Abstract
The present study investigates the feasibility of micro perfusion of femoral head specimens from femoral neck fracture patients by the inferior retinacular arteries and performing intraosseous artery quantitative analysis of the femoral head. Twelve femoral neck fracture patients who had undergone conventional hip replacement surgery were included in this study. Femoral head specimen arteries were first dissected and exposed and then perfused by the inferior retinacular arteries and all the femoral heads underwent micro‐CT scanning. After micro‐CT scanning, a digital 3‐D model was reconstructed to quantify the femoral head intraosseous arteries for comparison with a normal femoral head. The artery length density, artery volume density, and artery length/volume ratio were calculated separately and compared with normal femoral head parameters. Micro‐CT scanning displayed the epiphyseal arterial network structure and their fine vascular branches in all 12 femoral neck fractures. Blood was supplied from the inferior retinacular artery to the epiphyseal arterial network then to all the fine blood vessels within the femoral head. No statistical differences were observed in femoral heads’ intraosseous artery length densities or volume densities between the normal and femoral neck fracture specimens, while the artery length/volume ratio showed a statistical difference, and the ratio increased from 19 to 46. Micro perfusion of the femoral head by the inferior retinacular arteries is possible and can present the epiphyseal network and their fine arterial branches in pathologic conditions to provide a morphological basis for the study of femoral head disease.
Keywords: Femoral neck fracture, Inferior retinacular artery, Intraosseous artery, Micro‐CT, Micro perfusion
Introduction
Avascular necrosis of the femoral head (ANFH) is a common clinical disease, although the pathogenesis of ANFH remains uncertain1, 2. Both traumatic and non‐traumatic ANFH are usually caused by disruption of the blood supply to the femoral head. The traditional view is that the femoral head receives its primary blood supply from the superior retinacular artery. The stem of the superior retinacular artery is located under the joint synovial fold, close to the lateral edge of the femoral head. A femoral neck fracture can damage this artery, and superior retinacular artery injury is considered to be the main cause of traumatic ANFH3, 4. A femoral neck fracture can directly damage the femoral head blood vessels and cause hematoma. Traction will increase the pressure inside the hip capsule, causing pressure even greater than arterial perfusion pressure, which will subsequently reduce arterial perfusion and venous reflux5.
A recent study shows that the branches of the superior, inferior, and anterior groups constitute an epiphyseal arterial branch after entering the femoral head and then anastomose with each other from the periphery to the center and form an epiphyseal arterial network above the epiphyseal scar6. Assessment of residual blood supply after femoral neck fracture in adults based on the preoperative digital subtraction angiography showed that the inferior retinacular artery is less affected after femoral neck fractures; thus, theoretically, the inferior retinacular artery and epiphyseal arterial network could be two important structures for maintaining the femoral head blood supply after femoral neck fractures4, 6.
Currently, the main methods for the clinical study of intraosseous blood vessels are enhanced computed tomography (CT) scanning, super selective digital subtraction angiography (DSA) angiography, and enhanced magnetic resonance image (MRI) scanning7, 8, 9, 10, 11. However, enhanced CT scanning, super selective DSA angiography, and enhanced MRI scanning are limited by the resolution scope and cannot display the epiphyseal network or the fine blood vessels within the femoral head in pathologic conditions (e.g. femoral neck fracture, hip dysplasia, or necrosis).
It is possible to study the structure of the microvasculature within the bone using ex vivo micro angiography, but it is significantly limited in that it usually must be observed by being sliced into pieces12. Reportedly, a normal anatomic specimen can be reconstructed by vascular perfusion without destruction of the bone, which can be used to directly reconstruct the blood vessels in the bone, to display the intraosseous arterial structure and the fine vascular branch, and to quantify the bone structure simultaneously13. However, most research has focused on the study of anatomical structures in normal cadavers through injections into the femoral artery (ϕ = 7 mm), and lower limb specimens of the skin and soft tissue structures must remain intact13, 14, 15. In the existing research method for femoral head samples, the intraosseous artery must first be decalcified16. The mean diameter of the femoral head main intraosseous artery and the fine vascular branch is approximately 0.3 mm, and this is outside the resolution scope of conventional CT and MRI6. The main femoral head intraosseous arterial structure and the fine vascular branch have important effects on bone cell physiology and play an important role in the pathological process of fracture union and femoral head necrosis. To provide intraosseous arterial structure evidence for preoperative planning, scholars have conducted a great deal of basic and clinical research on the femoral bone blood supply; however, the intraosseous artery supply of the femoral head after femoral neck fracture is still not clear.
