ELASTOGRAPHIC ANALYSIS OF THE SUPRASPINATUS TENDON IN DIFFERENT AGE GROUPS.

OBJECTIVE: To compare the mechanical properties of the supraspinatus tendon in different age groups using Supersonic Shearwave Imaging (SSI) elastography.
METHODS: We evaluated 38 healthy individuals of both genders, 20 being in the range of 20 to 35 years and 18 being over 60 years. The shear modulus of the supraspinatus tendon was measured by SSI elastography, always on the right side. Means between age groups were compared and statistically analyzed using the Shapiro-Wilk normality test followed by the student's t-test and were established as a statistically significant value of p ≤ 0.05.
RESULTS: A statistically significant difference was observed when the mean values of the shear modulus of the supraspinatus tendon of young adults (23.98 ± 9.94 KpA) were compared with those of older adults (17.92 ± 6.17 KpA).
CONCLUSION: We found a difference between the means of the shear modulus measured by the SSI elastography, showing a significant decrease of the shear modulus with the chronological age progression. Level of Evidence III, Diagnostic Studies - Investigating a Diagnostic Test.

INTRODUCTION

Rotator cuff injuries, especially supraspinatus muscle tendon (SP), are among the most prevalent in upper limbs. Its etiology is multifactorial, including degenerative, traumatic and inflammatory causes. ( Yamamoto et al. ( underwent ultrasonography of 1,366 individuals aged between 22 and 87 years (mean age 57.9 years) and observed a high prevalence of rotator cuff injuries, reaching 20.7%. In addition to being very prevalent, such injuries may disable the individuals, because pain intensity can withdrawal they from sports and work activities. ( )- (

The prevalence of rotator cuff disease increases with age. Sher et al.5 underwent magnetic resonance imaging in asymptomatic individuals and found rotator cuff injuries in 4% of patients under 40 years old and in 54% of those aged 60 years or older. ( Tempelhof et al. ( carried out shoulder ultrasonography of 411 asymptomatic volunteers and found a global prevalence of rotator cuff injury of 23%. This study also reported that the prevalence of this injury increased with age, with 13% of the individuals with 50 years or older, 20% in the sixth decade and 31% in the seventh decade. (

Although magnetic resonance imaging is the most widespread imaging method for assessing changes in rotator cuff tendons, elastrography has been shown to be as effective as the first in diagnosis and characterization of these alterations. ( ), ( In a wide-ranging literature review, Washburn et al. ( showed that elastography was used in studies of various structures, including the calcaneus, patellar, quadriciptal and rotator cuff tendons. (

There are two main modalities of elastography: compression (EC) and shear (ES). ES provides noninvasive estimation of tissue mechanical properties. The technique involves a mechanical disturbance in the tissue with an impulse of forces generating a shear wave, visualizing the displacements of tissue and then estimating the speed of the local shear wave (LSW), estimating the “flight time” of this wave. Soft tissue LSW measurements can be interpreted as an indirect evaluation of the shear modulus. (

When compared to isolated ultrasonography, ES potentially increases the sensitivity and diagnostic accuracy of tendinopathies, in addition to detecting pathological changes earlier, enabling the prediction of which tendons are at risk of injury and evaluation of the recommended treatments. (

Objective

This study aims to compare mechanical properties of the supraspinatus tendon in two distinct age groups, using the measurement of the tendon shear modulus by elastography.

MATERIALS AND METHODS

Sample

This study had the ethical guidelines analyzed by the Research Ethics Committee of the Hospital, with approval recorded by The Embodied Opinion No.1,674,064 of August 8, 2016. The volunteers were recruited by convenience sampling and 38 participants were divided into two groups: one of young adults aged between 20 and 35 years (n = 20) and the other for older adults over 60 years of age (n = 18). All subjects agreed to participate in the study signing a free and informed consent form. The groups are clearly distinct from each other. Studies aforementioned show that the prevalence of rotator cuff ruptures is low in under 40 years old individuals and high in those over 60 years of age. This fact was used as criterion for defining age groups.

Anamnesis and physical examination were performed in the candidates, and presenting the right upper limb as dominant was the inclusion criteria. Patients with current or previous shoulder symptoms, those with a history of diseases and/or previous shoulder surgeries, as well as those with known systemic disease were excluded. Patients with ultrasound evidence of supraspinatus rupture were also excluded.

