Vol:.(1234567890)

Knee Surgery, Sports Traumatology, Arthroscopy (2018) 26:2080–2087https://doi.org/10.1007/s00167-017-4791-4

1 3

ANKLE

Achilles tendon elastic properties remain decreased in long term after rupture

B. Frankewycz1,3 · A. Penz1 · J. Weber1 · N. P. da Silva2 · F. Freimoser1 · R. Bell3 · M. Nerlich1 · E. M. Jung2 · D. Docheva1 · C. G. Pfeifer1

Received: 9 May 2017 / Accepted: 6 November 2017 / Published online: 16 November 2017 © European Society of Sports Traumatology, Knee Surgery, Arthroscopy (ESSKA) 2017

AbstractPurpose Rupture of the Achilles tendon results in inferior scar tissue formation. Elastography allows a feasible in vivo investigation of biomechanical properties of the Achilles tendon. The purpose of this study is to investigate the biomechani-cal properties of healed Achilles tendons in the long term.Materials and methods Patients who suffered from Achilles tendon rupture were recruited foran elastographic evaluation. Unilateral Achilles tendon ruptures were included and scanned in the mid-substance and calcaneal insertion at least 2 years after rupture using shear wave elastography. Results were compared to patients’ contralateral non-injured Achilles tendons and additionally to a healthy population. Descriptive statistics, reliability analysis, and correlation analysis with clinical scores were performed.Results Forty-one patients were included in the study with a mean follow-up-time of 74 ± 30; [26–138] months after rupture. Significant differences were identified in shear wave elastography in the mid-substance of healed tendons (shear wave veloc-ity 1.2 ±1.5 m/s) compared to both control groups [2.5 ±1.5 m/s (p < 0.01) and 2.8 ±1.6 m/s (p < 0.0001) contralateral and healthy population, respectively]. There was no correlation between the measurements and the clinical outcome.Conclusions This study shows that the healed Achilles tendon after rupture has inferior elastic properties even after a long-term healing phase. Differences in elastic properties after rupture mainly originate from the mid-substance of the Achilles tendon, in which most of the ruptures occur. Elastographic results do not correspond with subjective perception. Clinically, sonoelastographical measurements of biomechanical properties can be useful to provide objective insights in tendon recovery.

Keywords Achilles tendon · Achilles tendon rupture · Shear wave elastography · Elasticproperties · Biomechanical properties · Tendon biomechanics

* B. Frankewycz borys.frankewycz@ukr.de

A. Penz andrea.penz@stud.uni-regensburg.de

J. Weber johannes1.weber@ukr.de

N. P. da Silva natascha.platz-batista-da-silva@ukr.de

F. Freimoser florian.freimoser@ukr.de

R. Bell rb622@cornell.edu

M. Nerlich michael.nerlich@ukr.de

E. M. Jung ernst-michael.jung@ukr.de

D. Docheva denitsa.docheva@ukr.de

C. G. Pfeifer christian.pfeifer@ukr.de

1 Department of Trauma Surgery and Laboratory of Experimental Trauma Surgery, Regensburg University Medical Center, Franz-Josef-Strauß-Allee 11, 93053 Regensburg, Germany

2 Department of Radiology, Regensburg University Medical Center, Franz-Josef-Strauß-Allee 11, 93053 Regensburg, Germany

3 Sibley School of Mechanical and Aerospace Engineering, Cornell University, 341 Upson Hall, Ithaca, NY 14853, USA

2081Knee Surgery, Sports Traumatology, Arthroscopy (2018) 26:2080–2087

1 3

Introduction

The Achilles tendon (AT) is one of the most frequently rup-tured tendons in the human body with an increasing inci-dence [1]. Ruptured tendons heal if the tendon stumps have a significant amount of contact, but the healing results in scar tissue formation [2]. During the healing process, bio-mechanical properties are weakened and loading too early, especially in younger and active patients [3], can lead to re-rupture. Inferior properties of healed tendons most likely result from mechanical adhesions, changes in structural components, and scar tissue [4]. Information about biome-chanical properties and the correlation with the clinical and subjective outcomes of healed tendons in vivo is lacking. While biomechanical tests with excised tendon samples allow for more precise description of tendon elastic proper-ties, the feasibility is limited to ex vivo research or animal models. A combination of utilization of dynamometers and strain mapping with B-mode ultrasound allows the calcula-tion of biomechanical parameters of ATs in vivo (stiffness, Young’s modulus and hysteresis) [5]. However, settings in these methods are dependent on muscle force of both gas-trocnemius and soleus muscles, so the calculated values can be biased as they refer to the muscle–tendon complex and not the tendon only [5, 6].

