Application of virtual touch tissue imaging quantification in diagnosis of supraspinatus tendon injury

Abstract

OBJECTIVE:

To explore the value of virtual touch imaging and quantification (VTIQ) shear wave elastography (SWE) in diagnosis of supraspinatus tendon tear.

METHODS:

Eighty patients with unilateral supraspinatus tendon tear underwent shoulder arthroscopy were prospective studied. Tendinopathy, partial-thickness tear or full-thickness tear of supraspinatus tendon were diagnosed according 2D ultrasound examination. Sensitivity, specificity and accuracy of ultrasonic diagnosis of supraspinatus tendon tear were calculated by arthroscopy as the gold standard. VTIQ was applied to measure the shear-wave velocity (SWV) of both normal and affected supraspinatus tendon. The differences of SWV in three types of supraspinatus tendon tear and receiver operating characteristic (ROC) curves were analyzed.

RESULTS:

Among 80 patients, there were 20 tendinopathy, 31 partial tears and 29 full-thickness tears diagnosed by shoulder arthroscopy. Sensitivity, specificity and accuracy of 2D ultrasound in diagnosis of tendinopathy, partial tear and full-thickness tear groups were 78%, 90%and 83%; 71%, 86%and 73%; 86%, 88%and 88%, respectively. SWV of 80 supraspinatus tendon tears was 4.59±1.00 m/s, which was lower than that of normal supraspinatus tendon (4.59±1.00 m/s vs. 6.68±1.05 m/s, P < 0.01). SWV of supraspinatus tendon in tendinopathy, partial tear and full-thickness tear groups respectively were 5.66±0.97, 4.66±1.00, and 3.78±0.55 m/s, all lower than that of the contralateral normal supraspinatus tendon (all P < 0.05). In addition, the analysis of variance and pairwise comparison showed that SWV of supraspinatus tendon among three different degree of injury was statistically significant (all P < 0.001). The cutoff thresholds of SWV was 4.83 m/s to identify tendinopathy tear from partial tear and was 4.08 m/s to identify full-thickness tear from partial-thickness tear.

CONCLUSION:

VTIQ SWE with SWV might identify degree of supraspinatus tendon tear and improve the value of ultrasonography, which should be further evaluated in large multicenter studies.

Keywords

Supraspinatus tendon tear virtual touch imaging and quantification (VTIQ)ultrasonography shear-wave velocity

1 Introduction

The rotator cuff is four muscles connected by tendons to the humerus, or upper portion of the shoulder [1]. Rotator cuff disease is one of the most common musculoskeletal disorders in the adult population, leading to shoulder pain and limitation of movement [2]. When a rotator cuff tear occurs, one or more of the tendons detaches from the humerus. Particularly, the supraspinatus tendon is the most commonly affected tendon, that when there is an injury or weakness thereof, the normal balance of forces acting on the glenohumeral joint is interrupted, thus causing instability to said joint [3]. This condition may have high impacts on social life and associate to chronic pain, weakness and dysfunction of the upper extremities. Therefore, it is necessary to accurately and quantitatively evaluate the quality of rotator cuff tendon.

The current imaging techniques used to evaluate the rotator cuff tendon, including MRI and ultrasound, are qualitative and subject to high interobserver variability [4]. Among them, the ultrasonic examination has been used to diagnose shoulder diseases for decades, which can evaluate two-dimensional (2D) structure changes of rotator cuff and conduct dynamic scanning of rotator cuff tendon. The diagnostic value of 2D ultrasound in rotator cuff injuries has been widely recognized by clinicians [5, 6]. Recently, ultrasonic elasticity imaging is a new technology that widely applied to hamstring tendon tissue, which can be analyzed the elasticity and hardness information, quantitative assessment of rotator cuff tendon degeneration, each component damage and healing all kinds of pathologic states such as related mechanical properties change, and it is a useful supplement to conventional 2D ultrasound diagnosis [7].

Virtual Touch tissue imaging and quantification (VTIQ), as a new type of ultrasound elastography, can be used the acoustic radiation force impulse (ARFI) imaging technology to gently displace tissue for qualitative visualization and quantitative evaluation of tissue stiffness [8 –10]. Shear wave ultrasound elastography (SWE) is a relatively mature quantitative method for evaluating tissue elasticity or stiffness, which shows a promising result in musculoskeletal system [11, 12]. The speed of the shear wave, also known as the shear wave velocity (SWV). VTIQ can be used to record multipoint SWV with a wider range, which is directly related to the shear elastic modulus of tissue. Multiple region of interests (ROIs) can be placed on the elastogram to detect the pulse sequence, which can measure localized SWV from 0.5 to 10 m/s in multiple locations [12]. A higher SWV implies stiffer, less deformable tissue [4, 9]. VTIQ SWE has been shown to correlate with mechanical properties of tendon, and potentially tendon quality [7]. However, to our knowledge, VTIQ SWE has not been used in the discrimination of supraspinatus tendon tear. The purpose of this study is to evaluate whether VTIQ SWE with SWV can predict the degree of supraspinatus tendon tear and thus make ultrasonic examination play a greater role in the perioperative period of supraspinatus tendon tear.

