Faiza Sharif ( University Institute of Physical Therapy, University of Lahore, Pakistan )
Ashfaq Ahmad ( University of Lahore, Pakistan )
Syed Amir Gilani ( University of Lahore, Pakistan. )
Raham Bacha ( University Institute of Medical Imaging Technology, University of Lahore, Lahore, Pakistan )
Asif Hanif ( The University of Lahore, Lahore, Pakistan. )
March 2023, Volume 73, Issue 3
Substantiating the predictive role of ultrasound imaging in athletes with lower limb tendinopathy: a systematic review
Faiza Sharif ( University Institute of Physical Therapy, University of Lahore, Pakistan )
Objective: To explore the potential of ultrasound imaging to anticipate and monitor future symptoms of patellar or Achilles’ tendinopathy.
Method: The systematic review comprised prospective studies that used ultrasound imaging of Achilles’ OR patellar tendons in asymptomatic patients at baseline and measurements of pain and/or function at follow-up. The Critical Appraisal Skills Programme checklist used to assess study quality and it was done by two independent reviewers.
Results: Of the 19 studies reviewed, 9(47.3%) investigated patellar tendon alone, 6(31.5%) did both patellar and Achilles’ tendon, and 4(21.2%) did Achilles tendon alone. The method of ultrasound administration was almost uniform for both the tendons. The studies showed that the use of ultrasound to predict lower limb tendinopathy was indefinite, but that a higher proportion of tendon disorganisation increased the risk of developing tendinopathy. In addition, promising results were obtained for the use of ultrasound in both Achilles’ and patellar tendinopathy in monitoring the effect of load or treatment on tendon structure.
Conclusions: The included studies had participants from different sports. Tendon irregularities at baseline on ultrasound were related to increased risk and future occurrence of both patellar and Achilles’ tendinopathy.
Key Words: Ultrasonography, Tendinopathy, Achilles’ tendon, Patellar tendon.
Submission completion date: 01-11-2021
Acceptance date: 16-05-2022
Tendinopathy is used to represent the clinical picture of localized pain, tenderness and/or functional limitation that increases with loading. It is a highly prevalent musculoskeletal condition affecting both athletes and non-athletes. This musculoskeletal condition most commonly affects Achilles’, patellar and rotator cuff tendons.1 Different imaging modalities are used to visualise tendon structure and abnormalities, such as magnetic resonance imaging (MRI) and ultrasound, which appear to have similar accuracy and sensitivity levels. The use of ultrasound has increased among musculoskeletal practitioners because of its minimally invasive, quick and feasible application in sports and other conditions. Clinically, ultrasound has been used to image the tendons to rule out diagnosis, monitoring the interventions and rule out the risk of developing future symptoms. In athletic population, ultrasound has been used to image painful tendons and find out structural abnormalities, such as tendon thickening with hypoechoic areas, and increased vascularity.2 Prospective studies have suggested that these structural abnormalities increased the probability of producing symptoms of tendinopathy in future. Therefore, it has been suggested that if these abnormalities are identified at baseline, the high-risk asymptomatic athletes can be ruled out and their training protocols and/or interventions can be modified to prevent the occurrence of future symptoms.3 The cross-sectional designs of many studies exploring tendon structure describe that it is unclear whether structural abnormalities on imaging predict future symptoms, or whether they are just a normal physiological response to particular sporting demands which does not warrant an increased risk of future symptoms.4 So, healthcare professionals are unable to understand whether to alter training regimes of athletes and/or intervention to prevent the future occurrence if they find structural abnormalities on imaging. Therefore, the current systematic review was planned to determine the ultrasound imaging in the prediction of future symptoms of lower limb tendinopathy.
Materials and Methods
The systematic review was done in January 2021 and comprised prospective studies that used ultrasound imaging of Achilles’ OR patellar tendons in asymptomatic patients at baseline and measurements of pain and/or function at follow-up. The review was done in line with the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) statement.5 Ethical approval was obtained from the The Institutional Review Board committee of the University of Lahore (IRB-UOL-FAHS/829-I/2021). A detailed search strategy was designed and implemented using databases and key words along with Boolean operators (Table 1).