Ultrasound elastography allows visualization of elastic properties in vivo. With the use of Acoustic Radiation Force Impulses (ARFI), shear waves can be created perpendicu-lar to the ARF impulse and their velocity can be measured by the same transducer. Shear wave velocity (SWV) is pro-portional to Young’s modulus of the scanned tissue, and therefore, it can be utilized for quantification of the elastic properties of the tissue of interest [7, 8]. While well estab-lished in other fields, especially in liver diagnostics [9, 10], Shear Wave Elastography (SWE) has begun to gain accept-ance for musculoskeletal diagnostics. With this technique, several studies investigated the AT and its biomechanical properties in dependence of the ankle position [11, 12], dif-ferences in anatomical regions of the tendon [12] and in a fresh rupture situation [13]. However, no data exist on long-term biomechanical changes of formerly ruptured ATs as evaluated by SWE.

The purpose of this study was to investigate long-term elastic properties of healed tendons in patients who suffered from AT rupture (ATR). In particular, the goal was to iden-tify any biomechanical changes in the restored tendon after the healing process was fully completed. It was hypothesized that (i) ruptured ATs, which have completed therapy with a successful union of the stumps, have persistently decreased elastic properties due to scar tissue healing. Furthermore, the goal of this study was to evaluate the diagnostic value of elastography, and the following hypothesis has been

proposed (ii): the elastographically measured values cor-relate with the clinical outcome.

Materials and methods

The database of University Hospital Regensburg was ret-rospectively searched for patients who underwent therapy for ATR between 2004 and 2014. Inclusion criteria were operative or non-operative treatment, at least 18 years of age at the time of injury and regular follow-up visits dur-ing treatment. To focus on comparable long-term results, only patients with a minimum period of 24 months between injury and examination were included. Exclusion criteria were arthrodesis of one of the upper ankle joints, contralat-eral Achilles tendon rupture in the history, neuropathic or malignant diseases, diseases or circumstances that prohib-ited full weight bearing or mobilization 6 weeks after trauma and incomplete documentation during the first 3 months of treatment. After image acquisition, ARFI images were evaluated by a second independent reviewer for validity of the measurements. Measurements were endorsed when the boarders of the tendon were clearly visible throughout the whole length of the tendon and the region of interest (ROI) was explicitly placed within these visible boarders. Whenever the ROI overlapped with tissue outside the ten-don, the measurement was defined as invalid and excluded. In addition, all patients were excluded from the study when the corresponding contralateral side showed invalid meas-urement series. 41 Patients could be included in the study (34 male and 7 female, see Fig. 1). For hypothesis (i), the formerly ruptured ATs (group R) were compared to the con-tralateral (non-ruptured) tendon (group C). Mean age of the patients at time of examination was 53.2 ± 11.1; (31–77) years, and mean follow-up-time after injury was 74 ± 30; (26–138) months. An additional population of healthy par-ticipants (group H, n = 36), who had no AT in their history, was also investigated (n = 36; 14 male, 22 female; mean age was 23.1 ± 3.5; (20–33)]. Prior to inclusion, both their ATs were evaluated in B-Mode and Doppler ultrasound for abnormalities. All participants provided written, informed consent prior to voluntary participation. For evaluation of the clinical outcome, patients completed two validated AT scores (VISA-A and FAOS) [14, 15] at time of examination.