In this paper, femoral head specimens were perfused by the inferior artery (ϕ = 0.4 mm), and microscopic CT scans were taken without the strict requirements for soft tissue integrity. We used femoral head specimens from femoral neck fracture patients after hip replacement to introduce this new research technique of micro perfusion, and present a quantitative analysis of the femoral head intraosseous artery.
Materials and Methods
Inclusion and Exclusion Criteria
Inclusion criteria: (i) patients over the age of 55 years with femoral neck fracture (Garden I to Garden IV type); and (ii) patients who underwent conventional hip replacement surgery.
Exclusion criteria: (i) patients who had any previous hip pathologies or surgeries and had known history of previous traumatic injuries; (ii) patients who had infectious diseases; and (iii) patients with congenital abnormalities.
Patients
Twelve clinical femoral head specimens from June 2016 to December 2016 were included in this study, including 2 male and 10 female patients. The mean age of the patients was 69.5 years (range, 55–90 years; Table 1). Our Institutional Review Board granted approval for this study and approved the informed consent form for the patients.
Table 1.
Femoral head samples data after hip replacement
| Number | Gender | Age (years) | Fractures of the hip | Garden type | Fracture–perfusion interval (days) |
|---|---|---|---|---|---|
| 1 | F | 74 | R | 4 | 98 |
| 2 | F | 77 | L | 4 | 7 |
| 3 | F | 75 | R | 4 | 5 |
| 4 | F | 83 | R | 3 | 5 |
| 5 | F | 60 | L | 3 | 3 |
| 6 | F | 84 | L | 3 | 9 |
| 7 | F | 56 | R | 3 | 6 |
| 8 | F | 63 | L | 3 | 4 |
| 9 | M | 62 | R | 3 | 10 |
| 10 | F | 55 | L | 2 | 5 |
| 11 | F | 56 | L | 1 | 8 |
| 12 | M | 90 | R | 1 | 8 |
F, female; L, left; M, male; R, right. Fracture–perfusion interval indicates interval days between femoral neck fracture occurring and vascular perfusion.
Published data for normal human femoral head intraosseous quantifying artery length densities, artery volume densities, and artery length/volume ratio were used for the normal control group13. These femoral heads were free of any previous hip pathologies or surgeries and had no known history of previous traumatic injuries and no congenital abnormalities. The mean donor age at the time of death was 37.2 years (range, 25–67 years).
Contrast Agent Preparation and Micro Perfusion Methods
The technique for the visualization of the intraosseous arteries of the femoral head was based on previously described methods in investigations of the normal human femoral head artery, with some improvements6, 13. In each femoral head, the inferior retinacular artery was dissected and exposed (Fig. 1). The inferior arteries of the femoral head were infused with a gelatin barium sulfate suspension as a contrast agent.
Figure 1.
Photograph shows a femoral head inferior retinacular artery that was dissected and exposed. A customized catheter (ϕ = 0.4 mm) was inserted into the inferior retinacular artery.
Under a surgical microscope at approximately eight times magnification, a customized catheter (ϕ = 0.4 mm) was inserted into the inferior retinacular artery, and a knot was tied with 4–0# surgical suture (Fig. 1). The femoral head was placed in a 37°C water bath 2 h prior to perfusion. A customized device that created and maintained a constant pressure (130–140 mm Hg) was used for at least 20 min to perfuse the suspension into the femoral artery. After perfusion, the femoral head was placed in a 0°C water bath for 20 min to allow the suspension to enter a gel state. Finally, all the femoral heads underwent micro‐CT scanning.
