions should be carefully detected to avoid missed diagnosis. T2 Type II signal bone resorption lesions may indicate destructive repair type.

ONFH

Bone resorption

ARCO stage 2/3

Osteonecrosis of the femoral head (ONFH) is one of refractory diseases in orthopedics, mainly occurs in young and middle-aged people.Femoral head collapse is an important sign of progression. Previous study has found that bone resorption plays an important role in the deterioration of the collapse process in femoral head necrosis^,. Bone resorption in ONFH is the low-density lesion without bone trabeculae, considered to be caused by osteoclastic resorption of necrotic trabeculae, mainly composed of vascularize granulation and fibrous tissue^,. It is a manifestation of the repair process in ONFH, which first appears in ARCO stage 2. Since bone resorption is shown best on CT due to its low density, previous studies have focused on the CT imaging. There is no relevant research on the manifestation of bone resorption on MR currently. Because MR can demonstrate the bone resorption lesion in more detail with multi-parameter and multi-sequence imaging, therefore, this study aims to conduct a retrospective analysis on cases underwent both MR and CT examination of ARCO stages 2 and 3 in ONFH, analyze the detection rate and image characteristics of bone resorption on MR by referring to CT examination, and to explore the possible pathological basis of different MR signals in bone resorption lesion.

1. The signals of bone resorption on T1WI were as follows: iso-signal (14), slightly higher signal (17), and heterogeneous signal with iso- and slightly higher signal (15). Since the T1 signals were similar and have little discriminating value, so they were not compared between the two groups.

2.The performance of MR in detection of bone resorption lesion:

60 bone resorption lesions were found on MR, and 85 were identified on CT, sensitivity of MR was 70.6%, and specificity was 100%. The detail is seen in Table 1.

3.There was a strong correlation in MAC of bone resorption lesion between CT and MRI: r=0.931, P<0.001.

4.There were no significant differences in age, sex and ARCO staging between the two groups (P>0.05). The number, ADC value of bone resorption, BME, and the incidence of bone resorption connected to the subchondral fracture were significantly greater in group 2 than 1. Intensity of bone resorption lesion was significantly lower in group 2 than 1. (Table 2)

5.Interrater consistency for evaluation of MAC, density, and ADC value of the bone resorption lesion, and BME were seen in Table 3.

This is the first study focus on the MR imaging manifestation of bone resorption lesion. It’s found that MR has good sensitivity and strong specificity in the detection of bone resorption lesion. Due to multi-sequence and multi-parameter imaging, it is possible to have a more comprehensive observation and in-depth understanding of the bone resorption lesion on MR.

The sensitivity of MR in detecting bone resorption lesion is good, but nearly 30% have not yet been detected. The reasons are mainly in two aspects. First is due to its signal characteristics, the T2WI type I signal is not easy to detected due to the equal or slightly higher signal, especially with unclear boundaries (Fig. 3), 8 cases of type I signal with unclear boundaries were submerged in BME and not detected in this study. Second is the small size of bone resorption, in this study, 17 cases of type II signal were not found as their diameter were less than or equal to 4mm. Because the slice thickness of coronal-PDWI sequence was 4mm, and slice interval was 0.8cm, which is relatively thick for small bone resorption lesion and could be missed. According to the previous research, the smaller bone resorption lesion(≤ 4mm) is of little clinical significance. Therefore, attention should be paid to the detection of T2 type I signal bone resorption lesions, so as to minimize missed diagnosis, and CT examination should be performed when necessary.

The reason for high specificity of MR in detecting bone resorption lesion: heterogeneous or homogeneous high T2 signal with clear boundary, mostly located in the necrotic area is the main and typical manifestation of bone resorption lesion, which is not easy to be confused with other signs.

The T2 signals of bone resorption lesion can be heterogeneous, which indicate a complex internal composition. Previous studies have found that there are mainly vascular granulation tissue, fibrous tissue, and even ossification in bone resorption lesion⁻. In this study, two different types of T2 signals were found. The T2WI type II signal is high intensity (Fig. 4), and its ADC value is high. It is speculated that its components are rich in hydrogen protons. Besides, the density is relatively low. Therefore, it is most likely to be vascularize fresh granulation tissue, which is in the early stage of bone resorption. Since it is more often associated with subchondral fractures and large scale BME, indicated the destructive repair type, combined with severe inflammation, and femoral head collapse is prone to progress quickly.