The assessment of potential studies from database was done by two independent reviewers, and a third reviewer mediated any disagreements. The screening of titles and abstracts of the studies was done for eligibility after the removal of duplicates.
Inclusion criteria: Prospective studies exploring the predictive role of patellar, or Achilles’ tendon structure observed at baseline using ultrasound were included. The ultrasound readings must have been associated with a clinical outcome measure (pain and functional disability) to find the probability of developing patellar or Achilles’ tendinopathy in future. The duration of follow-up must have been at least 24 hours, and the tendon analysis must have been done both quantitatively and qualitatively. The included studies must have been published in English over the preceding 2 decades and must have had participants regardless of age and could include tendinopathies of either mid-portion or point of insertion at patellar or Achilles’ tendon as well as subjects with accompanying concurrent diseases.
Exclusion criteria: The studies evaluating only the development of tissue structure changes without associated clinical outcomes (pain and functional disability) and which explored changes in tendons other than patellar or Achilles’ tendon and those investigating animal tendon structures were excluded. The studies with only abstracts available and had copyright issues were also excluded.
Assessment of methodological quality: Due to lack of any standard tool to check methodological quality of prospective studies of this nature, the Critical Appraisal Skills Programme (CASP) checklist for cohort studies was used.6 There are 12 questions in the checklist, with the initial 2 being screening questions that can be answered quickly, and the remaining 10 questions investigating the conclusion, credibility and relevance to the local population. In the checklist, four questions (Nos: 2, 7, 8 and 9) investigate similar areas and were combined to review the studies. Hence, the appraisal of the included studies was done using eight leading questions. As the CASP has multiple reflections for every question, the key to reviewing studies is consistency. Therefore, the authors drew and agreed upon a criterion list for each question during the appraisal of the included studies. Since the CASP checklist was originally designed as an educational tool in workshop settings, there was no overall quality score for the included studies.
Data extraction: Data extracted from the included studies included patient demographic details, sample size, tendon structure measurement, total tendons that changed into symptomatic tendons along with normal or abnormal ultrasound imaging at baseline, and the description of tendon abnormal structural changes. Tendon pathologies were explained as any alteration in normal structure such as hypo-echogenicity, increased thickness, and hyper-vascularity seen on colour doppler ultrasound. The studies with similar clinical outcome measures, the involved tendons, the included subjects, and the prediction of symptoms in future led to pooled data analysis. For unavailable data, the methods needed clarification, and the corresponding authors of the original studies were approached. If after this contact, the missing data was not available, the studies were excluded.
Studies identification: Of the 1,393 potentially relevant studies identified after electronic search, 884(63.5%) were excluded because of overlapping data. After screening of titles and abstracts of each study, 32(3.6%) full-text studies were recognised as potentially relevant. After screening the full text of the shortlisted studies, 13(40.6%) were excluded. The remaining 19(59.4%) studies were reviewed (Figure).
Features of the included studies: The included studies had similar mean age of the participants ranging 15-66 years. All the included studies had similar participant characteristics, and all 19 except 1 were from the sporting population; 5(26.3%) involved volleyball,7-11 2(10.5%) had basketball,12,13 3(15.8%) had soccer players,14-16 1(5.2%) had elite fencers,17 3(15.8%) had runners’ population,18-20 1(5.2%) involved badminton,21 2(10.5%) had ballet dancers,22 and 1(5.2%) had different sports playing populations.23 In contrast, 1(5.2%) study had patients from the general population.24 Of the total, 6(31.6%) studies had only male participants,9,12,14-16,18 and the remaining 13(68.4%) had participants of both genders. The period of follow-up had a wide range from 2 days to 4 years. All the included studies had ultrasound as tool of investigation for tendon structure, while only 1(5.2%) study included ultrasound tissue characterisation (UTC) for tendon structure evaluation.7 Further, 9(47.4%)studies explored tendon thickness, hypo-echogenicity and vascularity,8-11,14,17,19,20,24 5(26.3%) studies investigated tendon thickness and hypo-echogenicity,12,13,15,16,23 2(10.5%) investigated thickness, hypo-echogenicity, intratendinous delamination and calcifications,18,25 2(10.5%) investigated hypo-echogenicity,7,22 and 1(5.2%) investigated vascularity only.21 There was a wide range of clinical outcome measures of pain, and/or function and consisted of subjective pain, and functional ability, such as the Victorian Institute of Sport Assessment (VISA) scale, performance special tests, like single leg squat and plyometric movements, and pain and tenderness on palpation (Table 2).
