Evaluation of distal femoral cartilage by B-mode ultrasonography and shear wave elastography in patients with knee osteoarthritis: a preliminary study

Abstract

Background

Degenerative change in articular cartilage is one of the most important factors in the development of osteoarthritis. Shear wave elastography can be used to identify pathologic cartilage.

Purpose

To evaluate distal femoral cartilage by shear wave elastography in patients with symptomatic knee osteoarthritis.

Material and methods

Twenty patients with bilateral knee osteoarthritis (study group) and 20 volunteers with the same demographic characteristics but without symptomatic knee pain (control group) were included in the study. A total of 80 knee joints of 40 individuals were evaluated. At the medial, intercondylar, and lateral condylar levels distal femoral cartilage thickness was measured by B-mode ultrasonography and stiffness was measured by shear wave elastography.

Results

The medial, intercondylar, and lateral cartilage thickness measurements were similar between the two groups and no statistically significant difference was observed (P = 0.711, P = 0.766, and P = 0.575, respectively). The shear wave velocity values in the medial and intercondylar cartilage were significantly higher in the study group (P = 0.002). Shear wave velocity values measured from lateral cartilage were higher in the study group and the difference between the groups had a borderline statistical significance (P = 0.053).

Conclusion

Shear wave elastography seems to be a reliable, non-invasive, and acceptable method for the assessment of pathologic cartilage.

Keywords

Shear wave elastography ultrasound distal femoral cartilage osteoarthritis

Introduction

Osteoarthritis (OA) is the most common form of arthritis. Although many joints in the body are affected, load-bearing joints, especially the knee joints, are frequently involved. The prevalence of OA increases with age, approximately 40% of adult population aged > 60 years have symptomatic knee OA (1,2).

Articular cartilage is a special connective tissue surrounding the distal part of the bone in synovial joints. Focal degeneration and progressive loss of articular cartilage occur in joints with OA involvement. Therefore, determination of cartilage degeneration is important for understanding the pathophysiology and clinical progression of OA (3,4).

Plain radiography is frequently used in the diagnosis and follow-up of OA patients; it may show indirect findings of femoral articular cartilage involvement, but it is not sensitive to show minor changes in cartilage. Although arthroscopy is a reliable and sensitive method, it is an invasive technique that limits its use. Magnetic resonance imaging (MRI) is a non-invasive method that provides multiplanar imaging and good soft-tissue contrast; however, being expensive and time-consuming limits its routine use (1,4).

Ultrasonography (US) is a reliable tool for assessing the integrity and thickness of articular cartilage. Other advantages include being inexpensive, non-invasive, fast, and easily accepted by patients (3,4). US elastography is a new non-invasive imaging method that can identify differences in stiffness between tissues and has different types based on different technical principles. In the present study, we use the shear wave elastography (SWE) technique, which works with the principle of acoustic radiation force impulse (ARFI) imaging. SWE is a method that quantifies the elasticity of tissues by measuring the velocity of shear waves in tissues. Shear wave velocity (SWV) is expressed in m/s. The obtained SWV value is proportional to the stiffness level of the tissue to which it belongs (5,6). When we searched in the literature, we found that there were studies using the strain elastography method for articular cartilage in OA of the knee, but there was no study using the SWE technique. Since the SWE technique is a newer and user-independent dynamic method, we think that we can better evaluate the structural change in articular cartilage with this technique. The data obtained will help us to better understand the degeneration process of articular cartilage in patients with OA.

Material and Methods

Patients

Twenty patients (4 men, 16 women) with bilateral symptomatic knee OA followed by physical medicine and rehabilitation clinic of our hospital were included in the study. Patients who had previous knee trauma or surgery and had a history of previous fracture and septic arthritis were excluded from the study. The control group consisted of 20 volunteers (4 men, 16 women) with the same demographic characteristics but without symptomatic knee pain. A total of 80 knee joints in 40 individuals were examined. The study was approved by the Institutional Ethics Committee. Before participation in the study, all patients and volunteers were informed about the procedure and written informed consent was obtained.