The T2WI Type I signal is equal to slightly higher intensity (Fig. 2), the ADC value is relatively low, and the density is relatively high, so it is most likely to be fibrous granulation tissue or even with a small amount of calcium deposition, probably in the late stage of bone resorption. As there are fewer subchondral fractures and a relatively small range of bone marrow edema, indicated the limited repair type¹⁰.

Limitations of this study: First, there were no pathological specimens in all cases, and it is difficult to make an exact explanation of the signal characteristics of the bone resorption lesion; second, this was a single center with a single MR machine study.

General information

Patients with ONFH staged as ARCO 2/3 from January 2015 to August 2021 were retrospectively analyzed. The diagnosis standard was Chinese Experts' Consensus on the Diagnosis and Treatment of Osteonecrosis of the Femoral Head in Adults (2016), and the cases were staged according to ARCO 2019. The criterion of ARCO stage 2 is osteosclerosis, focal osteoporosis, or cystic changes are seen in the femoral head on plain radiographs or CT scan, and there is no evidence of subchondral fracture, fracture in the necrotic portion, or flattening of the femoral head; and criterion of ARCO stage 3 is subchondral fracture, fracture in the necrotic portion, and/or flattening of the femoral head is seen on plain radiography or CT scan, without manifestation of hip osteoarthritis, stage 3 is subdivided into early and late sub-stages according to the amount of femoral head depression (≤ 2 mm versus > 2 mm)¹². As ARCO stage 1 is clinically rare and does not contain bone resorption lesion. ARCO stage 4 is associated with osteoarthritis and may contain subchondral bone cyst, which may be confused with the bone resorption, so ARCO stages 1 and 4 were not included. The ARCO staging was determined by two orthopedics based on hip CT image with negotiation.

Inclusion criteria: ARCO stage 2/3, with bone resorption lesion on hip CT image, the interval of MR and CT examinations within 1 month. Because patients underwent hip MR examination are relatively less than CT in our hospital, screening is based on MR.

Exclusion criteria: Without CT examination, the interval between CT and MR examinations exceeded 1 month, no bone resorption lesion on CT, ARCO stage 1/4, history of hip surgery or trauma, and connective tissue diseases.

There were 359 ONFH cases underwent MR examination, after excluding all kinds of unqualified patients, 41 cases were finally collected, of which 5 cases were bilateral ONFH, so there were 46 cases. Among them, 16 cases were ARCO stage 2, 14 cases were ARCO stage 3A, and 16 cases were ARCO stage 3B. M/F = 29/12. See Fig. 1 for details.

This study was approved by the Medical Ethics Committee and patient consent was waived.

Mr Protocol

MRI was performed at 3 T (Skyra, Siemens AG, Germany) using a phased array body coil. Scanning protocols included: axial T1W Turbo Spin Echo (TSE) sequence, axial T2W fat-saturated (FS) TSE sequence, and coronal proton density weighted imaging (PDWI)-FS-Dixon fat/water image. Among the enrolled patients, 8 cases underwent additional axial DWI sequence examination, b-values: 0, 500, and 1000 s/mm2. (The sequence parameters are summarized in Table 1).

Ct Protocol

CT was performed with SOMATOM Definition Flash, Siemens. The scan parameters were: tube voltage:140 kVp; automatic tube current modulation (90–130 mA); DFOV: 35.6×35.6 cm; slice thickness:0.75 mm. Both hip joints were scanned simultaneously. The scanning range was from the top of the acetabulum to the femoral lesser trochanter. Coronal views were reconstructed with bone windows using the B60s kernel, sharp,3 mm for all hip joints. Besides, supplemental coronal views reconstructions were performed in the PACS system (Tianjian RIS 6.0) with the slice thickness of 1mm.

All subjects were placed in supine position with feet in the neutral position.

Ct Image Evaluation

The size and density of bone resorption were blindly measured by three radiologists (SS, 9 years working experience; LS, 7 years working experience; HB T, 25 years working experience) and take the average as result. The number and shape of bone resorption lesions, and whether they were connected to subchondral fractures were determined by two radiologists (SS, 9 years working experience; HB T, 25 years working experience) with negotiation. All the CT signs were measured and evaluated on the coronal reconstructed image (slice thickness 3mm), with referring to the original axial image and supplemental coronal reconstruction image.

