股骨头前外侧骨质状态在股骨头坏死塌陷进展中的作用

doi:10.3969/j.issn.2095-4344.1148

中国组织工程研究 ›› 2019, Vol. 23 ›› Issue (16): 2516-2522.doi: 10.3969/j.issn.2095-4344.1148

• 骨与关节图像与影像 bone and joint imaging • 上一篇下一篇

股骨头前外侧骨质状态在股骨头坏死塌陷进展中的作用

魏秋实^1，2，方斌²，陈镇秋²，何敏聪³，陈哓俊³，杨帆³，张庆文^1，2，何伟^1，2

广州中医药大学第一附属医院，¹三骨科保髋病区，²三骨科，广东省广州市 510407；³广州中医药大学，广东省广州市 510405

出版日期:2019-06-08 发布日期:2019-06-08
通讯作者: 何伟，主任医师，教授，博士生导师，广州中医药大学第一附属医院，三骨科保髋病区，三骨科，广东省广州市 510407
作者简介:魏秋实，男，1982年生，辽宁省沈阳市人，蒙古族，2012年广州中医药大学毕业，博士，博士后，主要从事股骨头坏死和骨质疏松症发病机制方面的研究。
基金资助:
the National Natural Science Foundation of China, No. 81573996 (to CZQ) and 81473697 (to HW)| the Science and Technology Plan Program of Guangdong Province, No. 2016A020226028

Role of bone status in anterolateral portion of femoral head in the progression of osteonecrosis of the femoral head

Wei Qiushi^{1, 2}, Fang Bin², Chen Zhenqiu², He Mincong³, Chen Xiaojun³, Yang Fan³, Zhang Qingwen^{1, 2}, He Wei^{1, 2}

¹Hip Preserving Ward of Third Department of Orthopedics, ²Third Department of Orthopedics, the First Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou 510407, Guangdong Province, China; ³Guangzhou University of Chinese Medicine, Guangzhou 510405, Guangdong Province, China

Online:2019-06-08 Published:2019-06-08
Contact: He Wei, Chief physician, Professor, Doctoral supervisor, Hip Preserving Ward of Third Department of Orthopedics, Third Department of Orthopedics, the First Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou 510407, Guangdong Province, China
About author:Wei Qiushi, MD, Hip Preserving Ward of Third Department of Orthopedics, Third Department of Orthopedics, the First Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou 510407, Guangdong Province, China
Supported by:
国家自然科学基金(81573996)，项目负责人：陈振秋|国家自然科学基金(81473697)，项目负责人：何伟|广东省科技计划项目(2016A020226028)

摘要/Abstract

摘要：

文章快速阅读：

文题释义：

股骨头坏死：是由于不同原因引起股骨头内活性成分(骨细胞、骨髓造血细胞和脂肪细胞)死亡以及随后的修复，导致骨的结构发生改变，出现股骨头塌陷、关节软骨破坏等一系列病理过程，与多种疾病、激素应用、药物因素和髋关节创伤有关。

股骨头坏死塌陷：是股骨头坏死最关键的病理改变，塌陷的发生以头内骨小梁成片断裂为前提，X片通常不能诊断，CT、MRI有帮助。塌陷发生后，骨小梁成片断裂一定存在，对股骨头及髋关节带来的最主要、最直接影响是各种形式的不稳定。

摘要

背景：机械应力在股骨头坏死塌陷进展中起重要作用。因此，负重区骨结构的状态可能是塌陷的危险因素。

目的：研究股骨头坏死前外侧部分负重区的骨保留与塌陷进展之间的关系。

方法：选取未经系统治疗的87例102髋经MRI诊断为ARCOⅡ期的股骨头坏死患者。通过双髋正位和蛙式侧位X射线片观察股骨头塌陷与负重区骨量保留情况。按照坏死病变部位与股骨头前外侧部的关系，将坏死分为3种类型：1型：坏死区位于后内侧和中心部位；2型；坏死区占据前外侧一部分；3型：坏死区涉及整个前外侧部。对不同类型的塌陷发生率和塌陷时间进行评估。

结果与结论：①所有患者经历3-58个月的随访；②在所有塌陷的60髋中，46髋(76.7%)由双髋正位X射线片证实塌陷，57髋(95.0%)由蛙式侧位X射片证实有塌陷，有显著差异(P < 0.01)；③102髋ARCOⅡ期股骨头坏死，3型塌陷率明显高于2型(P < 0.001)，且发生塌陷的时间明显较短。6髋1型股骨头坏死在随访期均未发生塌陷；④结果提示，股骨头坏死前外侧部的骨保留与潜在的塌陷进展有关。