Data acquisition

Ultrasound scans were performed using an Acuson S2000 machine (Siemens Healthcare GmbH, Erlangen, Germany) with a 4–9 MHz linear transducer (type 9L4). Tendon elas-tic properties were determined using VTTQ mode (SWV in [m/s]). Patients were scanned in prone position with over-hanging foot and a fully extended knee. Since ATR tendon

2082 Knee Surgery, Sports Traumatology, Arthroscopy (2018) 26:2080–2087

1 3

length may change (shortening or lengthening) due to indi-vidual treatment variations, the ankle joint was kept in a neutral, relaxed position to avoid pre-load-bias. Both ATs of all patients were scanned in the distal and mid-substance portions of the tendon (subgroups dist/mid). The distal por-tion was defined as the area very adjacent to the calcaneal bone, and the mid-portion was defined by measuring the distal one-sixth of the distance between the palpable tuber calcanei and popliteal fossa. In both areas, tendon diam-eter and fiber alignment were evaluated in B-mode. In the formerly ruptured tendons, scar tissue was also identified in B-mode. Cross-sectional area (CSA) was measured in the mid-substance of the tendon. For evaluation of tendon elastic properties, five VTTQ measurements were acquired of every area. The predefined ROI was virtually positioned on the middle height of the AT (see Fig. 2). The study was performed after approval of the university’s ethical review committee (University of Regensburg, AZ 15-101-0019).

Statistical analysis

Results of the data are noted as mean ± SD; (range). The Wilcoxon and Mann-Whitney tests were used for the com-parison of the three groups for paired and unpaired groups and subgroups, respectively. Kendall’s τ-b rank correlation coefficient was used to correlate values of distal and mid-substance images to both the VISA-A and FAOS scores. Values of p < 0.05 were considered significant. Reliability (internal consistency) was measured very high (Cronbach’s ∝ > 0.94 for both distal and medial portion in all groups). Based on pilot data, an a priori power analysis showed that 34 specimens would provide 80% power to detect a

significant difference between two matched groups with an effect size of 0.5 and alpha level set to 0.05.

Results

ARFI elastography using VTTQ

All of the examined tendons presented a solid continuity in B-mode ultrasound, showing a healed union of the tendon stumps. Of 41 patients, 21 had been treated operatively (o) and 20 non-operatively (no). There were no differences in elastographic stiffness when comparing o vs. no, neither in the distal, nor in the mid-substance areas [n.s.]; therefore, in further calculations, the two treatment groups were pooled. Mean SWV of all groups are shown in Table 1c. SWV of formerly ruptured tendons (R) were significantly lower com-pared to both the contralateral non-injured (C) and those of the healthy population (H) (Figs. 2, 3). CSA was signifi-cantly increased (p < 0.0001) between both R vs. C, R vs. H and also C vs. H (Table 1a, b). A negative correlation was found between SWV and CSA of the formerly ruptured tendons in the mid-substance (τ-b = − 0.22, p = 0.05), but this was not resembled in the healthy population (τ-b = 0.45 [n.s.]). In addition, a highly significant positive correla-tion was found between the distal and the mid-substance diameters of the ruptured tendons, resembling a permanent structural deformation of the whole tendon after rupture (τ-b = 0.35, p = 0.001). Scar tissue was identified in 25 ten-dons (R), of which 2 were located in the distal part and 23 in the mid-substance of the AT. In numerous cases, the shear wave velocity was incalculable, which was indicated

Fig. 1 Prisma diagram of patient inclusion Database

Achilles tendon ruptures 2004 – 2014

(n=208)

Eligible pa�ents

(n=154)

113 Ineligible pa�ents

5 deceased 45 not able to contact54 declined to par�cipate9 excluded by second reviewer

Included pa�ents

(n=41)

54 Excluded Pa�ents

16 ≤ 24 months a�er injury7 no follow-up within first

within 3 months6 contralateral injury in the past4 avulsion fracture3 malignant diseases18 other exclusion criteria

2083Knee Surgery, Sports Traumatology, Arthroscopy (2018) 26:2080–2087

1 3

Fig. 2 Representative pictures of Achilles tendon  ARFI measure-ments, shear wave velocity (SWV) of ROI given in m/s (green). a, b Uninjured tendon shows parallel alignment of collagen fibers in the distal portion (a) and the mid-substance (b), with SWV values of typ-ically more than 3 m/s. c–f Formerly ruptured tendons. c, d 55-year-old patient, 74 months after rupture: SWV is within normal range at the calcaneal insertion (c) with thickening of the tendon more proxi-mal (yellow arrow), whereas the rupture site expresses low SWV (d).

e In contrast, in this thinned out calcaneal insertion of an 83-year-old patient, the fiber structure is almost dissolved and the combination with a very low SWV suggests a weakening of the whole tendon. f 58-year-old patient, 108  months after rupture: elastography shows typically thickened diameter, scar tissue formation (hyperechoic con-trast), inhomogeneous alignment, and irregular tendon borders (yel-low arrows) as a sign of state after reparation with decreased SWV. CB calcaneal bone, respectively

