MRI of the Achilles tendon—A comprehensive pictorial review. Part one

Highlights • Presence of normal septation between subtendons may mimic an intrasubstance tear.• MRI is superior to ultrasound in detection of partial tears.• Ultrasound is as useful as MRI in detection of tendinopathy and full-thickness tears.• Kager's fat pad is involved in infection more than in postoperative changes.• The Achilles tendon xanthoma has a higher signal on T1- and T2-weighted sequences.

The normal Achilles tendon is composed of twisted subtendons separated by thin high signal septae, which are a potential pitfall on MRI because they mimic a tendon tear.
Tendinopathy and full thickness tears may be assessed effectively both on MRI and ultrasound. MRI is superior to ultrasound in detection of partial tears and for postoperative assessment. The use of fat suppression sequences allows the ability to detect focal lesions. Sagittal and coronal sections are useful for assessing the distance between stumps of a ruptured tendon. Sequences with contrast are indicated in postoperative investigations and suspicion of infection, arthritis or tumor. MRI may reveal inflammatory changes with minor symptoms long before the clinical manifestations of seronegative spondyloarthropathy. The most common non-traumatic focal lesion of the Achilles tendon is Achilles tendon xanthoma, which is manifested by intermediate or slightly higher signal on T1-and T2-weighted images compared to that in the normal Achilles tendon. Other tumors of the Achilles tendon are very rare, whereas the involvement of the tendon from tumor in adjacent structures is more frequent.
The novel MRI sequences may help to detect disorders of the Achilles tendon more specifically before clinical manifestation. Regeneration or remodeling of the Achilles tendon can be non-invasively detected and monitored in diffusion tensor imaging. Assessment of healing is possible using T2-mapping while evaluating the tendon vascularization in intravoxel incoherent motion MRI.

The normal Achilles tendon
The normal Achilles tendon is composed of three twisted subtendons; two from the medial and lateral heads of the gastrocnemius muscle and one from the soleus muscle [1,2]. The anterior outline of the Achilles tendon is mainly composed of a subtendon from the lateral head of the gastrocnemius. The medial part of the Achilles tendon consists of the soleus subtendon, while the posterior outline forms the subtendon from the medial head of the gastrocnemius [1,3]. The signal of the normal Achilles tendon on the PD-and T2-weighted sequence is low, with some thin high signal septae separating the individual subtendons (Fig. 1). The most consistently visualized septae are present in the anterior part of the tendon between the subtendons from the soleus and the lateral head of the gastrocnemius muscle. Normally present septation may be a pitfall on MRI and can be mistaken for a tear [3][4][5] (Fig. 1).
The Achilles tendon is covered by the paratenon, although normally it is not visible on MRI. The plantaris tendon contributes to the medial part of the paratenon in 40 % of patients [6][7][8] (Fig. 2). The paratenon is highly vascularized and thus is important in healing of the Achilles tendon [9]. Microscopically, the paratenon enters between the Achilles tendon fibers as the endotenon, where vessels, nerves, and tenocytes are located [10]. The enthesis of the Achilles tendon is a complex of the following structures accounting for the connection between the Achilles tendon and calcaneus; sesamoid cartilage and fibrocartilage, which are located at the anterior outline of the tendon; periosteal fibrocartilage covering the calcaneus; the retrocalcaneal bursa; and the part of Kager's fat pad that protrudes into the bursa [11][12][13]. The retrocalcaneal bursa is a synovial lined structure occupying the space between the Achilles tendon and calcaneus. The superficial calcaneal bursa is located between skin and the Achilles tendon insertion [1].