2 Materials and methods

2.1 Patients

The study was approved by the Ethics Committee of the Third Hospital of Hebei Medical University, and all patients enrolled in this study provided informed consent to include the data for analysis. A total of 80 patients with unilateral supraspinatus tendon tear which were detected by VTIQ, underwent arthroscopic shoulder surgery from October 2018 to July 2019, were prospective studied. The inclusion criteria were as follows: (1) the time interval between ultrasound examination and surgery < 1 week; (2) untreated patients with unilateral shoulder pain; (3) the patients could tolerate ultrasound examination; (4) completely underwent arthroscopic shoulder surgery.

The case exclusion criteria were defined as follows: (1) the patient with a ruptured or infected shoulder; (2) a history of rotator cuff repair or shoulder replacement surgery; (3) patients with shoulder dislocation, calcified tendonitis or adhesive shoulder arthritis; (4) both sides of the shoulder joint were suspected to have lesions. According to the results of shoulder arthroscopy, the patients were divided into three groups: tendinopathy group, partial tear group and full-thickness tear group. The contralateral shoulder was taken as the normal control group.

2.2 US examination

All patients underwent a sonographic examination of supraspinatus tendon including color Doppler ultrasonography using a Siemens Acuson S3000 diagnostic ultrasound system (Siemens Medical Solutions, Erlangen, Germany) equipped with a 9L4 linear array transducer with a bandwidth of 4–9 MHz. The examination started with 2D ultrasonography, followed by VTIQ SWE. All conventional ultrasonographic and elastographic examinations were performed by a radiologist with 3 years of experience who had been trained by a VTIQ applications specialist. Afterward, two other investigators who did not participate in image acquisition and were blinded to patients’ medical information reviewed all of the sonograms images independently.

2.2.1 2D ultrasonography

The patient took the sitting position, and the supraspinatus tendon was scanned according to the standard shoulder joint examination method recommended by the musculoskeletal ultrasound technology guidelines reported by the European Society of Musculoskeletal Radiography (ESSR) [13, 14]. The supraspinatus tendon was examined in cross or longitudinal section, consisting of internal rotation and mild hyperextension. The patient was asked to move the shoulder joint for dynamic examination. The observations included the deformation, continuity, internal echo and surrounding bursa of tendon fibers, and the presence of joint effusion, synovial hyperplasia, smooth humeral head surface, and hyperosteogeny and osteochondral defects. According to the 2D ultrasonography diagnostic criteria of previous literatures [14, 15], the grading of supraspinatus tendon tears were as following: (1) Normal, the tendon is attached to the greater tuberosity of the humerus, has continuous parallel linear structure in the long axis and a moderately echoic with hyperechoic spot-like structure in short axis. (2) Tendinopathy, the tendons are extensively thickened with diffuse non-uniform hypoecho inside. The tendon was extensively thickened with diffuse and heterogeneous hypoechogenicity. (3) Partial tear, a) there were bursal surface, hypoechogenicity or no echogenicity within the tendon; b) the thickness of tendon was different, and part of tendon became thinner; c) the echo inside tendon was uneven, and part of tendon was broken and discontinuous. (4) Full-thickness tear: (a) the normal anatomical position of tendon did not show tendon structure, tendon continuity was completely interrupted and local loss; (b) hypoecho or no echo signal appears in the whole tendon layer; and (c) the broken end of the tendon is retractable, sometimes accompanied by thickening, mean while there were effusion in the bursa of deltoid under acromion and hydrops in tendon sheath of long head of biceps brachii.

2.2.2 VTIQ examinations

Following 2D ultrasound examination, the VTIQ velocity mode was switched. The radiologist located the probe vertical to supraspinatus tendon long axis and applied the probe with minimal pressure to create complete contact with the skin while letting the patient hold his or her breath. In SWV map, hard sections presented as red, medium-hard sections presented as yellow or green, and soft region sections presented as blue, which was able to determine the regions of interest (ROI) placement to evaluate the hardness of the tendon according to the various colors. SWVs were obtained in multiple 1 mm×1 mm regions of interest ROIs drawn within the insertional 2 cm of the supraspinatus tendon at the mid-portion of the superior greater tuberosity facet [16]. The number of ROIs ranged from three to five, depending on the degree of tendon retraction and the size of visualized intact tendon. The dynamic range for SWV measurements was 0.5–10 m/s. The arithmetic mean of three SWV values was calculated. VTIQ examination was performed on the contralateral normal shoulder joint of patients.