Table 1 Tendon diameter, cross-sectional area, and shear wave velocity

Tendon diameter (a), cross-sectional area (b), and shear wave velocity measured in Virtual Touch Quan-tification mode (c) of all three groups (formerly ruptured tendons (R), contralateral non-injured (C), and healthy population (H) and subgroups (distal and mid-substance)mid mid-substance, dist distal portion of the AT, respectively† p < 0.0001 for all three groups, compared to each other respectively# Significance levels of SWV shown in Fig. 3

R C H

a) D (mm) Dist 7 ± 2; [4–12]† 6 ± 1; [4–9]† 5 ± 1; [3–6]†

 Mid 11 ± 2; [4-16]† 7 ± 2; [4–13]† 5 ± 1; [3–7]†

b) CSA (mm2) Mid 159 ± 69; [32–311]† 80 ± 32; [42–175]† 46 ± 10;

[23–72]†

c) SWV (m/s) Dist 2.7 ± 2.1; [0.5–7.8]# 3.1 ± 1.9; [0.5–7.2] 3.5 ± 2.0;

[0.5–7.5]#

 Mid 1.2 ± 1.5; [0.5–7.2]# 2.5 ± 1.5; [0.5–6.6] # 2.8 ± 1.6; [0.7–7.3]#

2084 Knee Surgery, Sports Traumatology, Arthroscopy (2018) 26:2080–2087

1 3

by “Vs = X.XX m/s” in the display. However, in most cases, more gel and placing the probe stationary without any move-ments resolved the problem. Yet still, in 33 out of 820 meas-urements, data acquisition was not successful, in most cases due to the very superficial position of the AT. Cronbach’s ∝ was 0.97/0.99 for R, 0.97/0.94 for C, and 0.99/0.95 for H (dist/mid, respectively).

No differences were found between genders, or smokers vs. non-smokers, or between age groups (data not shown). When comparing the two areas of the Achilles tendon, highly significant differences were found between R and C, and R and H in the mid-substance of the tendon (Fig. 3b). No significant differences were found between the contralat-eral healthy side (C) and the healthy individual group (H). VISA-A score was 83 ± 20; (3–100), and FAOS was 89 ± 13; (56–100) for the ruptured tendons of the patients. Correlat-ing SWE results (group R) to the clinical scores, no cor-relation was found [VISA score: τ-b = 0.19 [n.s.] − 0.10 [n.s.]; FAOS score: τ-b = − 0.17 [n.s.] − 0.11 [n.s.] (dist/mid, respectively)].

Discussion

This study shows that formerly ruptured Achilles tendons have long-term diminished elastic properties, compared to their contralateral side. Calculating stiffness with the aid of dynamometers, Bressel et al. found no differences in stiff-ness between the formerly ruptured and the contralateral non-ruptured tendons in the long-term results (1–5 years after rupture) [6]. Since stiffness does not take into account the tendon thickness, this finding could be consistent with our finding of increased thickness for ruptured tendons. Since SWV is evaluated in one designated section (ROI), it is not influenced by the tendons’ thickness. SWV is propor-tional to the shear modulus, which can be calculated to the

Young’s modulus under the assumption of a linear isotropic model [16]. In addition, SWV serves as an indicator of stiff-ness, independently from CSA. To discuss this correlation hereinafter, the measured SWV will be referred to as “elas-tographic stiffness”.

The results showed a highly significant decrease of elasto-graphic stiffness even after a long period of healing. Earlier elastographic studies of ruptured ATs have shown an imme-diate decrease of elastographic stiffness after injury. Chen et al. examined 14 AT sonoelastographically, 12 of them within 24 h after rupture [13]. They have found significantly lower SWE values compared to healthy tendons (p = 0.006). The immediate loss of stiffness after rupture is not surpris-ing due to loss of anatomic continuity of the tendon and sonographic measurements of the posttraumatic hematoma. At later timepoints, the AT is reported to regain its elas-tographic stiffness. Zhang et al. have examined ruptured ATs 12, 24 and 48 weeks after rupture and found a gradual increase of the elastographically measured Young´s modulus [17]. This increase can be explained with the physiological healing process of tendon tissue which occurs in consecu-tive phases [18]. However, these studies did not address the long-term outcome compared to uninjured tendons.

