The association between patellar tendon stiffness measured with shear-wave elastography and patellar tendinopathy—a case-control study

Participants were consecutively enrolled. National sports federations and regional healthcare providers facilitated recruitment. Athletes performing sports involving frequent jumping or cutting maneuvers were eligible. Potential subjects underwent initial online screening to assess the location of tenderness on a self-reported pain map [16]. The Victorian Institute of Sports Assessment questionnaire for patellar tendons (VISA-P) was administered to measure symptoms, function, and ability to play sports [17]. A VISA-P < 80 was one of the inclusion criteria for PT [18]. All eligibility criteria are listed in Table 1.

Jumping athletes with suspected PT and asymptomatic athletes were invited to our hospital to confirm eligibility. Clinical evaluation was performed by a sports physician (R.V.) with 10 years’ experience, and athletes were regarded positive for PT if tenderness at the inferior patellar pole or patellar tendon could be reproduced on palpation and a single-leg squat [19]. Provocation tests of the patellofemoral joint were performed to exclude patellofemoral pain [20]. Subsequently, GSUS and power Doppler US (PDUS) were performed to verify the clinical diagnosis. US criteria for PT were presence of structural and/or hypoechoic changes and/or tendon thickening (anterior-posterior diameter > 6 mm) and/or the presence of intratendinous Doppler flow [21]. We defined our reference standard for having PT as a clinical diagnosis with affirmative findings on GSUS and/or PDUS. For athletes with bilateral PT, the individual selected the most painful side. Asymptomatic athletes who had a maximum VISA-P score (100/100) and no history of anterior knee pain or diagnosis of PT were used as controls (Table 1). GSUS and PDUS were acquired, but findings were not an eligibility criterion in this group. Weight and height measures were used to calculate body mass index (kg/m²). Activity level was assessed using the Cincinnati Sports Activity Scale (CSAS) [22].

US was performed by one trained examiner (S.B.: radiologist-in-training with 5 years’ experience) using an ultrasound machine equipped with SWE (LOGIQ E9, GE Healthcare). A linear 5–15-MHz transducer (ML6-15, GE Healthcare) was used for GSUS and PDUS and a linear 3.1–10-MHz transducer (9L, GE Healthcare) for SWE. Ultrasound gel (Sonogel Vertriebs GmbH) was used at room temperature (21 °C).

Participants were examined in supine position with the back rest of the examination table upright in 60° for patient comfort and improved patellar tendon relaxation. GSUS was performed with both knees in 30° flexion, supported by a foam roll. PDUS and SWE were performed in passive extension of both knees. The standardized US acquisition protocol included longitudinal and transverse GSUS of the patellar tendon and transverse cine-loops for PDUS. The patellar tendon was designated as vascular if it demonstrated one or more blood vessels in the posterior portion of the patellar tendon or within the tendon. SWE was performed with mild pressure, in the longitudinal plane with the inferior patellar pole just in the field-of-view. Elastograms were generated in dual-screen mode, displaying GSUS and the overlaying elastogram. Three elastograms were acquired, of which one was randomly selected for the first analysis directly after the image acquisition. A second analysis of all elastograms in PT athletes was performed by the same examiner (S.B.) after the recruitment of subjects had finished, blinded for the results of the first analysis. The second analysis consisted of stiffness measurements in all three elastograms acquired using the same method as the first analysis. Patellar tendon stiffness was averaged for the three elastograms and the relative variability of these measurements was calculated. The maximum thickness of subcutaneous tissue overlying the proximal patellar tendon was measured on a transverse GSUS image, at a standardized location within 1 cm below the inferior patellar border. A subset of controls was invited consecutively to be re-examined with SWE at the same time point by an independent examiner (A.V.) with 2 years’ experience, who also performed the analyses of these collected images, blinded for the results of the first examiner. Quantitative analysis of patellar tendon stiffness was performed on the ultrasound machine, with maximum transparency of the elastograms to avoid subjective placements of regions-of-interests (ROIs). A reference ruler of 20 mm was set posterior to the patellar tendon, starting 5 mm distal to the inferior patellar pole. This guided placement of circular ROIs and avoided inclusion of artifacts from the patella (Fig. 2). ROIs were not fixed in size or number. Median tendon stiffness (kPa) was calculated for each ROI and overall median stiffness including all ROIs. The separate ROIs were labeled “ROI1-ROI4” from proximal to distal in the proximal patellar tendon.