2.3 Statistical analysis

All statistical analyses were performed with the SPSS 21.0 software (SPSS, Chicago, IL) and MedCalc (Mariakerke, Belgium) software. The sensitivity, specificity and accuracy of 2D ultrasonic diagnosis of various supraspinatus tendon tear were calculated using the results of shoulder arthroscopy as the gold standard. The SWV of supraspinalis tendon at the affected side and the normal side were in normal distribution (P = 0.200, 0.081), and were expressed as mean±standard deviation. The differences of SWV values between two groups were performed with Paired-Samples T-test or Wilcoxon Rank-sum Test. One-way ANOVA was used to compare SWV with different lesion degrees among multiple groups. Spearman rank correlation coefficient was used to test the correlation between SWV and the degree of supraspinatal tendonopathy. The ROC curve was drawn by MedCalc and the diagnostic value of SWV was determined according to the area under the curve and thus to obtain cut-off value, sensitivity and specificity. Interobserver correlation agreement between the two radiologists was tested using an interclass correlation coefficient test. The ICC between the 2 observers was 0.81, indicating good reliability. P < 0.05 was considered statistically significant.

3 Results

In total of 80 patients with unilateral supraspinatus tendon tear (28 left shoulders, 52 right shoulder) were included in this study, in which 24 males and 56 females with a mean age±SD of 53.7±10.3 years (range, 30–79 years). All the enrolled patients had unilateral shoulder joint pain and limited mobility. Among the 80 affected shoulders, there were 20 cases of tendinopathy (aged 51.7±13.7 years, 7 males and 13 females, 9 left shoulders and 11 right shoulder) 31 cases of partial tear (aged 52.8±8.8 years, 8 males and 23 females, 11 left shoulders and 20 right shoulder) and 29 cases full-thickness tear (aged 56.1±9.1 years, 9 males and 20 females, 8 left shoulders and 21 right shoulder) that diagnosed by shoulder arthroscopy. The comparison diagnostic results of 2D ultrasonography and arthroscopic surgery were shown in Table 1. Taking arthroscopy as the gold standard, the sensitivity, specificity and accuracy of 2D ultrasound in the diagnosis of tendinopathy group, partial tear group and full-thickness tear group were 78%, 90%and 83%; 71%, 86%and 73%; 86%, 88%and 88%, respectively (Table 2).

Table 1
The comparison diagnostic results of 2D ultrasonography and arthroscopic surgery

2D ultrasonography Arthroscopic surgery Total

Tendinopathy (n) Partial tear (n) Full-thickness tear (n)

Tendinopathy (n) 14 5 1 20

Partial tear (n) 4 22 3 29

Full-thickness tear (n) 2 4 25 31

Total (n) 20 31 29 80

2D ultrasonography	Arthroscopic surgery	Total
Tendinopathy (n)	14	5	1	20
Partial tear (n)	4	22	3	29
Full-thickness tear (n)	2	4	25	31
Total (n)	20	31	29	80

Table 2

Diagnostic efficacy of two-dimensional ultrasound imaging in supraspinatus tendon injury

Group	Sensitivity (%)	Specificity (%)	Accuracy (%)
Tendinopathy	70	90	83
Partial tear	71	86	73
Full-thickness tear	86	88	88

Each patient successfully completed the VTIQ examination of bilateral supraspinatus tendon, which took an average of 20 mins, and the patient did not complain of discomfort during the examination. The color diagram of normal tendon elasticity showed the color of red-yellow, and the VTIQ elastic color diagram of supracondymal tendon injury showed that the tendon became soft, in which the tendinopathy group showed the color of yellow-green, partial tear group showed the color of blue-green, and the full-thickness tear group showed the color of blue-green to complete blue, as shown in Fig. 1.

Fig. 1

(A-D) Two-dimensional ultrasonography of normal supraspinatus tendon, tendinopathy, partial tear and full-layer tear. (E-H) Elasticity graphs of A-D patients were respectively corresponding to the mean SWV of 6.77 m/s, 5.53 m/s, 4.78 m/s and 3.91 m/s, respectively.