Since tendon healing is a long process, that is accom-panied by long-term structural and metabolic changes and can last for more than 1 year [18, 19], we included patients who suffered Achilles tendon ruptures from a minimum of 24 months prior to investigation. Recently, a similar approach was presented with the utilization of dynamom-eters. Geremia et al. examined 18 patients 2 years after surgical AT repair (electro)physiologically in combination with B-mode ultrasound [20]. They found a significant loss of force, stiffness, stress, and Young’s modulus of formerly ruptured ATs compared to the contralateral uninjured ones. Even though a direct correlation of physiologically and elastographically assessed values cannot be postulated,

Fig. 3 Results of shear wave velocity (SWV) measurements: a SWV of formerly ruptured Achilles tendons (distal and proximal measure-ments combined) is significantly lower than those of the contralateral non-injured AT and of healthy individuals. b Highly significant dif-

ferences were found in the mid-substance of the Achilles tendons. (n = 41 for R/C and 36 for H; — Wilcoxon test, ---- Mann-Whitney test for nonparametric groups; whiskers: 10–90 percentile; p values: * ≤ 0.05; ** ≤ 0.01; *** ≤ 0.0001)

2085Knee Surgery, Sports Traumatology, Arthroscopy (2018) 26:2080–2087

1 3

this study supports our results of decreased biomechanical properties.

In accordance with results from the study of Geremia et  al. [20], we also found the CSA to be significantly increased. A physiological increase of CSA is known in ath-letes, where repetitive micro-traumas and consecutive struc-tural remodelling are suggested to cause tendon thickening [21]. In long-term results after ATR, the CSA is increased, suggesting permanent changes due to undergone repair mechanisms and changes in fibril organization, resulting in scar tissue formation [20]. The significantly bigger CSA in the contralateral healthy tendon (C) compared to the healthy control group (H) is most likely due to the younger age of the control group, and it might indicate an asymptomatic pathol-ogy in the contralateral tendon. Bleakney et al. have found differences in the contralateral healthy tendon and healthy tendons of matched patients, suggesting that patients with a ruptured tendon have a tendinopathic predisposition for rupture [22]. However, from our elastography results, this finding cannot be concluded, since there were no substantial differences between C and H in SWE.

According to the literature, the contralateral tendon has a higher risk of rupture; therefore, we also compared the formerly ruptured tendons to those of healthy individuals [23]. The highest differences of SWV were found in the mid-substance of the tendon. A combination of the lowest blood supply in this area, with the bradytrophic character of tendon tissue, the mid-substance of the AT, appears to have inferior resilience and reparation capacity compared to more proximal and distal portions [24]. This makes this area not only prone for rupture [25, 26], but may also con-tribute to an inferior healing capacity after rupture, result-ing in a significant loss of biomechanical properties. After injury, tendon healing results in scar tissue formation. The microstructure of healed tendon and ligament tissue shows an altered collagen composition [27] and fibril diameters [28], which may contribute to the change in biomechanical properties. A similar significant loss of stiffness has been shown in tendinopathically altered tendons in both physi-ological [29] and SWE elastographical [30] studies. In tendi-nopathy, the loss of collagen fiber integrity, changes in struc-tural components, and water content are discussed as cause [29, 30]. Change in matrix components significantly affects biomechanical properties of tendons, but to correlate more detailed mechanisms of structural organization and organic elastic properties, further studies are required.

The ROI of 5 mm height in some cases exceeded the thickness of the tendons, particularly those of healthy and young patients. This certainly resembles a limitation of the used technique. Like other authors [19, 21], we experienced an invalid gauging in a considerable amount of measuring procedures. According to the manufacturer, this occurs when (a) the value is beyond the measuring range or (b) that the

software was not able to gather enough information to com-pute the SWV. The variety of SWE technologies and manu-facturer specific modifications do not allow a comparison of SWV results expressed in [m/s] [16, 31]. Moreover, differ-ent measuring methods and measuring units complicate the direct comparison of SWE result outcomes. For example, Ruan et al., using the same method as ours, have shown that tendon elastographic stiffness increases with both age and tension [8]. Their study investigated SWV in four different age groups in a relaxed and tense state, also using VTTQ mode under the same conditions. The range of values for their young healthy population corresponds to our results for the young and healthy population [2.5 ± 0.9; (0.7–3.4) vs. 2.8 ± 1.6; (0.7–7.3)]. In contrast, Fu et al. showed no differences in age, using the same manufacturer and same conditions as ours (9L4 linear transducer, mid-substance of the tendon, relaxed tendon, and no standoff) but a different technique (Virtual Touch IQ, Siemens Acuson 3000) [32]. These differences highlight the technique-dependent varia-tions of SWE.

