Introduction Tendon structure in mid-portion Achilles tendinopathy (mid-AT) appears poorly associated with symptoms. Yet, degenerative tendon changes on imaging have been associated with an increased risk of mid-AT. We aimed to investigate the prognostic value of ultrasound tissue characterisation (UTC) for a mid-AT recurrence in service members reporting to be recovered following standard care.
Methods Mid-portion aligned fibrillar structure was quantified post-treatment in 37 participants. Recurrences were determined after 1 year of follow-up, based on self-perceived recurrence (yes/no) combined with a decrease in post-treatment Victorian Institute of Sports Assessment–Achilles score of at least the minimal important change of 7 points. Receiver operating characteristic curve analyses were used to determine a threshold for dichotomisation of outcomes for aligned fibrillar structure (normal representation/under-representation). Using multivariable logistic regression, the association between a mid-AT recurrence (yes/no) and the dichotomised aligned fibrillar structure was determined.
Results Eight participants (22%) experienced a recurrence. The threshold for aligned fibrillar structure was set at 73.2% (95% CI: 69.4% to 77.8%) according to Youden’s index. Values below this threshold were significantly associated with a mid-AT recurrence (odds ratio (OR) 9.7, 95% CI: 1.007 to 93.185). The OR for a mid-AT recurrence was 1.1 (95% CI: 1.002 to 1.150) for each additional month of symptom duration. The explained variance of our multivariable logistic regression model was 0.423; symptom duration appeared to be a better predictor than aligned fibrillar structure.
Conclusions This study identified mid-portion aligned fibrillar structure and symptom duration as potential prognostic factors for a mid-AT recurrence in military service members. The threshold for aligned fibrillar structure of 73.2% can guide preventative interventions (eg, training load adjustments or additional tendon load programmes) aiming to improve tendon structure to minimise the future recurrence risk.
Trial registration number https://www.toetsingonline.nl/to/ccmo_search.nsf/Searchform?OpenForm, file number ToetsingOnline NL69527.028.19
- SPORTS MEDICINE
- Foot & ankle
Data availability statement
Data are available upon reasonable request. The data supporting the findings of this study are available from the corresponding author upon reasonable request.
This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
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WHAT IS ALREADY KNOWN ON THIS TOPIC
Degenerative Achilles tendon changes on imaging have been associated with an increased risk of mid-portion Achilles tendinopathy (mid-AT).
WHAT THIS STUDY ADDS
An under-representation of aligned fibrillar structure in the Achilles tendon mid-portion as quantified with ultrasound tissue characterisation, that is, below a threshold of 73.2%, significantly increases the risk of a mid-AT recurrence (OR 9.7, 95% CI: 1.007 to 93.185) in military personnel.
Every additional month of symptom duration increases the risk of a mid-AT recurrence (OR 1.1, 95% CI: 1.002 to 1.150) in military personnel.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY
Mid-portion aligned fibrillar structure and symptom duration can be used to identify individuals at risk of a mid-AT recurrence.
The threshold for aligned fibrillar structure can guide preventative interventions (eg, training load adjustments or additional tendon load programmes) aiming to improve tendon structure to minimise the future recurrence risk.