SPSS software (version 25; IBM Corp.) was used. Normal distribution was tested using Shapiro-Wilk’s test. Median and interquartile range (IQR) were obtained for non-normally distributed data. Between-group differences were assessed with Student’s t test for normally distributed data and Mann-Whitney U test for non-normally distributed data. Analyses included the influence of tendon calcifications on patellar tendon stiffness in specific ROIs. In athletes with unilateral PT, we compared patellar tendon stiffness between the symptomatic and the asymptomatic patellar tendon. Logistic regression analysis was performed to calculate odds ratios (ORs) and 95% confidence intervals (95% CIs). Univariate (unadjusted) and multivariate models adjusted for potential confounders, including age, sex, body mass index, and thickness of subcutaneous tissue, were applied. Determinants with p value < .10 were used in the multivariable model. Interaction terms for age*stiffness and sex*stiffness were added, based on findings in previous research [23, 24]. Multicollinearity was tested using variance inflation factor (VIF), with an acceptable maximum of 2.5. The relative variability of the three SWE measurements was assessed using coefficient-of-variation (CV) and coefficient-of-repeatability (CR). The intraobserver reliability for the analyses of the different elastograms and interobserver reliability for independent SWE acquisitions and analyses were assessed using CV, CR, intraclass correlation coefficient (ICC), and Bland-Altman analysis [25‐27]. An ICC value reflected “poor” (less than 0.5), “moderate” (between 0.5 and 0.75), “good” (between 0.75 and 0.9), and “excellent” (greater than 0.90) [28]. P values < .05 were considered statistically significant.

Participants were consecutively enrolled between January 2017 and June 2019. A total of 313 applications from potentially eligible PT athletes and asymptomatic controls were initially screened, of which 138 participants were invited to our hospital to verify or exclude the diagnosis of PT. Finally, 111 participants remained eligible for inclusion (Fig. 1). Clinical and demographic characteristics of the study population are listed in Table 2. Participants with PT were significantly older, had higher BMI, and consisted of more men than asymptomatic controls. Athletes with PT (n = 76) participated in volleyball (n = 26), soccer (n = 17), basketball (n = 16), korfball (n = 8), track and field (n = 4), field hockey (n = 3), and handball (n = 2) as primary sports. Asymptomatic controls (n = 35) participated in basketball (n = 15), korfball (n = 10), volleyball (n = 9), and track and field (n = 1). No significant differences were found in activity levels between athletes with PT and asymptomatic controls. In PT athletes, the left patellar tendon was the primary site of symptoms in 41 participants (54%) and the right patellar tendon in 35 participants (46%). The diagnosis of PT was unilateral in 44 participants (58%), of which 26 were left-sided. Median duration of symptoms in PT athletes was 104 weeks (IQR, 43–208 weeks).

Stiffness of the proximal patellar tendon was significantly higher in PT athletes (median 74.9 kPa, IQR [56.4–105.4]) than in asymptomatic athletes (median 35.6 kPa, IQR [29.9–43.0]) (p < .001) (Fig. 2). In PT athletes, no significant difference in patellar tendon stiffness was found between primary left-symptomatic athletes and primary right-symptomatic athletes (p = .360). Only in ROI 1, patellar tendon stiffness was significantly higher in PT with tendon calcifications than in PT without calcifications (p = .017). In PT athletes without tendon calcifications, symptomatic tendons were still significantly stiffer than asymptomatic tendons in ROI 1, both on the left (p = .043) and right (p = .005) side, but not in other ROIs. This increased stiffness in ROI 1 was not observed in the asymptomatic tendons (left p = .679 and right p = .396).

For the patellar tendon stiffness assessments in all ROIs, the CV was 5.3% (95% CI 4.0–6.3) and the CR was 6.6 kPa (IQR 3.6–12.1). For analysis in separate ROIs, the CV ranged from 10.8 to 11.8% and the CR ranged from 7.3 to 10.7 kPa.

Patellar tendinopathy was associated with significantly higher patellar tendon stiffness, both in univariate analyses (OR 1.094, 95% CI 1.061–1.128, p < .001) and in adjusted multivariate regression analyses (OR 1.294, 95% CI 1.044–1.605, p = .018). The odds ratios for patellar tendon stiffness are estimated for each kilopascal (kPa). In univariate analysis, 7 determinants were associated with the presence of PT symptoms with a p value < 0.10, and therefore included in the multivariate model (Table 3). The variance inflation factors were well within the acceptable limit (range VIF, 1.25–1.56).

The intraobserver reliability analysis (Table 4) revealed an intraclass correlation coefficient (ICC) of 0.95 (95% CI 0.92–0.97) for the median patellar tendon stiffness using all ROIs between analysis 1 (median stiffness 74.9 kPa [56.4–105.4]) and analysis 2 (median stiffness 69.9 kPa [54.7–100.3]). The coefficient-of-repeatability (CR) and coefficient-of-variation (CV) were 11.9 kPa [5.1–24.9] and 10.3% (95% CI 7.9–12.2), respectively. For the separate ROIs, the ICC ranged from 0.85 to 0.92 and CR (CV) from 13.3 to 20.2 kPa (15.1–19.2%). The mean difference from Bland-Altman analysis (Fig. 3) was 5.6 kPa (95% CI 3.1–8.1, p < .001) and limits of agreement were −15.8 kPa (lower limit) and 26.9 kPa (upper limit).

For the interobserver reproducibility, 56 paired measurements in 28 healthy athletes were used (Table 5). The ICC between examiner 1 (S.B.) and examiner 2 (A.V.) was 0.79 (95% CI 0.65–0.88) and CR (CV) was 18 kPa (21%). The mean difference from Bland-Altman analysis (Fig. 4) was 4.6 kPa (95% CI 1.9–7.2, p < .001) and the limits of agreement were −14.8 kPa (lower limit) and 24.0 kPa (upper limit).