中国组织工程研究杂志出版内容重点：人工关节；骨植入物；脊柱；骨折；内固定；数字化骨科；组织工程
orcid: 0000-0002-1274-9997(Wei Qiushi)

关键词: 股骨头坏死, 骨结构, 负重区, 塌陷, 蛙式侧位片, 影像学, 骨保留, 国家自然科学基金

Abstract:

BACKGROUND: Mechanical stress plays an important role in the progressive collapse in osteonecrosis of the femoral head. Therefore, the bone structure of weight-bearing area may be the risk factor for collapse.

OBJECTIVE: To investigate the relationship between the bone preservation of weight-bearing area and collapse progression in necrotic femoral head.

METHODS: Eighty-seven patients (102 hips) with ARCO stage II osteonecrosis of the femoral head, diagnosed by MRI, were enrolled. All patients underwent a natural progression. Collapse and bone involvement of the weight-bearing area were viewed by anteroposterior and frog-leg lateral radiographs. According to the location of the necrotic lesion on the anterolateral portion of the femoral head, the necrosis was divided into three types: type 1, the posteromedial and central portions; type 2, part of the anterolateral portion; type 3, the entire anterolateral portion. The collapse rate and the time to collapse in different types were assessed.

RESULTS AND CONCLUSION: (1) All patients were followed up for 3-58 months. (2) Of the 60 hips with collapse, 46 (76.7%) hip collapse was identified on anteroposterior radiograph. On frog-leg lateral radiograph showing collapsed femoral head could be identified in 57 (95.0%) hips, which was significantly different (P < 0.01). (3) In all 102 hips, the collapse rate in type 3 osteonecrosis of the femoral head was significantly higher than that of type 2 osteonecrosis of the femoral head (P < 0.001), and the time to collapse was markedly shortened. None collapse occurred in all six hips with type I osteonecrosis of the femoral head during follow-up. (4) In summary, preservation of anterolateral portion is associated with potential collapse progression in necrotic femoral head.

Key words: osteonecrosis of the femoral head, bone structure, weight-bearing area, collapse, frog-leg lateral radiographs, imaging, bone preservation, the National Natural Science Foundation of China

中图分类号:

R445.2

魏秋实，方斌，陈镇秋，何敏聪，陈哓俊，杨帆，张庆文，何伟. 股骨头前外侧骨质状态在股骨头坏死塌陷进展中的作用[J]. 中国组织工程研究, 2019, 23(16): 2516-2522.

Wei Qiushi, Fang Bin, Chen Zhenqiu, He Mincong, Chen Xiaojun, Yang Fan, Zhang Qingwen, He Wei. Role of bone status in anterolateral portion of femoral head in the progression of osteonecrosis of the femoral head[J]. Chinese Journal of Tissue Engineering Research, 2019, 23(16): 2516-2522.

图/表（结果） 6

Imageology evaluation

MRI and radiographs were analyzed in consensus by two experienced orthopedic surgeons in the diagnosis and treatment for ONFH. By screening T1-weighted MRI images, the diagnosis of ONFH was identified on the basis of previously published criteria, and the stage of the disease and subclassifications were defined according to the ARCO staging system^[18]. The extent of the necrotic lesion in MRI was graded from A to C, representing less than 15% (type A), 15%-30% (type B) and more than 30% femoral head involvement (type C). Although the value of the China-Japan Friendship Hospital classification of ONFH based on 3 pillars of the femoral head is higher in predicting the collapse risk^[19], the disadvantage is that the missed diagnosis rate of collapse is existent (Figure 1). Based on this, FLL classification was proposed according to the site of the necrotic lesion on the anterolateral portion of the femoral head. Accordingly, the location of the necrotic lesion within the femoral head was described as posteromedial and central portions (type 1), part of the anterolateral portion (type 2), and the entire anterolateral portion (type 3), which account for 25%, 50%, and 25% of the head width, respectively (Figure 2). The collapse rate and the time to collapse in different types were assessed.

Statistical analysis

The data were analyzed using SPSS version 13.0 (SPSS Inc., USA). A P value of less than 0.05 was considered statistically significant. Chi-square and Fisher’s exact tests were used for statistical analysis.