Mid-portion Achilles tendinopathy (mid-AT) is defined as persistent Achilles tendon (AT) pain, located 2–7 cm proximal to the calcaneus, and with loss of function related to mechanical loading.1 2 This disorder is most common between the ages of 40 and 59 years,3 typically affecting athletes4 and service members.5 6 Mid-AT can be a career-ending injury for professional athletes,4 while in service members, it may have a profound impact on activity levels and military operational readiness.5 6 In professional football, recurrence rates are as high as 27%.4 A prior lower limb tendinopathy is considered to be the strongest risk factor for the development of mid-AT.2 5 7
The treatment of mid-AT is initially conservative, with tendon loading programmes currently representing the best evidence-based practice treatment.2 Not all patients seem to respond adequately to these programmes, since up to half of them report seeking one or more alternative treatments after 5 years of follow-up.8 Although most patients eventually recover,2 still 19% of them experience symptoms after 10 years.9
Histologically, mid-AT is characterised by degenerative changes that may progress as a result of tendon loading,3 10 in rare occasions (4%) leading to a tendon rupture.3 Degenerative tendon pathology can also exist in the absence of symptoms.11 12 The exact pathophysiology and source of nociception of mid-AT are currently unknown.2 10 12
Ultrasound tissue characterisation (UTC) is an imaging modality that can quantify the AT structure into four echo types (I–IV), discriminating aligned fibrillar structure (echo types I+II) from disorganised tendon structure (echo types III+IV).13 Growing evidence indicates that AT structure is poorly associated with self-reported symptoms,14–16 as measured with the Victorian Institute of Sports Assessment–Achilles (VISA-A) Questionnaire.17 Yet, UTC has been found to be able to discriminate symptomatic from asymptomatic ATs, using a threshold for aligned fibrillar structure.13 Taking into account that degenerative AT changes on imaging have been associated with an increased risk of developing mid-AT,18 we hypothesised that UTC may have prognostic value in predicting a mid-AT recurrence. Insight in variables predicting a recurrence may help to identify individuals at risk, and allow for targeted preventive strategies.2 6 Our objective was to determine the validity of UTC as a predictive modality for a mid-AT recurrence, in service members treated successfully with a conservative programme for mid-AT.
Study design and setting
This study was conducted at the Sports Medicine Centre of the Department of Training Medicine and Training Physiology of the Royal Netherlands Army, Utrecht, the Netherlands. Data were collected from January 2020 to July 2022 as part of a larger prospective cohort study (https://www.toetsingonline.nl/to/ccmo_search.nsf/Searchform?OpenForm, file number ToetsingOnline NL69527.028.19).
Consecutive patients referred to the Sports Medicine Centre for AT were eligible for inclusion according to the following criteria: (1) military personnel in active duty (18–60 years), (2) a clinical diagnosis of mid-AT2 and (3) symptoms for at least 2 months. Participants were excluded on the basis of concomitant insertional Achilles tendinopathy or on the presence of factors that may have adversely affected the mid-portion AT structure: (1) signs of a complete AT rupture, (2) prior surgery to the AT, (3) use of statins, fluoroquinolones or corticosteroids,19 and (4) a previous diagnosis of rheumatoid arthritis, diabetes mellitus or psoriasis.19 In case of bilateral symptoms, only the side with the lowest score on the VISA-A Questionnaire was included in the study.
Ultrasound tissue characterisation
We used UTC for the assessment of mid-portion AT structure.13 UTC is an imaging modality that can quantify tendon structure into four echo types: intact and aligned tendon bundles (echo type I); less integer and waving tendon bundles (echo type II); mainly fibrillar matrix (echo type III); and mainly amorphous matrix with loose fibrils, cells or fluid (echo type IV).13 Combined, echo types I+II represent aligned fibrillar structure, whereas echo types III+IV can be seen as disorganised tendon structure (figures 1 and 2). The UTC scans were collected and processed according to a standardised protocol that showed excellent intrarater and inter-rater reliability in the same patient group used for this study.20 Post-treatment UTC scans from our previous study14 were used as baseline measurements for the current study. A single examiner in UTC (MAP) collected these scans. An independent researcher (MM), blinded to the VISA-A scoring, processed all UTC scans to quantify mid-portion tendon structure. The percentage of aligned fibrillar structure in the tendon mid-portion was used as outcome for this study.
At baseline, the following patient characteristics were retrieved: age (years), body mass index (BMI, %), sex (male/female), symptom duration (months), mid-portion echo types I+II (%) and VISA-A.
VISA-A is a validated, disease-specific questionnaire to assess pain, function in daily living and sporting activity.17 Scores range from 0 to 100, where 100 equals a perfect asymptomatic score.
All patients underwent a conservative treatment programme14 and were evaluated directly post-treatment and after 1 year of follow-up. The post-treatment measurements for this study consisted of a written VISA-A Questionnaire followed by a UTC examination.14 20
VISA-A was taken again after 1 year of follow-up, extended with the following additional items: (1) ‘Since the UTC scan was taken, have you experienced AT pain and reduced function (yes/no)?’; (2) ‘Upon yes, for how long were these symptoms present?’; (3) ‘What was the maximum score for pain (NRSmax) (0: no pain, 10: worst conceivable pain)?’; (4) ‘Have you received any additional treatments for your AT?’; (5) ‘Upon yes, which treatments (eg, exercises, medication, surgery)?’.