Elastog raphy

For the shear modulus collection, the equipment (Figure 1) Aixplorer, v9 (Supersonic Shearwave Imaging, Aix-in-Provence, France), with Super Linear Transducer TM SL 10-2, width of 40mm, 256 pizoelectric elements, operating in the ranges of 2 to 10 MHz and lateral resolution of -6dB: 0.3mm was used. The participants were placed in the sitting position, with the back of the right hand resting on the lumbar region, to evidence the supraspintus tendon, with the left upper limb extended along the body, hips and knees flexed at 90º and feet supported to the ground (Figure 2). ( The volunteers kept their muscles relaxed throughout the examination.

Figure 1

Ultrasound device with elastrography imaging activation mode. Aixplorer, v9 (Supersonic Shearwave Imaging, Aix-in-Provence, France).

Figure 2

Patient’s exam positioning, sitting, with the back of the right hand resting on the lumbar region.

An experienced radiologist in the acquisition of musculoskeletal ultrasound images acquired the images using the transducer longitudinally to the fibers, adopting minimal compression and gel for the best acoustic coupling (Figure 3). A total of three images were acquired to determine the reliability of the method. ( Before activating the elastography mode, supraspinatus tendon was assessed for its integrity and the best ultrasound image was chosen. Then elastographic mode was activated, with the elastogram in the range of 0-800-kPa. A rectangular, mapping area was selected, demonstrating the tendon boundaries and surrounding structures, positioned in the central region of the tendon (Figure 4). (

Figure 3

Transducer positioned longitudinally to supraspinatus fibers.

Figure 4

Elastographic image of the supraspinatus tendon, measured in kilopascal (kPa).

Image processing was implemented in a MATLAB routine (Mathworks, Massachusetts, USA), to estimate the shear modulus, measured in kilopascal (kPa). In this routine, a circle was manually traced in the mapping area, defining the central region of the tendon as a region of interest. The shear modulus was obtained from each region of interest in each image.

Statistical analysis

Intraclass correlation coefficient (ICC2,1) was applied to evaluate the measurements reliability performed on the same day. The Shapiro-Wilk normality test was performed. After confirming the normality of the shear modulus, Student t-test was performed for independent samples comparing means of both young and older adults groups, as well as for the comparison between women and men. All statistical treatment was performed by the commercial package GraphPad Prism 5.0 (Graphpad software inc., USA) with 5% statistical significance.

RESULTS

ICC2.1 estimation indicated reliable measurements (Table 1). A significant difference was found between the means of the supraspinatus tendon shear modulus of youth groups when compared to the older adults (p = 0.033) (Figure 5). The mean age in the groups of young and older adult was, respectively, 28.05 and 67.9 years. The group of young individuals was composed of four women and 16 men, while the older adults group was composed of 11 women and seven men. There was no significant difference in shear modulus found in women and men (p = 0.891) (Figure 6).

Table 1

Results of the calculation of the intraclass correlation coefficient (ICC) performed using a single rater, absolute agreement and two-way mixed effect model.

Measure	Intraclass correlation coefficient	95% confidence interval		F Test
		Inferior Limit	Superior Limit	Value	P value
Shear Modulus	0.726	0.452	0.863	3.652	<0.001

Figure 5

Mean and standard deviation of the shear modulus of older adults and young individuals (p = 0.033).

Figure 6

Mean and standard deviation of the shear modulus of women and men.