Micro‐Computed Tomography Scanning, Intraosseous Artery 3‐D Reconstruction and Quantification
The femoral head was fixed on a scanning bed and scanned under the same conditions using a micro‐CT scanner (Inveon Multi Modality, Siemens Medical Solutions, Malvern, PA, USA). The acquisition protocol was as follows: Binning1, system magnification low–med, total rotation 360°, real‐time reconstruction, down sample factor 2, resolution 24.37 μm, and exposure time 200 ms. After the scan, the digitized perfused femoral head data were imported into Image Research Workplace V4.1 software (Siemens Medical Solutions, Illinois, USA) and exported as a file in the digital imaging and communications in medicine (DICOM) format for the standardized quantitative measurement of digital bones and arteries, including the density, morphology and distribution of the trabecular bone, arterial length density, arterial volume density, and vascular anastomosis.
The perfused femoral head DICOM‐format data were imported into MIMICS 14.0 (Materialise Europe, Leuven, Belgium) and AMIRA 5.4.3 (FEI Visualization Sciences Group, Hillsboro, OR, USA) and the intraosseous 3‐D arteries were reconstructed, including the femoral head intraosseous artery area, and the arterial volume and femoral head bone volume were quantified. The artery length density, artery volume density, and artery length/volume ratio were calculated separately and compared with normal femoral head parameters13. The arterial volume‐rendering and 3‐D orthogonal projection views of the intraosseous vasculature are presented as screenshots from Image Research Workplace V4.1.
Statistical Analysis
The data was expressed as mean ± standard deviation (SD). Statistical analysis was performed with SPSS 17.0 software (SPSS, Chicago, IL, USA). Independent‐sample t‐test analysis was used for comparisons of the femoral neck fracture and normal femoral head intraosseous arteries length densities, artery volume densities and artery length/volume ratio. In all tests, P < 0.05 was considered statistically significant.
Results
In this study, 12 femoral head specimens taken from patients following hip replacement were perfused successfully by the inferior retinacular artery. Micro‐CT scanning and arterial 3‐D reconstructions were performed, displaying the epiphyseal arterial network structure above the epiphyseal scar and the fine vascular branches of the epiphyseal arterial network in all 12 femoral heads of Garden I‐IV type femoral neck fractures (Fig. 2).
Figure 2.
A 74‐year‐old female, Garden IV‐type, 98 days between femoral neck fracture occurring and vascular perfusion. The postoperative femoral head specimen was perfused. After micro‐CT scanning, a 3‐D projection of the intraosseous blood vessels was reconstructed. (A) X‐ray showing the patient’s femoral neck fracture in the hip anteroposterior position. (B) Diagram of the femoral head specimen after hip arthroplasty. (C, D) Femoral head vascular 3‐D orthogonal projection (anteroposterior and lateral views). (E) Orthogonal projection views of the arterial network and 3‐D reconstruction of the intraosseous vascular of the femoral head. (F) Enlargement of intraosseous vascular 3‐D reconstruction.
Volume‐rendering and 3‐D Orthogonal Projection
The volume rendering and 3‐D orthogonal projection present the location of the arteries in the bone, the artery direction, and the arterial branch distribution and anastomosis with the adjacent vessels (Fig. 2). After femoral neck fracture, blood supply is impaired. Even after many days interval, the distribution of blood vessels in the femoral head model is consistent with the normal adults, and damage is limited. Blood was supplied from the inferior retinacular artery to the epiphyseal arterial network then all the fine blood vessels within the femoral head. The morphological characteristics and the development of vascular branches at all levels were present in this study.
Digitization of the Intraosseous Artery
The data can be imported into the IRW, the AMIRA, and MIMICS software programs for quantitative research. Data of the femoral head intraosseous artery quantitative statistics are shown in Table 2. Artery length is 3571 ± 1879 mm, and length density is 0.2237 ± 0.1283. Artery volume is 101 ± 65 mm3, and volume density is 0.0058 ± 0.0036. The length/volume ratio is 46 ± 21.
Table 2.