Study quality and scoring: The study population and recruited participants of the included studies followed a predesigned inclusion criterion. However, these studies had a variety of methodological quality and measurement of clinical outcome measures. Few of the included studies did not follow the inclusion criteria completely and it may have influenced the inference and generalisability of the results. All the included studies had clear study aims and objectives, with appropriate study designs and methodological quality (Table 3).
Mostly, studies included 1-2 positions to execute ultrasound scan of patellar and Achilles’ tendons: the supine positions and prone positions, respectively (Table 4).
Of the supine position, various knee flexion angles were used: 20 degrees,8,10 30 degrees,12,17 90 degrees,15, 22100 degrees,7 120 degrees.18 Besides, 1(5.2%) study used patient in supine with knee extension,11 while for Achilles’, the ankle flexion was used at 90 degrees with feet hanging over the table.14,15,17,18,20,24 Further, 1(5.2%) study evaluated anterior knee tendons with supine and 15 degrees knee flexion,21 5(26.3%) studies did not describe patient position for ultrasound scan.9,13,16,23,25 Further, 6(31.6%) studies used proximal to distal approach for ultrasound scan,7,8,15,17,22,25 while the rest of the studies did not describe the approach used. Only 2(10.5%) studies used unilateral ultrasound limb scan,7,22 while the rest had bilateral scan of either patellar or Achilles’ tendons.
Majority of the reviewed studies concluded that ultrasound could probably predict the future occurrence of tendinopathy. However, some suggested there was either no or weak association with the structural abnormalities at baseline and future tendinopathy. Of the total, 1(5.2%) study suggested that there was no remarkable change in tendon structure (echo types I-IV) during the sports event,7 and 1(5.2%) study concluded that ultrasound appearance of the tendon should not be solely responsible for the management of patellar tendinopathy.23 In addition, 1(5.2%) study investigated tendon and suggested that there was no association between structural abnormality and future tendinopathy.14
Role of ultrasound in predicting tendinopathy: The identification of risk factors of lower limb tendinopathy is very important owing to its significance in athletes taking part in different sports and to prevent the negative results and improving quality of life.26 The tendon dimensions are usually visualised through MRI and ultrasound with the latter becoming popular and modality of choice among healthcare practitioners due to its affordability and accessibility in tendon disorders and sports medicine.27 The current systematic review showed a compatible trend of high probability of developing future patellar and Achilles’ tendinopathy if the tendons exhibited irregularities on ultrasound at baseline. It is therefore possible that asymptomatic individuals with structural changes in their tendons may serve as markers of future pathology, which is later regarded as increased pain and/or functional disability.28 Due to effectiveness and uniformity of the included studies, the results can be used for the prevention and management of patellar and Achilles’ tendon disorders. The ultrasound scan values can identify the athletes at risk and provide prevention and interventions strategies, such as lower limb load management, during sports. However, there is lack of evidence to support the implementation of these strategies. Consistent with the results of the current review, a systematic review concluded that the presence of structural abnormalities, such as high-intensity zones on MRI, could predict future symptoms of lower back pain (LBP).29
Different clinical modalities, such as ultrasound and MRI, have been used in many academic and clinical discussions.30 However, there is lack of direct relationship between tendon structural disorganisation and clinical symptoms, with images potentially producing confusing clinical pictures.31 Similarly, asymptomatic populations have structural abnormalities in the tendons. Yépez et al. studied structural changes in asymptomatic soccer players and concluded that there was no correlation of these changes and clinical features of femoroacetabular impingement syndrome.32 However, evidence suggests that unnecessary imaging can actually lead to adverse and negative effects on patients’ health and behaviour.33 One study showed that low-risk patients with LBP gave poor results in overall clinical outcomes (pain and individual health) after imaging, whereas patients without imaging procedures had better clinical outcomes.34
The current review showed the same ultrasound methods being applied to visualise tendon structural abnormalities. Most studies followed the Musculoskeletal Ultrasound Technical Guidelines: Knee, defined by the European Society of Musculoskeletal Radiology.35 These uniform methodologies warrant the uniformity of scientific results and facilitate comparisons and analysis. The standard protocol used for ultrasound scanning includes position of the patient, scan direction, side of the tendon and area of interest. For ultrasound readings in research settings, unilateral scanning is sufficient. However, sometimes contralateral asymptomatic tendon exhibits symptoms of tendinopathy.36 Therefore, in clinical practice, bilateral scan is recommended. This helps the clinicians to assess tendon irregularities to prevent future occurrence of tendinopathy.