In the clinical context, no significant differences were found between non-operatively and operatively treated ten-dons regarding SWV results. This is not unexpected, since no long-term biomechanical advantages of one of the two options had been shown so far in other correlated studies [6]. The clinical scores of our study population had a wider range compared to other studies, resembling a broad variety of the outcome. Nevertheless, no correlations were found between SWE and both clinical scores. To our knowledge, there is no validated ATR score; therefore, we used two common scores that are designed for Achilles tendinopathy (VISA-A) and a variety of foot and ankle-related problems (FAOS). Both focus on the clinical aspects (e.g., pain, symptoms, function, sport- and quality-of-life-related abilities); thus, they are not necessarily associated with biomechanical properties. In addition, clinical scores are subjective and do not address the quality of the tendon. In the context of our study, the question of clinical relevance of SWE directs into the post-operative biomechanical monitoring rather than evaluation of treatment outcome. Sufficient biomechanical properties are crucial for unobstructed function and provide a basis for resilience for future loads and performances, especially in active patients and athletes. The rather stiff properties of healthy tendons are important for responsiveness and also correlate with the ultimate stress failure [33]. Since all our healthy tendons (C + N) had higher elastographic stiffness, future ATR treatment should be directed to regain this range of stiffness. Tendon fatigue, atrophy, adhesions, and the risk of re-rupture are typical complications [34]. To focus and prevent these post-rupture complications, the non-invasive SWE technology might be a promising diagnostic tool. Especially, in young and active patients, who often tend to recover more aggressively, an overuse of the still weakened

2086 Knee Surgery, Sports Traumatology, Arthroscopy (2018) 26:2080–2087

1 3

tendon could be prevented and minimize the risk of re-rupture. As tendon tissue heals very slowly and results in scar tissue formation (not gaining its original properties), monitoring of tendon healing remains a clinical challenge. Therefore, more longitudinal studies, especially during the healing phases, are necessary to correlate SWE findings with biomechanically relevant and histological parameters.

A major limitation of the study was that the elastographi-cally measured values were not correlated with biomechani-cal ones from dynamometric gauges. In general, a high number of patients refused to participate, which is often the challenge in clinical studies, especially so long after treat-ment. In comparison, Geremia et al. recruited 18 patients for a study 2 years after their hospital visit [20]. In spite of the small sample group of 41 patients in our study, strong significances were found between our study groups which support our hypothesis. Another limitation is that the exami-nation was performed by one examiner only. However, an advantage of the SWE compared to strain elastography and other evaluation methods is the examiner-friendly applica-tion and a high examiner-independency [35]. The small ROI of 5 × 6 mm is a limitation of the technology we used. In that case, interfering structures (e.g., cysts, adjacent, or irregular peritendineum) may influence the measuring process. For this reason, a second independent reviewer was called to exclude all invalid measurements. As discussed above, the utilization of clinical scores is certainly a limitation. Clinical scores mostly resemble the individual subjective impression of the patient and are inferior to objective physical measure-ment methods.

Clinically, using non-invasive sonoelastography allows measurements of biomechanical properties of Achilles tendons that will be useful to provide objective insights in tendon recovery. This may be especially useful in advising patients and athletes whether or not to return to sports activi-ties or in guiding long-term rehabilitation programs.

Conclusion

In conclusion, this study was aimed to determine changes in biomechanical properties of formerly ruptured Achilles ten-dons (i). It revealed that the AT has inferior elastic properties even after long-term healing. The differences in elastic prop-erties after rupture mostly originate from the mid-substance of the AT, in which most of the ruptures occur. A correlation of elastographical and subjective clinical outcome could not be proven (ii).

Compliance with ethical standards

Conflict of interest The authors declare that there is no competing in-terest.