RESULTS

Clinical characteristics of the subjects

Based on the inclusion and exclusion criteria, eight hips from five patients were excluded because of previous hip surgery in one patient, recent trauma to the femoral neck in two patients, and developmental dysplasia of the hip in two patients. Finally, 87 patients (102 hips) were enrolled into the study, including 65 men and 22 women with an average age of (44.38±12.74) years (19-73 years). Fifteen patients had bilateral sides and 72 patients had unilateral side of ONFH. All patients were followed for 3 to 58 months.

MRI and radiographic imaging

On MRI, the size of the necrotic lesion in the femoral head was graded as type A in zero hip, type B in 9 hips and type C in 93 hips (Table 1). On anteroposterior X-ray images, collapsed femoral heads were observed in 46 of 102 (45.1 %) hips, which were assigned to two hips in type B and 44 hips in type C (Table 1). On FLL images, collapsed femoral heads were found in 57 of 102 (55.9 %) hips, which were classified as type B (n=3) and type C (n=54), respectively.

In the 60 collapsed-hips, the number of the collapsed femoral heads was viewed on FLL X-ray films and was significantly higher than that of on anteroposterior X-ray films (P < 0.01). However, the time to collapse were lower on FLL X-ray films than that of on anteroposterior X-ray films (16.28±12.69) months versus (17.35±13.28) months), although the P value was greater than 0.05 (Figure 3). Fourteen (23.3 %) hips were only seen on FLL X-ray films but not on anteroposterior X-ray images. The three collapsed-hips (5.0%) were only detected on anteroposterior images, but not on FLL images (Table 1).

Collapse rate

In all 102 hips with ARCO stage II ONFH, the collapse rate in type 3 ONFH was significantly higher than that of in type 2 ONFH (P < 0.001),and the time to collapse was markedly shortened. No femoral head collapse was found in six hips with type 1 ONFH. In nine hips with ARCO stage II type B ONFH, there was a higher collapse rate in type 3 ONFH compared with type 2 lesions (100% vs. 20%), but this was not statistically significant because of the low number of patients. In 93 hips with ARCO stage II type C ONFH, the collapse rate for type 3 ONFH was significantly higher than compared with both type 1 and type 2 (Table 2).

Only six hips were classified as type 1 at entry into the study. At the final examination, all these joints were still at ARCO stage II, the patients were free from symptoms (Figure 4). All 44 hips of type 2 were at stage II at the initial examination, 32 (72.7%) were still at stage II and 12 (27.3%) had collapsed of the femoral head during follow-up (Figure 5). The total incidence of collapse in all type 3 femoral heads, was 86.5% (45 to 52), 26 of these developed to stage III in three to 43 months (mean 21 months), and 19 of these having advanced to ARCO stage IV in three to 18 months (mean 11.5 months) after entry to the study (Figure 6).

参考文献

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[12] Yu T, Xie L, Zhang Z, et al. Prediction of osteonecrosis collapse of the femoral head based on the proportion of the proximal sclerotic rim. Int Orthop. 2015;39(6):1045-50.

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[27] Koo KH, Kim R. Quantifying the extent of osteonecrosis of the femoral head. A new method using MRI. J Bone Joint Surg Br. 1995; 77:875-880.

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引言

Osteonecrosis of the femoral head (ONFH) is a common disorder and generally progresses to collapse of the femoral head and secondary hip osteoarthritis^[1]. Hip pain and loss of function are the main complication of progressive collapse^[2]. It is known that patients between the ages of 35 and 55 are at highest risk^[3]. Available interventions should be used to preserve joint in the precollapse stages of ONFH^[4-5]. Therefore, it is critical to understand the mechanism of collapse and predict the potential risk of collapse.

Previous studies have indicated that elevated mechanical stress affect the development of the collapse of necrotic femoral head^{[6, 7]}. Daniel et al.^[8] reported that decreased the load-bearing capacity of the necrotic bone could cause high contact pressure in hip, which resulted in the collapse of the femoral head^[9]. The load-bearing ability of the necrotic lesion reduced as a result of impairment of bone structure properties in weight-bearing area^[10]. Therefore, an ideal method should aim at the bone preservation of the weight-bearing area to predict the progression of ONFH in precollapse stages, and an appropriate structural reinforcement of the femoral head was essential for the patients which had high risk of the collapse^[11].