Recurrence of mid-AT
Post-treatment, all patients were asked if they perceived themselves as recovered and functioning at their pre-symptom activity level (yes/no). Participants answering ‘yes’ were classified as recovered and were included in the current study. Individuals answering ‘no’ were excluded from this study.
A recurrence was determined after 1 year of follow-up post-treatment. We defined a recurrence either as: (1) the presence of AT pain and reduced function due to mid-AT symptoms (yes/no), combined with a decrease in post-treatment VISA-A score of at least the minimal important change (MIC) of 7 points, as assessed for this particular cohort,21 or (2) a self-reported recurrent episode in the past year, from which the participant was recovered at follow-up.
The characteristics of our study population were presented in two groups (mid-AT recurrence yes/no) with appropriate measures of central tendency and dispersion.
We used univariate logistic regression to test if covariates, that is, age, BMI, sex, symptom duration and baseline VISA-A scores, differed between groups.
Subsequently, a receiver operating characteristic (ROC) curve was created for aligned fibrillar structure to distinguish a mid-AT recurrence from a non-recurrence. For this, the post-treatment percentages of aligned fibrillar structure were plotted against mid-AT non-recurrences (coded: 0) and mid-AT recurrences (coded: 1). The area under the curve (AUC) was interpreted as follows: failed, 0.5–0.6; poor, 0.6–0.7; fair, 0.7–0.8; good, 0.8–0.9; and excellent, 0.9–1.0.22 Youden’s index was calculated to maximise sensitivity and specificity, using the formula: (sensitivity+specificity)−1. The optimal cut-off point for aligned fibrillar structure to distinguish a recurrence from a non-recurrence was determined with the Youden’s index value closest to 1. The 95% CI around this cut-off point was calculated.23
Next, outcomes for aligned fibrillar structure were dichotomised using this cut-off point as a threshold. All scores equal to or higher than this threshold were coded ‘0’, indicating a normal representation of aligned fibrillar structure within the AT mid-portion. Scores below this threshold were coded ‘1’, indicating an under-representation of aligned fibrillar structure within the tendon mid-portion.
Logistic regression was used to determine the strength of the potential association with 95% CI between a recurrent episode (0, no; 1, yes) as dependent variable, and the dichotomised aligned fibrillar structure. We considered a multivariable logistic regression model to adjust this association for covariates that statistically differed between groups (p<0.05) at baseline. The Nagelkerke R2 was used to express the proportion of variance of the dependent variable explained by the multivariable model (Nagelkerke, 1991).
Analyses were performed using SPSS (IBM SPSS Statistics for Windows, V.25.0).
A total of 40 participants were treated with the conservative treatment programme, without loss to follow-up. Post-treatment, 37 participants reported recovery and were included in this study (figure 3). Three participants had not yet returned to their pre-symptom activity level and were therefore excluded (figure 3). Baseline characteristics of the participants are reported in table 1.
After 1 year of follow-up, 8 out of 37 participants reported a mid-AT recurrence, with median symptom duration of 15.0 weeks (IQR 43.0 weeks). Mean VISA-A of this group was 94.4 (SD 5.3) post-treatment, and 78.6 (SD 12.3) after 1 year of follow-up. Mean aligned fibrillar structure was 71.2% (SD 13.0). No patients reported additional treatment. In the non-recurrence group, VISA-A was 95.3 (SD 6.4) post-treatment and 98.5 (SD 3.2) after 1 year of follow-up; mean aligned fibrillar structure was 74.2% (SD 13.0).
Seven of these eight individuals reported a recurrent episode combined with a decrease in VISA-A score exceeding the MIC. One subject reported a recurrent episode (NRSmax 8 combined with impaired function for at least 2 weeks) in the past year from which he was fully recovered.