B-mode US and SWE examination

B-mode US and SWE were performed in all patients and volunteers who participated in the study. All examinations were performed by a single radiologist with nine years and five years of experience in US and SWE, respectively. US and SWE examinations were performed with Siemens ACUSON S2000 (Siemens Healthcare, Erlangen, Germany) brand device. ARFI imaging-based SWE application was performed using a virtual touch tissue imaging quantification (VTIQ) option using a 4–9 MHz 9L4 linear transducer. The “breast” option was used as factory preset for the examinations. Individuals were allowed to lie comfortably on the examination table in the supine position and to keep their knees in maximum flexion. The US probe was placed on the suprapatellar region in the axial plane. At first, distal femoral cartilage thickness was measured from three separate sites: medial condyle, lateral condyle, and intercondylar area midpoints. The distance between hyperechoic lines at the synovial space–cartilage interface and the cartilage–bone interface was evaluated as cartilage thickness (Fig. 1). Following B-mode US examination, SWE was performed while the patient and the probe were in the same position as described above. Split-screen imaging mode was used to obtain B‐ mode and SWE images at the same location. The distal femoral cartilage contour was manually drawn by the radiologist on the B-mode screen; this drawing was automatically added to the SWE image on the split-screen. Three separate measurements were performed in the medial condyle, intercondylar area, and lateral condyle, and the mean value of these measurements was defined as the SWV value. In the study, only numerical results were evaluated without any color-coded maps (Fig. 2).

Fig. 1.

Ultrasound axial images of distal femoral cartilage with medial condyle, intercondylar area, and lateral condyle cartilage thickness measurements. (a) The knee of an asymptomatic female volunteer; cartilage interfaces are observed relatively sharply. (b) The knee of a symptomatic female patient; cartilage has less defined interfaces.

Fig. 2.

Shear wave elastography with virtual touch tissue imaging quantification of the distal femoral cartilage of an asymptomatic female volunteer (a) and a symptomatic female patient (b).

Intra-operator and inter-operator variability analysis

For intra-operator reliability, measurements were repeated 2 h later by the same radiologist. To assess the inter-operator variability, measurements were performed by a different radiologist, who had 15 years and five years of experience in conventional US and SWE, respectively, after the first radiologist. Ten individuals from the control group and 10 individuals from the study group were randomly selected for intra-operator and inter-operator variability analysis.

Statistical analysis

Descriptive statistics for the studied variables were expressed as mean ± SD, and minimum and maximum values. First, the normal distribution of parameters was confirmed by the Shapiro–Wilk test, and then parametric statistical analysis was performed. Independent t-test was used to compare group means in terms of continuous variables. Pearson correlation coefficients were used to determine the relationship between variables. Besides that, intra-observer and inter-observer reliability was presented as the intraclass correlation coefficient. Statistical significance was set at P < 0.05. SPSS software (ver.23) was used for all statistical analyses.

Results

Twenty patients (4 men, 16 women; mean age = 62 ± 7.6 years; age range = 48–74 years) followed up by physical medicine and rehabilitation clinic for bilateral symptomatic knee OA and 20 volunteers (4 men, 16 women; mean age = 60 ± 7.3 years; age range = 50–77 years) with the same demographic characteristics but without symptomatic knee pain were evaluated in the study. There was no statistically significant difference between the two groups in terms of mean age (P = 0.270). Body mass index (BMI) was 28.47 ± 2.55 kg/m² (range = 25.1–33.3 kg/m²) in the study group and 28.48 ± 3.52 kg/m² (range = 23.6–39.7 kg/m²) in the control group; there was no statistically significant difference (P = 0.988).

Comparative US and SWE results are summarized in Table 1. Cartilage thickness measurements from the medial condyle, intercondylar area, and lateral condyle were similar; no statistically significant difference was observed (P = 0.711, P = 0.766, and P = 0.575, respectively). The SWV values measured from the medial condyle and intercondylar area were significantly higher in the study group than in the control group (P = 0.002). SWV values in the lateral condyle were higher in the study group (7.36 ± 1.69) than in the control group (6.67 ± 1.44); the difference between the groups had a borderline statistical significance (P = 0.053).

Table 1.

Comparative cartilage thickness and SWV values.

	Study group		Control group
	Mean ± SD	Range	Mean ± SD	Range	P
Thickness of medial cartilage (mm)	1.77 ± 0.47	1.00–2.80	1.80 ± 0.28	1.30–2.50	0.711
Thickness of intercondylar cartilage (mm)	2.05 ± 0.54	1.00–3.20	2.02 ± 0.33	1.30–2.50	0.766
Thickness of lateral cartilage (mm)	1.71 ± 0.42	0.90–2.70	1.66 ± 0.32	0.90–2.40	0.575
SWV value of medial cartilage (m/s)	7.16 ± 1.66	3.97–9.94	6.05 ± 1.34	3.61–9.06	0.002
SWV value of intercondylar cartilage (m/s)	8.48 ± 0.96	6.04–9.93	7.77 ± 1.03	5.48–9.91	0.002
SWV value of lateral cartilage (m/s)	7.36 ± 1.69	4.07–9.93	6.67 ± 1.44	3.95–9.61	0.053

SWV, shear wave velocity.