The current review comprised only studies demonstrating the role of traditional ultrasound. A newer modality, the UTC, or sonoelastography, is gaining importance in tendon disorder management and may prove to be revolutionary in terms of providing high-resolution insight into the tendon structure and providing objective measures of tendons compared to the traditional ultrasound. Only one of the studies reviewed had used UTC as the modality of choice. Similarly, MRI is commonly used to check tendon abnormalities. Another limitation is the use of variety of terminologies to explain “abnormal tendon”. This can lead to overestimation or underestimation of future clinical symptoms development. Another limitation is the inclusion of only athletic population, given the high prevalence of tendinopathies in non-athletic population.
There was found to be a substantial role of ultrasound imaging in predicting the onset of future Achilles’ and patellar tendinopathies. These findings are potentially important and can be used to prevent and treat tendon disorders. However, there is only moderate association between both factors of tendon abnormalities and future occurrence of clinical symptoms. Similarly, asymptomatic population has high prevalence of tendon abnormalities. So, in predicting overall clinical picture of tendinopathy, one element should be ultrasound imaging. Combining the examination of the tendon imaging with other factors associated with the onset of pain, such as training loads and psychosocial health, may improve the management related to the prediction of Achilles’ or patellar tendinopathy.
Acknowledgements: We are grateful to all the study subjects.
Conflict of Interest: None.
Source of Funding: None.
1. Millar NL, Silbernagel KG, Thorborg K, Kirwan PD, Galatz LM, Abrams GD, et al. Tendinopathy. Nat Rev Dis Primers. 2021; 7:1-21. doi: 10.1038/s41572-020-00234-1.
2. Arias-Buría JL, Fernández-de-Las-Peñas C, Rodríguez-Jiménez J, Plaza-Manzano G, Cleland JA, Sendarrubias GMG, et al. Ultrasound Characterization of Patellar Tendon in Non-Elite Sport Players with Painful Patellar Tendinopathy: Absolute Values or Relative Ratios? A Pilot Study. Diagnostics. 2020; 10:882. doi: 10.3390/diagnostics10110882.
3. Cassel M, Risch L, Intziegianni K, Mueller J, Stoll J, Brecht P, et al. Incidence of Achilles and patellar tendinopathy in adolescent elite athletes. Int J Sports Med. 2018; 39:726-32. doi: 10.1055/a-0633-9098.
4. Fazekas ML, Sugimoto D, Cianci A, Minor JL, Corrado GD, d’Hemecourt PA. Ultrasound examination and patellar tendinopathy scores in asymptomatic college jumpers. Phys Sportsmed. 2018; 46:477-84. doi: 10.1080/00913847.2018.1513756.
5. Sarkis-Onofre R, Catalá-López F, Aromataris E, Lockwood C. How to properly use the PRISMA Statement. Syst Rev. 2021; 10:117. doi: 10.1186/s13643-021-01671-z.
6. Purssell E. Can the Critical Appraisal Skills Programme check-lists be used alongside Grading of Recommendations Assessment, Development and Evaluation to improve transparency and decision-making? J Adv Nurs. 2020; 76:1082-9. doi: 10.1111/jan.14303.
7. van Ark M, Docking S, van den Akker‐Scheek I, Rudavsky A, Rio E, Zwerver J, et al. Does the adolescent patellar tendon respond to 5 days of cumulative load during a volleyball tournament? Scand J Med Sci Sports. 2016; 26:189-96. doi: 10.1111/sms.12426.
8. Visnes H, Tegnander A, Bahr R. Ultrasound characteristics of the patellar and quadriceps tendons among young elite athletes. Scand J Med Sci Sports. 2015; 25:205-15. doi: 10.1111/sms.12191.