MRI vs. ultrasound in the assessment of the Achilles tendon
Ultrasonography is the most commonly used imaging modality for the assessment of the injured or painful tendon. The indications for MRI and ultrasound of the Achilles tendon somewhat overlap; however, a clinical examination is significant (Table 1) [14]. Ultrasound is a cheap and easily accessible modality; however, it is operator dependent, whereas MRI depends on an optimal protocol. Moreover, a different selection of patients for the previous studies makes an unambiguous comparison difficult. At our institution, postoperative changes are assessed by MRI with contrast because of the diversity of possible complications (Table 1). Clinical suspicion of arthritis, infection or tumor should be imaged with IV (intravenous injection) contrast. The degree of bursitis and presence of a tendon lesion within the insertion may also be determined effectively on MRI. Postoperative complications, such as calcaneus fracture, infection and abscess formation, tendon or graft rupture, can be assessed on MRI with contrast. Ultrasound is as good as MRI in detection of tendinopathy and full-thickness tears [15,16]. However clinical findings in tendinopathy correlate more with MRI than with ultrasound [17]. MRI is superior to ultrasound in detection of partial tears [16]. The use of new MRI sequences enables the early identification and differentiation between the types of tendinopathy, which is not possible in ultrasound at all [16]. In the enthesopathies, the degree of bursitis, the presence of tendon changes, and the presence of bone marrow edema in the bony insertion can be determined on MRI. Ultrasound allows dynamic assessment of the Achilles tendon, which is not possible on static MRI unless dynamic sequences are used.  Hypervascularization in the Achilles tendon can be assessed by Doppler ultrasound, in MRI novel sequences or in classical MRI IV contrast.
Ultrasound elastography is used to distinguish the normal tendon from the pathologic tendon, allowing earlier diagnosis and monitoring of remodeling and treatment. However, more studies are required to evaluate the clinical value of this method. MR elastography is a new method used mostly in research (discussed in the section regarding new MRI techniques).
Both ultrasound and MRI are used to assess heel involvement in spondyloarthritis. Erosions at the enthesis may help to differentiate peripheral spondyloarthritis from non-inflammatory lesions [18]. Neither MRI nor ultrasound could differentiate between inflammatory lesions without erosions [18]. However, only MRI showed bone marrow edema, which correlates with the level of HLA-B27 [19]. Thus, differentiation from mechanically induced disease may be performed in doubtful cases. Sequences with fat suppression and contrast enhancement are appropriate methods of visualizing active enthesitis [20].

Protocol
A MR protocol for the Achilles tendon should include sequences in all three orthogonal planes. Fat suppressed imaging with T2-or PDweighted images and at least one T1-weighted sequence for bone marrow evaluation are recommended ( Table 2). Using fat suppression allows to increase the contrast between the free water and collagen fibers.
Sagittal and axial sections are the most useful in evaluation of the Achilles tendon. T2-weighted images are useful due to their high ability to demonstrate the fluid accompanying tendon pathology. The protocols used most often at our institution are provided in Table 2. Sequences with contrast are used in postoperative investigations and suspicion of infection, arthritis or tumor. In other cases, we used protocols without contrast (Table 2).