The ROC curve is presented in figure 4. The AUC was interpreted as fair (0.616; 95% CI: 0.393 to 0.840). Youden’s index indicated an optimal cut-off point for aligned fibrillar structure at 73.2% (95% CI: 69.4% to 77.8%), with a sensitivity of 66% and specificity of 75%. Dichotomisation of outcomes for aligned fibrillar structure resulted in 21 participants considered to have a normal representation of aligned fibrillar structure, and 16 participants with an under-representation of aligned fibrillar structure.
Univariate logistic regression indicated that symptom duration was the only variable that significantly differed between groups (p=0.041). Symptom duration was therefore included in our multivariable model. The odds ratio (OR) of the association between mid-AT recurrence and aligned fibrillar structure was 5.7 (95% CI: 0.967 to 33.600), with a Nagelkerke R2 of 0.168. For symptom duration, an OR of 1.1 (95% CI: 1.003 to 1.133) and Nagelkerke R2 of 0.258 were found.
Multivariate logistic regression indicated that the odds for a mid-AT recurrence in a subject with an amount of aligned fibrillar structure below the threshold of 73.2%, compared with a subject with an amount of aligned fibrillar structure of 73.2% and higher, was 9.7 (p=0.049) (OR 9.7, 95% CI: 1.007 to 93.185). The odds for a mid-AT recurrence within the first year was 1.1 (p=0.044) (OR 1.1, 95% CI: 1.002 to 1.150) for each additional month of symptom duration.
The explained variance of the model was 0.423 (Nagelkerke R2), representing the amount of variation of the recurrent episodes that could be explained by the included variables.
The objective of this study was to determine the prognostic value of UTC for a mid-AT recurrence in military service members reporting to be recovered following conservative care. Our results indicate that an under-representation of mid-portion aligned fibrillar structure post-treatment, that is, below a threshold of 73.2%, was significantly associated with a recurrence (OR 9.7, 95% CI: 1.007 to 93.185). Moreover, every additional month of symptoms slightly increased the risk of a mid-AT recurrence within the first year (OR 1.1, 95% CI: 1.002 to 1.150). The explained variance of our multivariable logistic regression model was considerable (Nagelkerke R2=0.423). It should be noted that the explained variance from the univariate logistic regression analysis indicates that symptom duration appeared to be a better predictor than aligned fibrillar structure, with variances of 0.258 and 0.168, respectively.
Clinicians can use the threshold for aligned fibrillar structure to identify individuals at risk after successful conservative treatment, allowing for preventative interventions to improve tendon structure (eg, training load adjustments or complementary tendon loading programmes) to minimise future risk for a recurrence.2 6 To our current knowledge, no study so far has investigated the potential of UTC to predict a mid-AT recurrence.
Various prognostic UTC characteristics of the AT structure have been reported in asymptomatic and symptomatic individuals.6 7 15 16 24 Steinberg et al6 aimed to determine whether baseline mid-portion tendon structure was a risk factor for a wide range of musculoskeletal injuries during an infantry commander’s course. Subjects with echo type III >8.5% (OR 1.69, 95% CI: 1.35 to 2.12) were found to be at highest risk of injury.6 In football players, Docking et al7 investigated whether pre-season AT structure was related to the development of AT symptoms during the season and to symptom severity. Neither tendon AP diameter nor the extent of disorganised tendon structure was found to be predictive for symptom development or symptom severity. In a large cohort of first-year students without a history of AT, Wezenbeek et al24 could not identify echo type II as a risk factor for mid-AT. Due to a marginal representation of disorganised tendon structure in their study, this outcome did not allow for any conclusions concerning increased risk of mid-AT.24 In patients with mid-AT, two studies reported pretreatment aligned fibrillar structure not to be predictive for clinical outcome, as measured with VISA-A.15 16
Although the collection of UTC scans is highly standardised, the processing of these scans to quantify tendon structure allows variation, as UTC operators have the ability to select an anatomical region of interest (ROI) for quantification of tendon structure.13 20 A large variety in selecting ROIs is seen across studies.7 13–15 As UTC echo patterns vary along the anatomical course of the AT,13 20 selecting different ROIs is most likely a source of quantitative variation in UTC echo typing, possibly contributing to different study outcomes when evaluating (prognostic) characteristics of UTC. According to current consensus, mid-AT is defined on the basis of symptom location, that is, symptoms located >2 cm above the superior calcaneal insertion of the AT.2 For reasons of standardisation and uniformity in clinical terminology,25 we adhered to this definition when quantifying mid-portion tendon structure in our study, by selecting a ROI starting 2 cm proximal to the calcaneus, and continuing up to the myotendinous junction or to a length of 7 cm. The first 2 cm of the AT proximal to the calcaneal insertion was not included into our analysis, since this part of the tendon is defined as the AT insertion.2 Although our method for quantifying the AT mid-portion is not applicable to individuals with a free AT ≤2 cm, no such patients were included in our study. Since significantly shorter free ATs have been repeatedly observed in asymptomatic cohorts compared with symptomatic cohorts,26 27 our method may well be limited to tendinopathy populations.