Several pioneer methods have been proposed to predict the collapse of the femoral head base on the size and location of the necrotic lesion^[12-15]. These previously published studies concluded that the collapse occurred most often when the necrotic range was a large-sized and when the necrotic lesion was located more laterally of the weight-bearing surface of the femoral head. Additionally, Takashima et al.^[16] reported that lesion location was an important indicator for

predicting collapse in small necrotic lesions. The results of these studies demonstrated that lesion location occupying the lateral portion of the head was an important determinant in progression of necrotic femoral head. Likewise, Wen et al.^[10] showed that preservation of the lateral pillar of the femoral head was strongly associated with collapse progression in necrotic femoral head. However, during the clinical follow-up of ONFH, we found some patients with necrotic lesions occupying more than the medial two-thirds of the weight-bearing area without collapse on anteroposterior radiograph and with collapse on frog-leg lateral (FLL) radiograph. The FLL radiograph has a high accuracy in the detection of anterolateral femoral head-neck junction and is the imaging modality of choice in patients in whom there is a strong suspicion of cam femoroacetabular impingement^[17]. This phenomenon suggested that bone structure and load-bearing capacity of the anterolateral portion of necrotic femoral head might relate to femoral head collapse. Therefore, the current methods to predict the collapse of the femoral head may need to be improved to some extent so as to reduce the missed diagnosis rate of collapse.

中国组织工程研究杂志出版内容重点：人工关节；骨植入物；脊柱；骨折；内固定；数字化骨科；组织工程

The purpose of the present study was to investigate the relationship between bone preservation of anterolateral portion and collapse progression in necrotic femoral head, which might provide an accurate method for predicting the potential progression of collapse.

材料方法

讨论

The load-bearing ability of weight-bearing area within the femoral head has been reported to affect the progressive collapse in ONFH^{[20, 21]}. Contrast to it, seldom studies mentioned the exact portions of the necrotic femoral head referring to be the pivotal point of collapse. Our study showed that the location of the necrotic lesion involving anterolateral portion of femoral head played a vital role in potential collapse progression.

Collapse of the femoral head is the key morphologic change in osteonecrosis, due to its representing as destruction of the normal structure of the hip joint^[22]. To determine the prognosis of ONFH and assess whether conservative treatment or joint-preserving surgery, we must consider the risk of collapse. Previous studies have focused on size and location of the necrotic lesion affecting the progression of collapse in necrotic femoral head^{[23, 24]}. At present, there are different kinds of methods on the basis of the medical imaging system to assess size and location of the necrotic lesion for predicting the collapse. Until recently, the three-dimensional finite element model studies by analyzing MRI scans involving various angle, areas, and volume necrosis may be useful to predict the risk of collapse and to determine the therapeutic method for ONFH^{[10, 25, 26]}. These findings concluded that a small-sized necrotic lesion did not lead to collapse, whereas a medium- to large-sized necrotic lesion frequently did. However, most of the studies did not consider changes in necrotic location relative to the weight-bearing portion. When compared to two-dimensional medical images for predicting the collapse, MRI, CT, and X-ray have their own advantages. In the early stage of ONFH without plain radiologic evidence, MRI is the most sensitive diagnostic modality. Some scholars have proposed that MRI are extremely useful for predicting the collapse of the femoral head^{[20, 27]}. Koo et al.^[27] reported that the modified index of the necrotic portion, which was calculated on the basis of the arc of the necrotic portion in the mid-coronal image and that in the mid-sagittal image, was used to predict the risk of collapse and to ascertain the treatment modality in early-stage ONFH. Ha et al.^[28]reported that the Kerboul combined necrotic angle, which was the sum of the angles from the arc of the femoral head surface involved by necrosis on the midcoronal as well as the midsagittal magnetic resonance images, was used to assess future collapse of the femoral head. Nishii et al.^[29]demonstrated that collapse occurred frequently when the lesion volume was greater than 30% of the femoral head, and that lesion location was related to the risk of collapse when the lesion volume was less than 30% of the femoral head. Sun et al.^[13] reported that the China-Japan Friendship Hospital classification of ONFH, which based on the preservation of the lateral pillar within necrotic femoral head from MRI, was very helpful for prediction of the collapse risk. These studies were in line with a clinical study by Motomura et al.^[30] showed that collapse frequently occurred at the lateral boundary of the necrotic lesion and that the size of the necrotic lesion seemed to contribute to its progression. The above findings suggested that the extent and location of necrosis should be considered simultaneously for predicting the risk of collapse.

