Study design Case–control design.
Background Tendinopathy is characterised by pain on tendon loading. In persistent cases of upper limb tendinopathy, it is frequently associated with central nervous system sensitisation, whereas less commonly linked in the case of persistent lower limb tendinopathies.
Objectives Compare somatosensory and psychological profiles of participants with persistent patellar (PT) and Achilles tendinopathies (AT) with pain-free controls.
Methods A comprehensive battery of Quantitative Sensory Testing (QST) was assessed at standardised sites of the affected tendon and remotely (lateral elbow) by a blinded assessor. Participants completed the Victorian Institute of Sports Assessment, a health-related quality of life questionnaire, the Hospital Anxiety and Depression Scale and the Active Australia Questionnaire. Independent t-test and analysis of covariance (sex-adjusted and age-adjusted) were performed to compare groups.
Results Participants with PT and AT did not exhibit differences from controls for the QST at the remote site, but there were differences at the affected tendon site. Compared with controls, participants with PT displayed significantly lower pressure pain threshold locally at the tendon (p=0.012) and fewer single limb decline squats before pain onset, whereas participants with AT only displayed fewer single heel raises before pain onset, but this pain was of a higher intensity.
Conclusion PT and AT appear to be predominantly local not widespread pain states related to loading of tendons without significant features of central sensitisation.
Level of evidence Level 4.
- chronic pain
- central sensitization
- pain threshold
- athletic injuries
- jumper’s knee
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Lower limb tendinopathies such as patellar tendinopathy (PT) and Achilles tendinopathy (AT) are common overuse injuries in sports like volleyball and running, and are characterised by persistent pain and physical disability.1–3 There is a subgroup of patients with persistent tendon pain that has minimal or no inflammation or structural damage,4 5 indicating that their pain might be more than just a local tendon (peripheral) condition.6
Recent evidence suggests that widespread somatosensory changes within the nervous system are a feature of those with persistent tendon pain, but this refers predominantly to lateral elbow tendinopathy.7 8 Bilateral lower cold pain threshold (CPT) was found in a subgroup with severe lateral epicondylalgia (LE) and was a prognostic factor for a poorer outcome.9 10 The state of knowledge of the role of the somatosensory system in persistent PT and AT is not as advanced.8 In PT cohorts, mechanical hyperalgesia as measured with pressure pain thresholds (PPT) was lower than controls in one study,11 but not in another.12 In AT mechanical hyperalgesia was demonstrated at the site of the tendinopathy (ie, localised) but not at a remote site.13 14 This infers a locally mediated tendon pain, but is somewhat inconsistent with findings of an inefficient conditioned pain modulation14 and disrupted tactile acuity at the site of pain15 that infer centrally mediated mechanisms.
Psychosocial factors (kinesiophobia, anxiety and depression) and behavioural factors are implicated in persistent musculoskeletal conditions that exhibit central sensitisation.16–18 Knowledge of psychological characteristics associated with persistent tendinopathies is scarce and inconsistent.19 In LE, some studies have reported higher levels of anxiety and depression,20 21 whereas others have not.9 10 Pain and disability of shoulder impingement are associated with pain catastrophisation and kinesiophobia.22 Investigating lower limb tendinopathies, no association between anxiety, depression and PT was found, whereas there is a negative effect of kinesiophobia on the recovery from physical work of heel rise in AT.12 23
Improved understanding of somatosensory, psychosocial and behavioural factors might assist in the understanding of pain and disability reported by individuals with PT and AT. The primary aim of this study was to assess demographic, somatosensory and psychological factors in individuals with AT or PT compared with pain-free control participants and to evaluate any association with the level of severity of pain and disability. A secondary aim was to compare somatosensory and psychological factors between PT and AT to help determine any similarities or differences in these two lower limb tendinopathies.
In this case–control study, an investigator blind to the participants’ condition performed Quantitative Sensory Testing (QST) in participants with PT and AT and in participants without pain. The participants without pain served as controls for the PT and AT groups separately, and an attempt was made to match on the basis of age and sex. This was done because PT generally affects a younger population than does AT,24 25 and there is evidence of sex and age differences on QST,26 psychological27 and physical measures.28 Ethical approval was granted by the Medical Research Ethics Committee of the University of Queensland, and all participants provided informed consent prior to participation.