9. Malliaras P, Purdam C, Maffulli N, Cook J. Temporal sequence of greyscale ultrasound changes and their relationship with neovascularity and pain in the patellar tendon. Br J Sports Med. 2010; 44:944-7. doi: 10.1136/bjsm.2008.054916.
10. Gisslén K, Gyulai C, Nordström P, Alfredson H. Normal clinical and ultrasound findings indicate a low risk to sustain jumper’s knee patellar tendinopathy: a longitudinal study on Swedish elite junior volleyball players. Br J Sports Med. 2007; 41:253-8. doi: 10.1136/bjsm.2006.029488.
11. Gisslén K, Alfredson H. Neovascularisation and pain in jumper’s knee: a prospective clinical and sonographic study in elite junior volleyball players. Br J Sports Med. 2005; 39:423-8. doi: 10.1136/bjsm.2004.013342.
12. Benítez-Martínez JC, Martínez-Ramírez P, Valera-Garrido F, Casaña-Granell J, Medina-Mirapeix F. Comparison of pain measures between tendons of elite basketball players with different Sonographic patterns. J Sport Rehabil. 2020; 29:142-7. doi: 10.1123/jsr.2018-0240.
13. Cook JL, Khan KM, Kiss ZS, Purdam CR, Griffiths L. Prospective imaging study of asymptomatic patellar tendinopathy in elite junior basketball players. J Ultrasound Med. 2000; 19:473-9. doi: 10.7863/jum.2000.19.7.473.
14. Jhingan S, Perry M, O’Driscoll G, Lewin C, Teatino R, Malliaras P, et al. Thicker Achilles tendons are a risk factor to develop Achilles tendinopathy in elite professional soccer players. Muscles Ligaments Tendons J. 2011; 1:51-6.
15. Fredberg U, Bolvig L. Significance of ultrasonographically detected asymptomatic tendinosis in the patellar and achilles tendons of elite soccer players: a longitudinal study. Am J Sports Med. 2002; 30:488-91. doi: 10.1177/03635465020300040701.
16. Fredberg U, Bolvig L, Andersen NT. Prophylactic training in asymptomatic soccer players with ultrasonographic abnormalities in Achilles and patellar tendons: the Danish Super League Study. Am J Sports Med. 2008; 36:451-60. doi: 10.1177/0363546507310073.
17. Giombini A, Dragoni S, Di Cesare A, Di Cesare M, Del Buono A, Maffulli N. Asymptomatic A chilles, patellar, and quadriceps tendinopathy: a longitudinal clinical and ultrasonographic study in elite fencers. Scand J Med Sci Sports. 2013; 23:311-6. doi: 10.1111/j.1600-0838.2011.01400.x.
18. Cushman DM, Petrin Z, Eby S, Clements ND, Haight P, Snitily B, et al. Ultrasound evaluation of the patellar tendon and Achilles tendon and its association with future pain in distance runners. Phys Sportsmed. 2020:1-10. doi: 10.1080/00913847.2020.1847004.
19. Ooi CC, Schneider ME, Malliaras P, Counsel P, Connell DA. Prevalence of morphological and mechanical stiffness alterations of mid Achilles tendons in asymptomatic marathon runners before and after a competition. Skeletal Radiol. 2015; 44:1119-27. doi: 10.1007/s00256-015-2132-6.
20. Hirschmüller A, Frey V, Konstantinidis L, Baur H, Dickhuth HH, Suedkamp NP, et al. Prognostic value of Achilles tendon Doppler sonography in asymptomatic runners. Med Sci Sports Exerc. 2012; 44:199-205. doi: 10.1249/MSS.0b013e31822b7318.
21. Boesen AP, Boesen MI, Torp-Pedersen S, Christensen R, Boesen L, Hölmich P, et al. Associations between abnormal ultrasound color Doppler measures and tendon pain symptoms in badminton players during a season: a prospective cohort study. Am J Sports Med. 2012; 40:548-55. doi: 10.1177/0363546511435478.