DISCUSSION

This study showed that the supraspinatus tendon shear modulus varies with advancing age. In fact, younger patients, between 20 and 35 years of age, presented a mean shear modulus of 23.28 ± 9.94 kPa, higher than in the group over 60 years of age, which was 17.92 ± 6.17 kPa. Thus, supraspinatus tendon was shown to have a larger, firmer shear modulus among young patients, while in older adults the tendon was less rigid. In fact, with aging, rotator cuff tendons undergo structural changes, such as loss of fibrillar pattern and microruptures, which decreases their compressive strength. ( Consequently, the compression exerted by the transducer will cause greater tissue deformation, which was measured by the smaller tendon shear modulus in the group of individuals over 60 years of age. This finding agrees with previous studies. In a cadaveric study, Klauser et al. ( observed a correlation between histological and sonographic findings of calcaneus tendons. They observed that the progression of tendon degeneration was accompanied by the “softening” of the tendon to elastography. Studies about supraspinatus tendon, such as ours, also revealed that degenerative tendinopathy is associated with greater capacity of tendon deformation during elastographic evaluation. ( )- ( On the other hand, Baumer et al. ( evaluated the influence of age on supraspinatus tendon shear modulus in individuals of different ages and observed that older individuals had stiffer tendons. However, unlike our study, the measurement was carried out in the intra-muscular portion of the tendon, which does not allow the isolated evaluation of the tendon itself, but also involves the muscle belly itself. In a study that correlated elastographic results with magnetic resonance findings, Lee et al.21 also observed greater stiffness in tendons with tendon disease. However, differently from our study, the elastographic technique was based on the stretch ratio (strain ratio), in which the tendon elasticity is measured by taking the elasticity of another tissue as a reference, which may generate less accurate results.

A study with cadavers showed that aging can alter biomechanical properties of the myotendinous unit of the rotator cuff. ( However, the identification of these changes in vivo is not yet well established. Although MRI is the most widely applied method to assess rotator cuff injuries, it is not able to provide accurate information on the mechanical properties of tendons. In this context, elastography can help in the evaluation of such properties. Lee et al., ( ) in 2015, showed that elastographic findings correlate with MRI findings in patients with rotator cuff tendinosis, but they did not include patients with tendon rupture. In 2014, Seo et al., ( compared the results of elastography with those of MRI and ultrasonography, finding a good correlation between methods. In 2017, Krepkin et al., ( conducted a pilot study comparing MRI images obtained on T2 with the findings of shear wave elastography, observing good correlation. In relation to MRI, elastography has some additional advantages. Besides being also a noninvasive method, it is easy to perform, relatively inexpensive and it can be carried out with the patient in a comfortable position, being more easily tolerated by them. Furthermore, elastography proved to be a reproducible method in different studies. ( ), (

The evaluation of the tendon mechanical properties can bring important information and practical implications. Extensive rotator cuff injuries may be irreparable and some prognostic factors are useful to identify these injuries, among which, patient’s age, size of the injury, duration of symptoms, acromion-umeral distance less than seven millimeters, reduction of range of motion, muscle strength equal to or less than grade 3, intraoperative difficulties; surgeon’s experience, patient expectation; atrophy and fatty infiltration of the muscle belly involved. Such factors are not definitive to determine the possibility and feasibility of repairing a given lesion, even when associated, as this information does not directly relate to the elasticity and/or stiffness of the ruptured tendon. Therefore, the estimation of the shear modulus can add information in determining the repair condition of a rotator cuff injury. ( Moreover, some patients may present signs of rotator cuff dysfunction even without having complete injury of one or more tendons. They are patients whose tendons are inserted, but already have some degree of atrophy and fatty infiltration of the muscle belly. These patients may suffer dynamic rise of the umeral head, with secondary subacromial impact and worsening of anatomical tendons conditions. In these cases, by evaluating a mechanical property of the tendon, elastography can also bring valuable information before a tendon rupture occurs. A possible clinical application for this situation would be the preference for reverse to anatomical arthroplasty in a patient with shoulder arthrosis and rotator cuff tendons inserted, although very biomechanically compromised. (

Although there is still a lack of standardization to adequately evaluate the reproducibility of the results, elastography is very promising. Notably, tendons may have different elasticity modules. ( Therefore, it would be necessary multiple studies like this, in a larger population, divided into age groups, so that a value of the shear modulus could be found for each group and thus quantify and qualify the aging of the tendon based on its stiffness.

Negative points and limitations should be highlighted in this study. The heterogeneous gender distribution between groups may have caused some result bias, since, for example, the mean shear modulus, having been lower in older adults, may have been caused by the fact that there were more female individuals in this group. However, the comparison of the shear modulus between men and women did not show significant difference. Another point would be the fact that SSI elastography is a method that measures only the shear modulus in anisotropic tissues, such as tendinous tissue, not contemplating other mechanical properties of the tendon. However, there is an intimate relationship between shear modulus and tissue stiffness, which allows further analysis of this important biomechanical valence with elastographic data.

CONCLUSION

The modulus of supraspinatus tendon shear was significantly higher in young people, suggesting deterioration of biomechanical properties of the tendon in older adults.