We set the threshold for aligned fibrillar structure at 73.2% (95% CI: 69.4% to 77.8%) according to the Youden’s index value closest to 1, as this value is most accurate in distinguishing individuals with a mid-AT recurrence from those without a recurrence. Van Schie et al13 reported a similar threshold for aligned fibrillar structure (75%) to be most accurate in discriminating symptomatic from asymptomatic ATs. Both our threshold and that of van Schie et al13 are not indicative of normative values of mid-portion aligned fibrillar structure, as studies have reported much higher percentages in asymptomatic populations: 92.5% in military personnel,6 96.3% in freshman students24 and 99.2% in football players.28 In a large cohort study (n=508) investigating normative values for UTC of asymptomatic AT structure, an overall sample percentage for aligned fibrillar structure of 97.3% was reported.29
Strengths and limitations
The present study has several strengths. We used UTC to assess mid-portion AT structure, as conventional greyscale sonography is limited in quantifying intra-tendinous structure, relies largely on the subjective interpretation of ultrasound images and has greater operator dependency, in contrast to UTC.7 Moreover, we quantified mid-portion tendon structure analogous to the generally accepted definition of mid-AT based on symptom location,2 as uniformity in clinical terminology facilitates the communication between clinicians and researchers.25 Finally, in defining a mid-AT recurrence, we used a population-specific VISA-A MIC of 7 points, as recently assessed for this particular cohort.21
With regard to the definition of a mid-AT recurrence, several methodological choices made in the present study have to be taken into account. First, we cannot rule out that individuals defined as recovered in our study experienced a mid-AT recurrence beyond the 1-year follow-up period. Second, one included participant reported a mid-AT recurrence in the past year, from which he was fully recovered at follow-up; we do not know the potential influence of recall bias in this particular case. Third, we considered the combination of both patient perspective (re-occurrence of mid-AT symptoms yes/no) and clinically important decrease in post-treatment VISA-A to establish a mid-AT recurrence, to be a valid reflection of a mid-AT recurrence. If we had chosen to use merely VISA-A, some patients might not have considered a decrease of the MIC to reflect a true recurrence.
This study identified mid-portion aligned fibrillar structure and symptom duration as potential prognostic factors for a mid-AT recurrence in military service members. A threshold for aligned fibrillar structure of 73.2%, as quantified with UTC, can guide preventative interventions aiming to improve tendon structure to minimise the risk of a mid-AT recurrence. Future studies are needed to verify our findings.
Data availability statement
Data are available upon reasonable request. The data supporting the findings of this study are available from the corresponding author upon reasonable request.
Patient consent for publication
This study involves human participants and was approved by Ethics Committee: METC Brabant, Tilburg, the Netherlands (number of approval 1921). All participants provided written informed consent for anonymous use of their data.
Contributors MAP, EB, PH and FB contributed to the conception and design of the study. MAP, MM and EB contributed to the acquisition, analysis and interpretation of data. MAP, PH, EB, FB and MM drafted the manuscript or revised it critically for important intellectual content. MAP is acting as guarantor. All authors read and approved the final manuscript.
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Disclaimer The opinions or assertions contained herein are the private views of the authors and are not to be construed as official or reflecting the views of the Department of Defense or Dutch government.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.