22. Rudavsky A, Cook J, Docking S. Proximal patellar tendon pathology can develop during adolescence in young ballet dancers-A 2‐year longitudinal study. Scand J Med Sci Sports. 2018; 28:2035-41. doi: 10.1111/sms.13095.
23. Cook J, Khan KM, Kiss Z, Coleman B, Griffiths L. Asymptomatic hypoechoic regions on patellar tendon ultrasound: A 4 year clinical and ultrasound followup of 46 tendons. Scand J Med Sci Sports. 2001; 11:321-7. doi: 10.1034/j.1600-0838.2001.110602.x.
24. Khan K, Forster B, Robinson J, Cheong Y, Louis L, Maclean L, et al. Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? A two year prospective study. Br J Sports Med. 2003; 37:149-53. doi: 10.1136/bjsm.37.2.149.
25. Comin J, Cook JL, Malliaras P, McCormack M, Calleja M, Clarke A, et al. The prevalence and clinical significance of sonographic tendon abnormalities in asymptomatic ballet dancers: a 24-month longitudinal study. Br J Sports Med. 2013; 47:89-92. doi: 10.1136/bjsports-2012-091303.
26. Kabore C, Salier Q, Geerts P, Kaux JF. Management of systemic risk factors for chronic tendinopathy. Sci Sports. 2021.
27. Albano D, Coppola A, Gitto S, Rapisarda S, Messina C, Sconfienza LM. Imaging of calcific tendinopathy around the shoulder: usual and unusual presentations and common pitfalls. Radiol Med. 2021;12: 608-19. doi: 10.1007/s11547-020-01300-0.
28. Harris M, Schultz A, Drew MK, Rio E, Adams S, Edwards S. Thirty-seven jump-landing biomechanical variables are associated with asymptomatic patellar tendon abnormality and patellar tendinopathy: A systematic review. Phys Ther Sport. 2020; 45:38-55. doi: 10.1016/j.ptsp.2020.03.011.
29. Hill L, Aboud D, Elliott J, Magnussen J, Sterling M, Steffens D, et al. Do findings identified on magnetic resonance imaging predict future neck pain? A systematic review. Spine J. 2018; 18:880-91.
30. Gatz M, Bode D, Betsch M, Quack V, Tingart M, Kuhl C, et al. Multimodal Ultrasound Versus MRI for the Diagnosis and Monitoring of Achilles Tendinopathy: A Prospective Longitudinal Study. Orthop J Sports Med. 2021; 9:23259671211006826. doi: 10.1177/23259671211006826.
31. Sánchez Romero EA, Pollet J, Martín Pérez S, Alonso Pérez JL, Muñoz Fernández AC, Pedersini P, et al. Lower Limb Tendinopathy Tissue Changes Assessed through Ultrasound: A Narrative Review. Medicina. 2020; 56:378. doi: 10.3390/medicina56080378.
32. Yépez AK, Abreu M, Germani B, Galia CR. Prevalence of femoroacetabular impingement morphology in asymptomatic youth soccer players: magnetic resonance imaging study with clinical correlation☆. Rev Bras Ortop. 2017;52:14-20. doi: 10.1016/j.rboe.2017.06.005.
33. Lemmers G, van Lankveld W, Westert G, Van der Wees P, Staal J. Imaging versus no imaging for low back pain: a systematic review, measuring costs, healthcare utilization and absence from work. Eur Spine J. 2019;28: 937-50. doi: 10.1007/s00586-019-05918-1.
34. Hall AM, Bassler KA, Thorne B, Maher CG. Do not routinely offer imaging for uncomplicated low back pain. BMJ. 2021; 372:291. doi: 10.1136/bmj.n291.
35. Sconfienza LM, Albano D, Allen G, Bazzocchi A, Bignotti B, Chianca V, et al. Clinical indications for musculoskeletal ultrasound updated in 2017 by European Society of Musculoskeletal Radiology (ESSR) consensus. Eur Radiol. 2018; 28:5338-51.
36. Vallance P, Crowley L, Vicenzino B, Malliaras P. Contralateral mechanical hyperalgesia and altered pain modulation in men who have unilateral insertional Achilles tendinopathy: a crosssectional study. Musculoskelet Sci Pract. 2021; 52:102353. doi: 10.1016/j.msksp.2021.102353.
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