In normal control group, the SWV measured by VTIQ of 80 cases of supraspinatus tendon was 6.68±1.05 m/s, that of male normal supraspinatus tendon was 6.83±0.99 m/s, and that of female normal supraspinatus tendon was 6.61±1.08 m/s. There was no significant difference in SWV between different genders (t = 0.849, P > 0.05, P = 0.399). The correlation analysis between SWV and age showed that there was no significant difference in SWV of normal supraspinatus tendon between different ages (r = 0.012, P > 0.05, P = 0.915).

The SWV of 80 supraspinatus tendon tears was 4.59±1.00 m/s, which was lower than that of normal supraspinatus tendon (4.59±1.00 m/s vs. 6.68±1.05 m/s, P < 0.01). Further, the SWV of supraspinatus tendon in different degree of lesion groups were lower than that of the contralateral normal supraspinatus tendon (all P < 0.05). The analysis of variance and pairwise comparison showed that the SWV of supraspinatus tendon among the three groups with different degree of injury was statistically significant (P < 0.001, Table 3). Furthermore, there were statistically significant differences in term of SWV values of affected unilateral between tendinopathy and partial tear groups (5.66±0.97 m/s vs. 4.66±1.00 m/s, P < 0.05), tendinopathy and full-thickness tear groups (5.66±0.97 m/s vs. 3.78±0.55 m/s, P < 0.05), and partial tear and full-thickness tear groups (4.66±1.00 m/s vs. 3.78±0.55 m/s, P < 0.05). In addition, the correlation analysis showed that SWV values were negatively correlated with the grading of tendon tears (P < 0.001), that SWV gradually decreased with the aggravation of the damage degree (Fig. 2).

Table 3

Comparison of SWV values of supraspinatus tendon tear and undamaged tendon at different group

Group	SWV (m/s)		t^#	Z^#	P ^#	F^* (P)	r^* (P)
	Normal contralateral	Affected unilateral
Tendinopathy (n = 20)	6.89±0.93	5.66±0.97	–3.692	–	0.004	42.360 (< 0.001)	–0.756 (< 0.001)
Partial tear (n = 29)	6.57±1.08	4.66±1.00^Δ	–	–4.860	< 0.001
Full-thickness tear (n = 31)	6.66±1.11	3.78±0.55^Δ ★	–14.235	–	< 0.001

^*Comparison among three groups with different lesion degrees in affected side; ^#comparison between the affected side and the healthy side; ^Δcompared with the tendinopathy group, P < 0.05; ^★compared with partial tear group, P < 0.05.

Fig. 2

Plot of SWV as a function of the grading of supraspinalis tendon tears with associated linear regression.

The ROC curves were constructed to determine the optimal cut-off values for SWV in the differentiation of the grading of tendon tears. Therefore, the obtained cutoff values, sensitivity, and specificity were all based upon ROC corresponding to SWV. The results showed using ROC curves, 4.83 m/s was determined as a single cutoff for tendinopathy and partial tear groups, AUCs for SWV mean was 0.892 (95%CI, 0.803–0.950; P < 0.01), sensitivity was 85.00%and specificity was 90.00%; 4.08 m/s was determined as a single cutoff for partial tear and full-thickness tear groups, AUCs for SWV mean was 0.878 (95%CI, 0.768–0.948; P < 0.01), sensitivity was 68.97%and specificity was 93.55%(Table 4, Fig. 3). All the above indicated that the SWV value of supraspinalis tendon has a high application value in determining the grading of supraspinalis tendon tears.

Table 4

Diagnostic performance of VTIQ for predicting grading of supraspinalis tendon tears by ROC cures

Group	AUC (95%CI)	P	Cutoff value (m/s)	Sensitivity (95%CI)	Specificity (95%CI)
Tendinopathy vs. partial tear	0.892 (0.803, 0.950)	< 0.001	4.83	85.00 (73.4, 92.9)	90.00 (68.3, 98.8)
Partial tear vs. full-thickness tear	0.878 (0.768, 0.948)	< 0.001	4.08	68.97 (49.2, 84.7)	93.55 (78.6, 99.2)

Fig. 3

The ROC cures (A) tendinopathy vs. partial tear; (B) partial tear and full-thickness tear.

4 Discussion

The commonly used imaging methods to evaluate rotator cuff tear include X-ray, MRI and ultrasound examination [17]. X-ray examination can indicate tendon calcification and humeral head lesions, but cannot make a judgment on tendon structural damage; MRI has a high accuracy in diagnosing tendon tear, but with long inspection time, high price and many contraindications [18 –20]. Recently, ultrasonic examination has been more and more widely used in the assessment of rotator cuff injury, due to its low price, real-time, dynamic scanning and convenient long-term follow-up, especially for the dynamic examination of shoulder impingement sign, and its diagnostic value has been widely recognized by clinicians [21].