Ethical approval The study was performed after approval of the uni-versity’s ethical review committee (University of Regensburg, AZ 15-101-0019).

Informed consent Informed consent was obtained from all individual participants included in the study.

References

1. Ganestam A, Kallemose T, Troelsen A, Barfod KW (2016) Increasing incidence of acute Achilles tendon rupture and a noticeable decline in surgical treatment from 1994 to 2013. A nationwide registry study of 33,160 patients. Knee Surg Sports Traumatol Arthrosc 24:3730–3737

2. Wang JH-C (2006) Mechanobiology of tendon. J Biomech 39:1563–1582

3. Rettig AC, Liotta FJ, Klootwyk TE, Porter DA, Mieling P (2005) Potential risk of rerupture in primary Achilles tendon repair in ath-letes younger than 30 years of age. Am J Sports Med 33:119–123

4. Palmes D, Spiegel HU, Schneider TO, Langer M, Stratmann U, Budny T, Probst A (2002) Achilles tendon healing: long-term biomechanical effects of postoperative mobilization and immo-bilization in a new mouse model. J Orthop Res 20:939–946

5. Maganaris CN, Narici MV, Maffulli N (2008) Biomechanics of the Achilles tendon. Disabil Rehabil 30:1542–1547

6. Bressel E, McNair PJ (2001) Biomechanical behavior of the plan-tar flexor muscle-tendon unit after an Achilles tendon rupture. Am J Sports Med 29:321–326

7. Attia D, Schoenemeier B, Rodt T, Negm AA, Lenzen H, Lankisch TO, Manns M, Gebel M, Potthoff A (2015) Evaluation of liver and spleen stiffness with Acoustic radiation force impulse quan-tification elastography for diagnosing clinically significant portal hypertension. Ultraschall Med 36:603–610

8. Ruan Z, Zhao B, Qi H, Zhang Y, Zhang F, Wu M, Shao G (2015) Elasticity of healthy Achilles tendon decreases with the increase of age as determined by acoustic radiation force impulse imaging. Int J Clin Exp Med 8:1043–1050

9. Nierhoff J, Chávez Ortiz AA, Herrmann E, Zeuzem S, Friedrich-Rust M (2013) The efficiency of acoustic radiation force impulse imaging for the staging of liver fibrosis: a meta-analysis. Eur Radiol 23:3040–3053

10. Thiele M, Madsen BS, Procopet B, Hansen JF, Møller LMS, Detlefsen S, Berzigotti A, Krag A (2016) Reliability criteria for liver stiffness measurements with real-time 2D shear wave elas-tography in different clinical scenarios of chronic liver disease. Ultraschall Med. https://doi.org/10.1055/s-0042-108431

11. Aubry S, Risson J-R, Kastler A, Barbier-Brion B, Siliman G, Runge M, Kastler B (2013) Biomechanical properties of the calca-neal tendon in vivo assessed by transient shear wave elastography. Skeletal Radiol 42:1143–1150

12. DeWall RJ, Slane LC, Lee KS, Thelen DG (2014) Spatial variations in Achilles tendon shear wave speed. J Biomech 47:2685–2692

13. Chen X-M, Cui L-G, He P, Shen W-W, Qian Y-J, Wang J-R (2013) Shear wave elastographic characterization of normal and torn achilles tendons: a pilot study. J Ultrasound Med 32:449–455

14. van Bergen CJA, Sierevelt IN, Hoogervorst P, Waizy H, van Dijk CN, Becher C (2014) Translation and validation of the German version of the foot and ankle outcome score. Arch Orthop Trauma Surg 134:897–901

15. Lohrer H, Nauck T (2009) Cross-cultural adaptation and valida-tion of the VISA-A questionnaire for German-speaking Achilles tendinopathy patients. BMC Musculoskelet Disord 10:134–142

2087Knee Surgery, Sports Traumatology, Arthroscopy (2018) 26:2080–2087

1 3

16. Bamber J, Cosgrove D, Dietrich CF, Fromageau J, Bojunga J, Calliada F, Cantisani V, Correas J-M, D’Onofrio M, Drakonaki EE, Fink M, Friedrich-Rust M, Gilja OH, Havre RF, Jenssen C, Klauser AS, Ohlinger R, Saftoiu A, Schaefer F, Sporea I, Piscaglia F (2013) EFSUMB guidelines and recommendations on the clini-cal use of ultrasound elastography. Part 1: basic principles and technology. Ultraschall Med 34:169–184