1. The shape of bone resorption: evaluation was performed at the largest slice of the bone resorption lesion on the coronal CT, if the shape was approximately round or oval, regarded as regular and recorded as 1; other shapes were regarded as irregular, recorded as 2.

2. The maximum area in coronal position (MAC) and density of bone resorption lesion were measured by the methods used in the previous research³.

3. Whether the bone resorption is connected to the subchondral fracture: if the low-density bone resorption lesion was directly connected to the subchondral fracture, recorded as 1, otherwise was recorded as 0.

Mr Image Evaluation

Before the formal evaluation, 10 enrolled patients were randomly selected, and the MR signs of bone resorption were observed and studied by three radiologists by referring to the CT images.

1. The number and size of bone resorption:

Two radiologists blindly evaluated the number of bone resorption in the coronal PDWI-FS-Dixon water image, and they reached consensus through consultation if inconsistent. The measurement method of MAC of bone resorption is the same as on CT³.

2. MR T1WI and T2WI signal characteristics of bone resorption lesion:

The T1 and T2 signal characteristics of the maximum bone resorption in each enrolled patient were evaluated by referring to the CT image.

On the axial T2W FS TSE sequence, the signal of bone resorption was divided into two types, type I, with equal or slightly higher signal (equal signal: similar to bone marrow signal intensity, slightly higher-equivalent to bone marrow edema signal intensity); type II, with high signal (slightly lower than or equal to the signal intensity of joint effusion).

Besides, the heterogeneous of T2 signal was evaluated, heterogeneous was recorded as 1, and homogeneous was recorded as 0.

On the axial T1W TSE sequence, the signals of bone resorption were evaluated and recorded (iso-signal: equivalent to muscle signal; slightly higher signal - higher than muscle signal but still lower than bone marrow signal; heterogeneous signal with iso and slightly higher signal).

3. Bone marrow edema (BME).

BME was assessed on the axial T1W TSE and axial T2W FS TSE sequence, the extent of BME was scored from 1 to 3 according to its scope.

4.ADC value

For 8 cases underwent DWI examination, the ADC values were measured by referring to the axial T2W FS TSE or CT images. On the Siemens workstation(SYNGO VFA-SOF), select the largest layer of the axial bone resorption lesion and draw a largest circular or elliptical range of interest to measure.

In image evaluation, the number, shape, and MR signal characteristics of bone resorption, BME, and whether it is connected to subchondral fracture was determined by two radiologists in consultation (SS, HB T). The MAC, density, and ADC value of bone resorption were blindly measured by three radiologists (SS, LS, HB T).

Grouping Standard

The cases were divided into two groups according to the T2 signal type of bone resorption on FS T2WI. Group 1- T2WI signal type I, Group 2- T2WI signal type II.

Statistical Analysis

Continuous variables were summarized as medians with interquartile ranges. Categorical variables were presented as counts and percentages. Age, BME, MAC, intensity and ADC value of bone resorption between the two groups were compared by Mann-Whitney test. (SPSS 22.0). The Chi-square test was used to evaluate the differences of gender, shape and heterogeneous T2 signal of bone resorption, and whether the bone resorption is connected to the subchondral fracture between the two groups. The correlation between the MAC of bone resorption lesion on MR and CT was analyzed by Pearson’s correlation. The consistency of the data from the 3 radiologists was analyzed by intraclass correlation coefficient (ICC). P < 0.05 is statistically significant.

Conflicts of interest

Author Xuedong Yang has received research grants from CRIBJQY202109 and CI2021A03302;

Author Tong Yu has received research grants from CI2021A03320;

All the other authors declare that they have no conflict of interest.

Funding

Supported by

1.Beijing United Imaging Research Institute of Intelligent Imaging Foundation (No. CRIBJQY202109)

2. Scientific and technological innovation project of China Academy of Chinese Medical Sciences (No. CI2021A03302)

3. Scientific and technological innovation project of China Academy of Chinese Medical Sciences (No. CI2021A03320)

Acknowledgements

None

Author contributions

S.S.,conception, drafted the work, interpretation of data; L.S., acquisition, conception,analysis,

interpretation of data; X.D.Y., conception, revised, approved the submitted version, have agreed both to be personally accountable for the author's own contributions and to ensure that questions related to the accuracy or integrity of any part of the work; H.B.T., acquisition, analysis, interpretation of data; P.L., analysis, interpretation of data; L.M. X., acquisition, conception, revised; T.Y., acquisition, interpretation of data.