Quantitative data of femoral head intraosseous arteries (n = 12)
| Indexes | Mean | Standard deviation | Minimum | Maximum | Quartiles | ||
|---|---|---|---|---|---|---|---|
| Lower | Median | Upper | |||||
| Artery length (mm) | 3751.6 | 1879.2 | 337.1 | 6492.6 | 2177.7 | 4176.5 | 5066.5 |
| Artery volume (mm3) | 101.0 | 64.6 | 4.4 | 216.0 | 33.9 | 112.2 | 144.3 |
| Bone volume (mm3) | 17331.4 | 3942.4 | 11317.4 | 24737.5 | 14946.1 | 16956.8 | 20301.4 |
| Artery length density | 0.2237 | 0.1283 | 0.0298 | 0.4354 | 0.1069 | 0.2303 | 0.3253 |
| Artery volume density | 0.0058 | 0.0036 | 0.0004 | 0.0110 | 0.0017 | 0.0068 | 0.0084 |
| Artery length/volume | 46.43 | 21.70 | 20.39 | 93.10 | 34.01 | 36.97 | 57.98 |
Artery length density, artery length/bone volume; artery volume density, artery volume/bone volume.
The quantitative comparison of the femoral head vasculature between a normal and femoral neck fracture is shown in Table 3. No statistical differences were observed in intraosseous artery length densities or volume densities. However, the artery length/volume ratio showed a statistical difference. The ratio increased from 19 to 46.
Table 3.
Femoral head intra‐osseous artery length density, volume density, artery length/volume ratio (mean ± SD)
| Indexes | Femoral neck fracture (n = 12) | Normal (n = 13) | t‐value | P‐value |
|---|---|---|---|---|
| Artery length density | 0.2237 ± 0.1284 | 0.1400 ± 0.0632 | −2.042 | 0.058* |
| Artery volume density | 0.0058 ± 0.0036 | 0.0075 ± 0.0030 | 1.306 | 0.205* |
| Artery length/volume | 46.44 ± 21.70 | 19.08 ± 6.51 | −4.196 | 0.001† |
Independent‐sample t = test analysis: in all tests, P < 0.05 was considered statistically significant. Artery length density, Artery length/Bone volume; Artery volume density, Artery volume/Bone volume
No statistical difference between the normal and femoral neck fracture
Statistical difference between the normal and femoral neck fracture.
Discussion
Micro perfusion by a single inferior retinacular artery and the quantitative analysis of the femoral head intraosseous artery after hip replacement are possible. In this study, 12 femoral head specimens following hip replacement were perfused by the inferior retinacular artery. Micro‐CT scanning and arterial 3‐D reconstructions were performed. The epiphyseal arterial network structure above the epiphyseal scar and the fine vascular branches can be found in all the femoral heads from Garden I to Garden IV‐type femoral neck fractures in this study. Femoral neck fracture itself does not damage the epiphyseal arterial network structure above the epiphyseal scar or the fine vascular branches within the femoral head. From a clinical perspective, the femoral neck fracture Garden classification and femoral head artery injury have a positive correlation. Here, judging from the results of this small sample size, the femoral head intraosseous epiphyseal arterial network structure above the epiphyseal scar and the fine vascular branches may remain intact under the condition of a large degree of displacement. If at least one of the retinacular arteries survives, the epiphyseal arterial network structure above the epiphyseal scar and the fine vascular branches can maintain the entire blood supply to the femoral head after a femoral neck fracture6.
This study confirmed that Garden types I–IV femoral neck fractures and intact femoral head epiphyseal arterial networks and retinacular arteries (especially the inferior retinacular arteries) can co‐exist, which is the anatomical basis for the maintenance of blood supply to the femoral head. Preoperative DSA can verify the affected retinacular arteries and delineate the possible compensatory arterial supply to the femoral head after a femoral neck fracture4, 6. This approach can provide an objective basis for surgeons to develop an appropriate hip joint‐preserving therapeutic strategy, especially in young patients for whom femoral neck fractures have great significance.