17. Zhang L, Wan W, Wang Y, Jiao Z, Zhang L, Luo Y, Tang P (2016) Evaluation of elastic stiffness in healing Achilles tendon after sur-gical repair of a tendon rupture using in vivo ultrasound shear wave elastography. Med Sci Monit 22:1186–1191

18. Docheva D, Müller SA, Majewski M, Evans CH (2015) Biologics for tendon repair. Adv Drug Deliv Rev 84:222–239

19. Eliasson P, Couppé C, Lonsdale M, Svensson RB, Neergaard C, Kjær M, Friberg L, Magnusson SP (2016) Ruptured human Achil-les tendon has elevated metabolic activity up to 1 year after repair. Eur J Nucl Med Mol Imaging 43:1868–1877

20. Geremia JM, Bobbert MF, Casa Nova M, Ott RD, Lemos F, de A, Lupion, R de O, Frasson, Vaz VB MA (2015) The structural and mechanical properties of the Achilles tendon 2 years after surgical repair. Clin Biomech 30:485–492

21. Ying M, Yeung E, Li B, Li W, Lui M, Tsoi C-W (2003) Sono-graphic evaluation of the size of Achilles tendon: the effect of exercise and dominance of the ankle. Ultrasound Med Biol 29:637–642

22. Bleakney RR, Tallon C, Wong JK, Lim KP, Maffulli N (2002) Long-term ultrasonographic features of the Achilles tendon after rupture. Clin J Sport Med 12:273–278

23. Raikin SM, Garras DN, Krapchev PV (2013) Achilles tendon injuries in a United States population. Foot Ankle Int 34:475–480

24. Chen TM, Rozen WM, Pan W, Ashton MW, Richardson MD, Taylor GI (2009) The arterial anatomy of the Achilles tendon: anatomical study and clinical implications. Clin Anat 22:377–385

25. Longo UG, Ronga M, Maffulli N (2009) Acute ruptures of the achilles tendon. Sports Med Arthrosc Rev 17:127–138

26. Pedowitz D, Kirwan G (2013) Achilles tendon ruptures. Curr Rev Musculoskelet Med 6:285–293

27. Williams I, Heaton A, McCullagh K (1980) Cell morphology and collagen types in equine tendon scar. Res Vet Sci 28:302–310

28. Frank C, McDonald D, Shrive N (1997) Collagen fibril diameters in the rabbit medial collateral ligament scar: a longer term assess-ment. Connect Tissue Res 36:261–269

29. Arya S, Kulig K (2010) Tendinopathy alters mechanical and mate-rial properties of the Achilles tendon. J Appl Physiol 108:670–675

30. Aubry S, Nueffer J-P, Tanter M, Becce F, Vidal C, Michel F (2015) Viscoelasticity in Achilles tendonopathy: quantitative assessment by using real-time shear-wave elastography. Radiol-ogy 274:821–829

31. Dillman JR, Chen S, Davenport MS, Zhao H, Urban MW, Song P, Watcharotone K, Carson PL (2015) Superficial ultrasound shear wave speed measurements in soft and hard elasticity phantoms: repeatability and reproducibility using two ultrasound systems. Pediatr Radiol 45:376–385

32. Fu S, Cui L, He X, Sun Y (2016) Elastic characteristics of the normal achilles tendon assessed by virtual touch imaging quanti-fication shear wave elastography. J Ultrasound Med 35:1881–1887

33. LaCroix AS, Duenwald-Kuehl SE, Lakes RS, Vanderby R (2013) Relationship between tendon stiffness and failure: a metaanalysis. J Appl Physiol 115:43–51

34. Mark-Christensen T, Troelsen A, Kallemose T, Barfod KW (2016) Functional rehabilitation of patients with acute Achilles tendon rupture: a meta-analysis of current evidence. Knee Surg Sports Traumatol Arthrosc 24:1852–1859

35. Wu C-H, Chen W-S, Park G-Y, Wang T-G, Lew HL (2012) Mus-culoskeletal sonoelastography: a focused review of its diagnostic applications for evaluating tendons and fascia. J Med Ultrasound 20:79–86