Participants with unilateral or bilateral PT or AT and pain-free control participants were recruited within Brisbane, Australia, through social media (Facebook) and university online advertisement from February 2015 to April 2016. Volunteers with and without pain underwent eligibility screening with a survey (online and telephone) and a physical examination by a registered musculoskeletal physiotherapist. Inclusion criteria were (1) persistent pain of ≥3/10 on a Numeric Pain Rating Scale (NPRS) (0 is ‘no pain’, 10 is ‘worst pain imaginable’) for more than 3 months; (2) pain and tenderness on palpation of the patellar tendon or the Achilles’ tendon for PT and AT, respectively; and (3) provocation of pain on a loading test of the affected limb (ie, repeated decline squat for PT and heel raise for AT). Exclusion criteria for PT and AT were corticosteroid or other injections in the preceding 12 months; previous surgery in the area of pain; any major trauma to the knee or Achilles, respectively (eg, tendon rupture, ligament injuries, patella dislocation, muscular injuries); or any other significant musculoskeletal injuries limiting daily activities and seeking treatment within the last 6 months. Exclusion criteria for controls were a history of pain or previous surgery on the patellar or Achilles’ tendon. Exclusion criteria for all participants were neurological conditions or known neurological deficits, diabetes mellitus, previous surgery in the area of the lower back or fibromyalgia.
Quantitative Sensory Testing
QST measures response profiles to sensory stimulation with a range of modalities in order to evaluate somatosensory function.29 30 The German Network on Neuropathic Pain (DFNS) developed a standardised QST protocol consisting of seven different tests that measure 13 parameters, including various types of mechanical and thermal detection and pain measures.26 QST was performed in all individuals according to the methodology described by the DFNS.26 The full QST protocol was performed at two standardised locations for each individual. Participants with PT and their matched controls were tested unilaterally over the patellar tendon directly distal to the apex of the patella. Participants with AT and their matched controls were measured unilaterally approximately 2–5 cm proximal to the calcaneal insertion. For tendinopathy cohorts, the most affected lower limb was used in cases with bilateral expression of their tendinopathy, whereas for control participants, the test limb was randomly chosen. QST was also performed over a remote site in all participants: the lateral elbow (side randomly allocated).
Thermal tests were performed using the Thermal Sensory Analyser (Medoc, Ramat Yisha, Israel) and consisted of warm and cold detection thresholds, heat pain thresholds (HPT) and CPT. The baseline temperature was 32°C. Thermal measurements were obtained with ramped stimuli (1°C/s) and stopped when the participant pressed a button. Minimal and maximal temperatures were 0°C and 50°C. Thermal sensory limen (TSL) was assessed by alternating warm and cold stimuli, and participants were asked about paradoxical heat sensation. The mechanical tests consisted of seven different parameters. Mechanical detection thresholds (MDT) were measured with standardised von Frey monofilaments (1.65–6.65 mN or 0.008–300 g, respectively). Mechanical pain threshold (MPT) consisted of seven weighted mechanical pinpricks (MRC Systems, Heidelberg, Germany) with fixed stimuli intensities of 8, 16, 32, 64, 128, 256 and 512 mN (flat contact area, diameter 0.25 mm). The geometrical mean of five trials was calculated for MDT and MPT. Mechanical pain sensitivity (MPS) and dynamic mechanical allodynia (ALL) were performed as part of the stimulus response test, obtaining a pain response function on a scale from 0 to 10 after every stimulus (‘0’ indicating no pain, ‘10’ indicating worst pain imaginable). A pseudo-randomised schedule of five trials consisting of ten stimuli (seven pinprick and three tactile stimuli) was used, developed by the DFNS. MPS was assessed using the same set of pinpricks. For ALL, a set of three light tactile stimulators were used: a cotton wisp, a cotton wool tip fixed to an elastic strip and a standardised brush (SENSElab No 5, Somedic, Sösdala, Sweden), exerting forces of ~3 mN, ~100 mN and ~200–400 mN, respectively. Vibration disappearance threshold was performed three times with a Rydel Seiffer tuning fork (64 Hz, 8/8 scale). For the wind-up ratio (WUR) a pinprick of 256 mN was used. The geometrical mean of five trials was calculated, with 30 s of rest between trials. PPT was assessed with a pressure algometer (Somedic), with probe size of 1 cm2 and rate of pressure increase of 30 kPa/s. Three repetitions of each HPT, CPT and PPT with an interval of 30 s rest were performed and the mean value was calculated. After every trial for HPT, CPT and PPT, participants were asked to rate their pain intensity on the NPRS, with 0 indicating no pain and 100 indicating the worst possible pain imaginable, and had 30 s rest before testing started again.