We suggest that orthopedists who perform internal fixation of femoral neck fractures should try to avoid damaging the femoral head epiphyseal arterial network structure above the epiphyseal scar and the fine vascular branches to avoid further damage to the femoral head blood circulation. The quantitative values of the arteries of femoral neck fractures were similar to those of a normal femoral head, but the artery length/volume ratio showed a statistical difference13. Possible explanations for these results include the capability of the retinacular arteries and the epiphyseal arterial network structure to supply blood to the femoral head after femoral neck fracture, and the potential presence of more small blood vessels that are open in the femoral head of femoral neck fractures.
Limited by the small sample size, this study mainly discusses the feasibility of the micro perfusion method and the quantitative analysis of the femoral head intraosseous artery after hip arthroplasty for femoral neck fractures, but no further comparative study is available. Under the microscope at approximately eight times magnification, micro perfusion and micro‐CT scanning can be used to quantify the distribution of the intraosseous artery in the progressive pathology of femoral head necrosis.
After femoral neck fracture, the retinacular arteries (especially the inferior retinacular arteries) supply blood to support the femoral head tissue and maintain the vitality of the femoral head bone marrow. These arteries have a positive role in bone formation and reconstruction and are critical to the blood supply relative to the pathological changes that occur in femoral neck fractures and in femoral head necrosis17. Consequently, it is very important to study the relationship between the femoral head and the intraosseous arteries. Currently, the main methods for the clinical study of intraosseous blood vessels are enhanced CT scanning, super selective DSA angiography, and enhanced MRI scanning18, 19. However, enhanced CT scanning, super selective DSA angiography and enhanced MRI scanning are limited by the resolution scope and cannot display the epiphyseal network or the fine blood vessels within the femoral head7, 8, 9, 10, 11. Conventional perfusion techniques are usually performed in the femoral artery (ϕ7 mm) and lower limb specimens of the skin, muscles, and bone, and all soft tissue structures must remain intact (including the femoral head)13. Overall perfusion is mainly used to analyze cadaveric specimens. The traditional view was that the integrity of the specimen is the key factor in successful perfusion. In this paper, the femoral head specimens were perfused only by the inferior retinacular arteries (ϕ0.4 mm), which were observed with microscopic CT scans. The specimens are no longer needed to adhere to the strict integrity requirements for all soft tissues. If the inferior retinacular blood vessels viewed under a microscope are found to be in good condition and there is no thrombosis, then perfusion will be successful. In this study, the perfusion contrast agent could not reach the veins through the small arteries.
The high resolution of micro‐CT can be used to simultaneously observe and quantify the intraosseous arteries in 3‐D directions13, 20 ,21. Arterial perfusion does not interfere with histological observations. After a micro‐CT scan, we can also perform hard tissue slicing without tissue decalcification or we can conduct biomechanical testing. In addition, the time and cost requirements of micro perfusion are lower than for the Spalteholz method, and this procedure has great significance in the study of intraosseous arterial vessel changes in osteonecrosis. Therefore, the study of micro perfusion and the quantitative study of femoral head intraosseous arteries after hip replacement for femoral neck fractures are highly valuable, as these methods are more convenient, less time‐consuming, and more reliable than the commonly used methods to study the intraosseous vasculature.
The limitation of this study is that the sample size is small. Consequently, femoral head intraosseous artery conditions cannot be divided according to the classification of different types of femoral neck fractures. Internal fixation of femoral neck fractures should avoid breaking the intraosseous vascular system but we require more biomechanical experiment validation to provide further detailed clinical recommendations.
Conclusion
Micro perfusion of the femoral head specimens after total hip arthroplasty by the inferior retinacular arteries and performing intraosseous artery quantitative analysis are possible. The epiphyseal arterial network structure above the epiphyseal scar and the fine vascular branches of the epiphyseal arterial network can be found in all the femoral heads from Garden I to Garden IV‐type femoral neck fractures in this study. Internal fixation treatment of femoral neck fractures should avoid breaking the intraosseous vascular system.
Disclosure: Funding was provided by National Natural Science Foundation of China (No. 81371942).
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