We found a moderate negative correlation between BMI and age in both groups (P < 0.05, r = –0.401 in the study group, P < 0.05, r = –0.377 in the control group, respectively). In the control group, BMI did not correlate with cartilage thickness and SWV values that performed at three different sites. In the study group, BMI had a moderate negative correlation with intercondylar cartilage thickness and medial cartilage SWV value (P < 0.05, r = –0.346 and P < 0.05, r = –0.3336, respectively); however, it had no significant correlation with medial and lateral cartilage thickness or intercondylar and lateral cartilage SWV values.

Intra-operator and inter-operator reliability was high for SWV values, the intraclass correlation coefficients in medial, intercondylar, and lateral cartilage were 1.000, 0.995, and 0.998 (P < 0.01) for intra-observer evaluation, and 0.998, 0.984, and 0.990 (P < 0.01) for inter-observer evaluation, respectively.

Discussion

OA a common cause of rheumatic complaints and is an important public health problem. In OA, cartilage and soft tissues are affected as well as bone tissue, and degenerative changes emerge in the involved joint (7). The knee joint is one of the most commonly affected joints in OA, and plain radiography is the most commonly used imaging method in the diagnosis and follow-up of the disease. In plain radiographs, narrowing of the joint space is an important finding. However, plain radiographs are insufficient to show the loss of articular cartilage, which is one of the causes of joint narrowing (8). In the evaluation of articular cartilage, MRI and US seem to be effective among radiological methods. Quantitative data can be obtained in the evaluation of cartilage by advanced techniques such as delayed gadolinium-enhanced MRI of cartilage (dGEMRIC), T2 mapping, sodium MRI, and T1 rho-mapping, especially due to the developments in MRI technology (9). Ultrasonography is a more easily accessible, repeatable, and less costly examination; cartilage thickness and pathologies have been successfully demonstrated in studies with US (10 –12). In the present study, US examination was used, and there was no significant difference in terms of sonographic cartilage thickness between symptomatic patients and asymptomatic volunteers. Cartilage thickness measurements were in the range of 0.9–3.2 mm and our results were similar to other studies in the literature (1,4,13 –15). However, contour irregularities and echogenicity changes at interfaces due to cartilage destruction can be expressly seen by the B-mode US.

In the studies evaluating distal femoral cartilage by strain elastography technique, it has been reported that elastography is a simple and feasible method to differentiate healthy cartilage from pathologic cartilage (4,16). In the study by Cay et al. (4), strain ratios of 25 patients with pathological findings of distal femoral cartilage on MRI scans were higher than those of 25 patients with intact cartilage on MRI scans and elastography was reported to be an effective tool for demonstrating pathologic cartilage. To the best of the authors’ knowledge, this is the first study to evaluate the effect of OA on distal femoral cartilage by SWE technique. We measured significantly higher SWV values in the medial condyle and intercondylar area in the study group compared to the control group. SWV values measured in the lateral condyle were higher in the study group, and the difference between the two groups was borderline statistically significant. Akkaya et al. (15) and Güngör et al. (16) found a significant difference in medial cartilage strain ratio values in their study with the strain elastography technique. Given the fact that knee OA usually starts from the medial compartment, and this compartment is affected more than the lateral compartment, the data obtained from the studies may be significant. However, we believe that further studies, including histopathological findings, are still needed to evaluate the relationship between sonoelastographic findings and degenerative changes in cartilage.

The small sample size is one of the most important limitations of our study. Another limitation of the study was that the male population was less representative due to the small number of men in both groups. Furthermore, we could not compare the Kellgren–Lawrence grading system due to the lack of plain radiographs of the knee joint in the control group. The fact that our ultrasonographic data are not correlated with a method such as arthroscopy or MRI can be considered as another limitation of our study.

In conclusion, in light of the data obtained in our study, we found a significant difference in the stiffness/elasticity of cartilage especially in the medial compartment of the knee joint by SWE technique in symptomatic knee OA. We think that US and SWE may be preferred for the evaluation of joint cartilage, especially in cases where MRI is contraindicated. Further studies with larger sample sizes are needed to determine the importance and reliability of SWE in cartilage imaging.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Adem Yokuş

Nurşen Toprak

Hüseyin Akdeniz

Ali Mahir Gündüz

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