It is worth noting that most of the patients come to the hospital with radiographic findings and clinical symptoms. Once the radiographic change of osteonecrosis appears, the disease has a risk of developing into collapse. In our study, all investigated patients with ONFH had radiographic evidence and no collapse of the femoral head was found on radiograph, therefore they can be indicated ARCO stage II disease. Of note, the number of the collapsed femoral heads was significantly lower on anteroposterior radiograph compared with FLL radiograph. The FLL radiograph has been suggested as imaging option for viewing the anterolateral femoral head^[31]. A clinical study with follow-up investigations by Nagoya et al.^[32] and Zhao et al.^[33] showed that the collapse rate was decreased when the deep circumflex iliac pedicle bone graft was inserted in the anterolateral direction of the necrotic femoral head. We speculated that necrotic lesion involving the anterolateral portion of the femoral head might be an important point in collapse. In further, we proposed FLL classification of ONFH based on the preservation of anterolateral portion of the femoral head. Using this classification for evaluation of the natural progression of ONFH, we found that 45 of 52 femoral heads with type 3 ONFH collapsed when the lateral boundary of the necrotic lesion was located at the anterolateral region of the femoral head. Of the 44 hips with type 2 ONFH, 12 hips collapsed. In all six hips with type 1 ONFH, no collapse occurred. We therefore considered that the necrotic lesion involving the anterolateral region of the femoral head was the key point of a collapse. The more the lateral part of the necrotic area, the faster the collapse occurred, the more serious of the collapse.

Some studies concluded that the size of the necrotic lesion might be one of the influential factors in collapsed regions^{[23, 34]}. One of the important study by Nishii et al.^[29]found that large size of the necrotic lesion was strongly associated with risk of collapse, and that necrotic location was an important prognostic indicator of collapse in small necrotic lesions. In our study, the size of the necrotic lesion involved more than 30% of the femoral head (type C) in 91.2% of the cases, and that involved 15-30% of the femoral head (type B) in only 8.8% of the cases. In 93 hips with type C ONFH, the collapse rate in type 3 ONFH is 86%, and that in type 2 ONFH is 28.2%. In 9 hips with type B ONFH, all two femoral heads with type 3 ONFH collapsed, and 1 of 5 femoral heads with type 2 ONFH collapsed. Our results demonstrated that necrotic lesion involving anterolateral femoral head was an important predictive indicator of collapse and involved either 15%-30% or more than 30% of the femoral head. Although there was no significant difference in the collapse rate between different sizes of the necrotic lesion, we were uncertain whether the extent of the necrotic lesion contributed to the risk of collapse. This was probably due to the size of samples with ARCO stage II type B ONFH in our study was relatively small. We acknowledge that this study has several limitations. First, this study is a retrospective study; hence, no sufficient causality can be demonstrated for the relationship between involvement of anterolateral portion and femoral head collapse and time to collapse. The biomechanical study by three-dimensional finite element models will be better able to provide the theoretical basis. Second, the FLL classification could not be applied for the assessment of the prognosis of ONFH at ARCO stages 0 and I, because X-ray images did not show these imaging features, and only patients with ARCO stage II who were diagnosed with having ONFH on MRI imaging and plain films of the hip were included to this study. Third, this study was the lack of statistical significance in the ARCO stage II type B ONFH group due to lower sample size.

Our data indicated that the number of the collapsed femoral heads was viewed on frog-leg lateral radiographs was significantly higher than that of on anteroposterior radiographs. The FLL classification of ONFH based on the preservation of anterolateral portion has high clinical value for evaluating the prognosis of ONFH. This study might be helpful to decrease the missed diagnosis rate of femoral head collapse, to predict the prognosis of ONFH and to determine the appropriate treatment. Hip preservation surgery for preventing the collapse of the femoral head is necessary when anterolateral portion is involved in the necrotic lesion.

中国组织工程研究杂志出版内容重点：人工关节；骨植入物；脊柱；骨折；内固定；数字化骨科；组织工程

股骨头前外侧骨质状态在股骨头坏死塌陷进展中的作用

Role of bone status in anterolateral portion of femoral head in the progression of osteonecrosis of the femoral head

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