Additional Information Competing Interests:

The authors declare no competing interests.

Statement

1. This study was approved by the Medical Ethics Committee of Guang'anmen Hospital, China Academy of Chinese Medical Sciences, patient consent was waived (2016-080-KY-02)

2.All methods were carried out in accordance with relevant guidelines and regulations

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Shi, S et al Prediction of the progression of femoral head collapse in ARCO stage 2-3A osteonecrosis based on the initial bone resorption lesion Br J Radiol 94(1117),20200981;101259/bjr20200981(2021)
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Table 1. MR scanning parameters

	Axial-T₁WI	Axial-FS-T₂WI	Coronal-PDWI	DWI
TR (ms)	731	3600	2500	6300
TE (ms)	10	77	35	99
FOV (mm)	380×380	380×237	380×261	350×281
Slice thickness(mm)	4	4	4	5
Interslice gap(mm)	1.2	0.8	0.8	1.0
Bandwidth (kHZ)	250	246	257	766
Matrix size	512×384	384×180	512×299	154×192
Voxel size	0.7×0.7×4.0mm	1.0×1.0×4.0mm	0.7×0.7×4.0mm	1.8×1.8×5.0mm
Total scan time	1min 4sec	2min 4sec	3min 9sec	3min 28sec

Table 2. General information and CT/MR signs in two groups

		T2WI signal type I（n=15）	T2WI signal type II（n=31）	Test statistic	P value
General information	Age	37.0(31.0-50.0)	46.0(34.0-55.0)	-1.502	0.133
	Sex(F/M)	4/11	10/21	0.149	0.699
	ARCO staging	ARCO2-6(40%) ARCO3A-5(33.3%) ARCO3B-4(26.7%)	ARCO2-10(32.3%) ARCO3A-9(29.0%) ARCO3B-12(38.7%)	0.657	0.720
MR Signs	Number of bone resorption lesion	10	50	-3.472	0.001**
	MAC of bone resorption lesion	46(0-133)	72(27-143)	-1.372	0.170
	Heterogeneous T2 signal	0-7(46.7%) 1-8(53.3%)	0-21(67.7%) 1-10(32.3%)	1.855	0.170
	ADC value (10^-3mm²/s)	1.961 (1.941-N)	2.469(2.163-2.745)	-2.000	0.046*
	BME	0-2(13.3%) 1-6(40.0%) 2-5(33.3%) 3-2(13.3%)	0-2(6.5%) 1-5(16.1%) 2-12(38.7%) 3-12(38.7%)	-2.177	0.029*
CT signs	Number of bone resorption lesion	18	67	-2.373	0.018*
	MAC of bone resorption lesion	57(34-125)	86(49-147)	-0.926	0.355
	Intensity of bone resorption lesion	119(64-172)	62(44-75)	-2.789	0.005**
	Shape of bone resorption lesion	1-4(26.7%) 2-11(73.3%)	1-13(41.9%) 2-18(58.1%)	1.012	0.315
	Bone resorption connected to the subchondral fracture	0-11(73.3%) 1-4(26.7%)	0-11(35.5%) 1-20(64.3%)	5.804	0.016*

*Significant difference (P < 0.05).

**Highly significant difference (P < 0.01).

Table 3. Interrater consistency for evaluation of bone resorption

	Intraclass correlation coefficient	95% CI	P-value
MAC of bone resorption on MR	0.983	0.972-0.990	<0.001
ADC value	0.893	0.692-0.975	<0.001
MAC of bone resorption on CT	0.897	0.840-0.938	<0.001
Intensity of bone resorption	0.844	0.761-0.904	<0.001

No competing interests reported.

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Assessment Of Bone Resorption In ONFH With MR Imaging

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Abstract

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Introduction

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Discussion

Materials And Methods

General information

Mr Protocol

Ct Protocol

Ct Image Evaluation

Mr Image Evaluation

Grouping Standard

Statistical Analysis

Declarations

References

Tables

Additional Declarations

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