Elmorsy et al. [5] have reported the sensitivity and specificity of 2D ultrasound in the diagnosis of rotator cuff tear were 77%and 82%, respectively, which was similarly to the results of our study. It showed the application value of two-dimensional ultrasound in rotator cuff tear. Both previous literature [5] and this study found that patients with partial tear at the early stage of rotator cuff injury could not be accurately identified by conventional ultrasound due to atypical symptoms and signs, small tendon fractures, and no obvious contrast with the echo of surrounding tissues, resulting in a much lower diagnostic accuracy of partial tear than full-thickness tear (73%vs 88%).

Ultrasound elastography was first proposed by Dr. Ophir in 1991 [22] and currently, it has been widely used an effective imaging modality or tool to evaluate the hardness of biological tissues [23]. Its applications in tendon assessment include achilles tendon, patellar ligament, rotator cuff and hand tendon. After several generations of technological development, the latest ultrasonic elastic imaging technology takes VTIQ as the main highlight, uses acoustic radiation force pulse as the application method, and forms elastic images through measurement and calculation of transverse shear wave velocity, which can qualitatively and quantitatively evaluate tissue hardness [24].

There have been a few studies on the elasticity of supraspinatus tendon tear. Vasishta et al. [25] used ultrasound elastography to measure the tendon strain in 25 patients with supraspinalis tendinopathy and analyzed the correlation between tendon hardness and the grading of MRI tendinopathy. The results showed that the stiffness of supraspinalis tendinopathy decreased and was significantly correlated with the lesion degree shown by MRI (r = –0.508, P = 0.0094). The results of this study also showed that the hardness of supracondymal tendinopathy decreased, which was consistent with the trend reported in the literature [25]. Itoigawa et al. [26] reported 38 cases of supraspinatus tendon full-thickness tear repaired by shoulder arthroscopy, the elastic modulus of supraspinatus muscle measured by SWE was significantly positively correlated with the hardness of tendon muscle junction, especially with the elastic measurement value of posterior deep muscle tissue (r = 0.69, P < 0.01). Krepkin et al. [27] conducted ultrasound elastography and MRI correlation study on 6 patients with full-thickness tear and 2 patients with partial tear of suprarenal tendon, and the results showed that SWV of suprarenal tendon was significantly negatively correlated with the size of tear range (r = –0.79 –0.68, P < 0.05), and the average SWV of injured suprarenal tendon was 9.4±2.6 m/s.

This study showed that SWV was 4.66±1.0 m/s for partial supraspinatus tendon tear and 3.78±0.55 m/s for full-thickness tear, which were all lower than those of normal supraspinatus tendon and tenopathy that was consistent with previous studies. However, the SWV measured was smaller than that of previous studies, which might be due to the exclusion of patients with supraspinatus tendon tear caused by calcified tendinitis when selecting the enrolled personnel, one reason was that the SWV measured was too large because of calcification. In addition, through comparison between groups, it was concluded that with the aggravation of the injury degree, the elasticity value gradually decreased, showing the role of VTIQ in evaluating the degree of supraspinatus tendon injury. Furthermore, the ROC curve showed that the best cut-off value of SWV measured by VTIQ technology to judge supraspinatus tendon tear was 4.83 m/s, and the best boundary value to judge full-thickness supraspinatus tendon tear was 4.08 m/s. The area under the curve, sensitivity and specificity were at a high level, which provided an objective reference value for ultrasonic examination to evaluate the degree of supraspinatus tendon tear, which was conducive to clinical more accurate to judge the condition, choose the operation method and judge the prognosis.

However, there were some limitations in this study. First, the sample size was relatively small, with evaluations made at a single institution. Second, the research object was a single tendon, without a comprehensive evaluation of other rotator cuff tendons and muscles. Third, due to the different positions, scanning sites and directions and the characteristics of tendon anisotropy, there might be measurement errors. Therefore, the supraspinatus tendon long axis section was adopted in this study to reduce the existence of such errors.

5 Conclusion

VTIQ, as an effective auxiliary diagnostic method to assess supraspinatus tendon tear pre-operation, could be used to identify the degree of injury by measuring SWV, improving the value of ultrasonography. The usefulness and added value of the VTIQ for evaluating the degree of supraspinatus tendon tear should be further evaluated in large multicenter studies.

Conflict of interest

The authors declare that they have no conflict of interest.

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