New MRI techniques
Evaluation of the microscopic properties of the Achilles tendon with conventional MRI sequences is limited because of a very short T2-time. The application of new MRI sequences may help to identify subclinical lesions, enabling to us to differentiate between different sorts of tendinopathies. The novel techniques are based on the alteration of the normal collagen fibers by water, which change local homogenic structures and thus magnetic features of the Achilles tendon.
Modification of classical diffusion tensor imaging (DTI) MRI may reveal tendinopathy-induced microstructural disorganization in the very early stages. The process of regeneration, healing, remodeling and progress or treatment response are possible applications of DTI [31]. Assessment of the microarchitecture of the Achilles tendon after reconstruction with the possibility of the fiber tracing is a possible application of DTI [26,32].
T2-mapping is a promising method to assess tendon healing. The normal tendon has a shorter T2 value compared to that in the injured part of a tendon [33]. The concentration of water is higher after trauma and then decreases with the time, thus the healing process may be quantified using T2-mapping [34]. It may be used clinically as robust biomarker of tendon healing, making for easier decisions regarding the MRImagnetic resonance imaging. Symbols used in the table: ++ the preferred method, + the alternative method, -the method is not used. appropriate time to return to sport [33]. Low vascularization of the Achilles tendon may complicate the process of healing. The development of vascular networks after injury may be crucial for Achilles tendon healing. The microcirculation and microvasculature properties of the Achilles tendon could be assessed using an intravoxel incoherent motion MRI [35].
MR spectroscopy is a promising method for evaluating metabolic activities and biochemical composition. Detecting different signals from different molecules may help to assess the level of water, inorganic phosphate or adenosine triphosphate [36]. This method is used mostly for muscles, and application in tendons is technically challenging because of short T2 time. Ultrashort sequences allow quantitative imaging of water within the Achilles tendon. Direct imaging of water within the tendon may be a favorable way of diagnosing tendon disorders [37].
Pathological tendons exhibit higher levels of glycosaminoglycans, which attract sodium ions. Sodium MRI may help to evaluate the level of sodium in the tissue, allowing indirect evaluation of glycosaminoglycan content within the tendon [38]. Sodium MRI may reveal changes in the Achilles tendon during treatment with ciprofloxacin, while other new sequences, even T2*, show neither tendon lesions nor clinical symptoms are present [39]. Thus, sodium MRI may be applied in the prevention of tendon rupture in asymptomatic patients treated with fluoroquinolones.
MR elastography is used to assess the mechanical properties of a  muscle, mainly in neuromuscular disorders [40], but clinical application to tendons has not been done yet [32].

Infections
Infection of the Achilles tendon and paratenon are rare and often are complications of Achilles tendon repair or reconstruction (Fig. 3), Haglund debridement (Fig. 4), penetrating or non-healed wounds or open lacerations [25,41]. Infection may be difficult to distinguish from postoperative changes, especially in the early stages; however, infection usually causes more extensive and diffuse reactive changes within Kager's fat pad. Administration of IV contrast allows the exclusion of abscess formation (Figs. 3 and 4) [42].
Wounds and surgical incisions in the Achilles tendon area are more prone to infection and wound breakdown compared with other areas of the body because of worse vascularity (Fig. 5). This may be revealed as a thickened tendon and paratenon. Reactive changes are visualized as edema in the subcutaneous tissue and in Kager's fat pad. Following the administration of contrast, diffuse enhancement in the Achilles tendon, the paratenon and Kager's fat pad is seen (Fig. 3). A fistula may form between the skin and an abscess collection, particularly on the posterior aspect of the tendon (Fig. 5).

The Achilles tendon in seronegative arthropathies
Enthesitis is a key sign of spondylarthritis and psoriatic arthritis [11,43]. The perientheseal inflammation may be seen in early peripheral spondylarthritis and can be revealed on MRI as bone marrow edema in the calcaneus, allowing detection of subclinical cases (Fig. 6). The higher signal in the Achilles tendon and subcortical bone marrow edema at the insertion are MRI features and correlate with higher levels of HLA-B27 [19]. Erosions are present in one-third to two-thirds of patients and may help differentiate peripheral spondyloarthritis from other cases [18,44]. Tendon thickening, retrocalcaneal bursitis, edema of Kager's fat pad, erosions, bony irregularities, and enthesophytes of the plantar fascia may be seen on MRI in patients with spondyloarthritis. Hypervascularization of the enthesis may be easily evaluated by Power Doppler examination [45]. For visualization of active enthesitis, MRI sequences with contrast are recommended [20]. Assessing the degree of enthesitis is essential to evaluate disease activity and to monitor   6. A 26-year-old patient with a suspicion of spondylarthritis presenting with discomfort in the insertion of the Achilles tendon. a and c-T2-weighted with fat suppression; b -T2-weighted. MRI revealed retrocalcaneal bursitis (dashed arrow) and bone marrow edema in the Achilles tendon insertion, however no erosions are present. Thickening of the Achilles tendon in midportion is visible (*), however no alteration in the signal of the Achilles tendon was revealed. A-T2-weighted, b-PDweighted, c-PD-weighted with fat suppression. treatment [11,46].
Enthesopathies are pathological changes at the tendon insertion and can also be seen in degeneration, metabolic syndromes, endocrine disorders, and traumatic or mechanical conditions [11].

The Achilles tendon in rheumatoid arthritis
Enthesitis is not a hallmark of rheumatoid arthritis; however, some patients have an altered signal within the midsubstance of the tendon but without the thickening associated with classical tendinopathy [47]. The retrocalcaneal bursa may also have a higher signal, although there may be a paucity of clinical features [47]. Conversely, some patients have tendon thickening without a typical focal intratendinous signal.
Early retrocalcaneal bursitis may be seen because inflammation ascends from the synovial membrane lining the walls of the bursa [48].

Tumors
Tumors are uncommon in the Achilles tendon and "tumor-like" lesions occur more frequently. If a tumor is present, it is often benign. The differential diagnosis of a mass on the Achilles tendon is t tendinopathy, along with lesions such as xanthomas, giant cell tumors or fibromas. Loss of the anterior concavity of the Achilles tendon, a painless soft tissue mass occurring most commonly bilaterally and symmetrical at the distal portion of the Achilles tendon may be seen in Achilles tendon xanthoma [49]. The accumulation of lipid-laden macrophages within the Achilles  tendon results in an intermediate or slightly higher signal on T1-and T2-weighted images compared to those in the normal Achilles tendon [50].
A giant cell tumor is an extra-articular form of pigmented villonodular synovitis. Additionally, diffuse-type tenosynovial giant cell tumors have been reported [51]. MRI reveals an intermediate to low signal on T1-and T2-weighted images.A fibroma of the Achilles tendon is frequently a well-circumscribed mass and most commonly observed in children. MRI demonstrates a lower signal on T1-and T2-weighted images. If contrast is administered, mild heterogeneous enhancement may be seen.If malignant lesions involve the Achilles tendon, it usually occurs by local infiltration or mass effect from the adjacent tumor (e.g., originating from the gastrocnemius) (Fig. 7).
Most tumor-like focal lesions within the Achilles tendon are related to injury and are fluid-filled intrasubstance tears. In rare cases, a ganglion-like lesion may be found with typical features (Fig. 9). Lowprotein ganglions give a high signal on T2-weighted images and a low signal on T1-weighted images without contrast enhancement. Sometimes, multiple ganglia may be present (Fig. 8). Direct trauma to the Achilles tendon may result in a hematoma or seroma located on the tendon's surface at the site of direct injury (Fig. 9).  9. A 33-year-old patient who presents after suffering a direct injury to the Achilles tendon. There was neither rupture nor tendon dysfunction revealed on clinical examination. The posttraumatic focal swelling was understood as a hematoma. After 2 weeks, when the clinically suspected hematoma did not decrease in size, an MRI was performed. The heterogeneous fluid lesion with a higher amount of protein (a) (straight arrow) is located between the paratenon (curved arrow) and Achilles tendon. a -T1-weighted; b -STIR; c -PD-weighted with fat suppression; d -T2-weighted. An ultrasound-guided puncture was performed, and clear serous fluid was aspirated. e -ultrasound correlation is presented (longitudinal sagittal section, t -Achilles tendon).

Summary
The indications for MRI and ultrasound overlap, and there is no clear consensus for the use of imaging diagnostics in the diagnostic of the Achilles tendon. Appropriate MRI protocols and novel MRI sequences may help to differentiate disease entities from similar clinical manifestations. The novel sequences are the future of Achilles tendon imaging because they enable treatment monitoring and early detection of tendinopathy. In infection, it allows assessing the involvement of bone in osteomyelitis. Administration of contrast enables the exclusion of abscess. The higher signal in the Achilles tendon and subcortical bone marrow edema at the insertion are MRI features of seronegative arthropathies. Achilles enthesitis revealed on MRI precedes the onset of systemic disease. MRI helps to differentiate true tumors from tumor-like lesions.

Funding
This project did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Declaration of Competing Interest
The Swedish Ethics Committee approved the study and waived the need for informed consent (2020-06177). This project did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. The authors declare that there is no conflict of interest.