Quality of life
Health-related quality of life was measured in all participants with the EuroQol (EQ-5D). It consists of five dimensions: mobility, self-care, usual activities, pain/discomfort and anxiety/depression. Participants tick the most appropriate box for every dimension: no problems, some problems and extreme problems.31 Ratings were converted to utilities ranging from 0 to 1, with higher scores indicating greater quality of life.32
Anxiety and depression were measured with the Hospital Anxiety and Depression Scale, which consists of 14 items, with 7 items for both anxiety and depression. Total scores range from 0 to 21, with higher scores indicating higher levels of anxiety and depression.33
The Tampa Scale of Kinesiophobia was used to evaluate activity avoidance and fear of movement in participants with PT and AT. The questionnaire consists of 11 items on a 4-point Likert scale (‘1’ strongly disagree–‘4’ strongly agree). The total score ranges from 11 to 44 points, with higher scores indicating greater fear of reinjury due to movement.34
Activity was measured with the Active Australia Questionnaire.35 Participants reported their activity levels during the last week (walking, vigorous gardening or heavy work, vigorous physical activity, moderate physical activity) in sessions, minutes and hours. Total activity was calculated as the sum of walking time, moderate physical activity time and 2× vigorous physical activity time.35
Pain self-efficacy was measured with the Pain Self-Efficacy Questionnaire.36 It consists of 10 items that assess how confident individuals feel in completing a range of activities despite their pain, such as household chores, work and hobbies. It is rated on a 7-point Likert scale (‘0’ not confident at all–‘6’ completely confident), and the total score ranges from 0 to 60 points, with higher scores indicating greater self-efficacy.
Pain and disability
Participants with PT and AT were asked to report their average and worst pain intensity during the previous week on the NPRS, with ‘0’ indicating no pain and ‘10’ indicating worst pain imaginable.
The Victorian Institute of Sports Assessment – Patella (VISA-P) or Victorian Institute of Sports Assessment – Achilles (VISA-A) was used as an index for the severity of pain and disability. These questionnaires are frequently used and are shown to be valid, and both have a good test–retest reliability (r=0.99 and r=0.93, respectively).37 38 The total score ranges from 0 to 100, with higher scores indicating less pain and disability.
Single limb decline squats for PT and single heel raises for AT were used as a clinically applicable measure to quantify loading to pain onset. Participants were asked to repeat the task up to 25 times or until the first onset of pain. The number of repetitions to pain onset and the level of pain at pain onset on the pain NPRS were recorded.
Participants were asked not to consume analgesics or receive any treatment for PT or AT, lower back and/or leg pain 48 hours prior to assessment. The questionnaires were sent to participants prior to measurements and were checked for completeness on the day of measurements. A physical screening was performed before beginning the QST measures. The physical tests (single limb decline squat/single heel raises) were performed following QST measures to minimise provocation of symptoms that might have curtailed the QST testing or provided clues to the ‘blind’ QST rater. A demonstration of each test was included at a practice site (tibialis anterior). Starting side (right or left) and the side of the remote point were randomised among all participants by flipping a coin, but the order of QST protocol was the same for all participants.
Group data were reported as mean (SD) and frequency count as appropriate. Data for the affected tendon and remote sites of the PT and AT group were each compared with their respective control group, with point estimates of effect reported as mean differences (95% CI) where relevant. Continuous data were assessed with parametric tests (independent t-test, analysis of covariance (ANCOVA)), and ordinal data were assessed with non-parametric tests (χ2 test, Mann-Whitney U test). Age and sex differences have been reported for several QST parameters,26 so continuous QST data were assessed with an ANCOVA, adjusting for sex and age. SPSS V.21.0 was used to perform all statistical testing. For all statistical calculations, p values <0.05 were considered significant. Correlation coefficients expressed as R2 were rated as 0.01 small, 0.09 moderate, 0.25 large, 0.49 very large, 0.81 nearly perfect and 1 perfect.39
Nineteen participants (five women (26%); mean (SD) age: 29.5 (6.6) years) with PT and 15 controls (eight women (53%); 26.7 (3.0) years) were recruited (table 1). Statistically there were no significant differences in age between groups, although there was a disproportionate number of women in the control group. Participants with PT had a significantly higher body mass index (BMI) compared with controls (mean differences (MD): 3.09 kg/m2; 95% CI 0.86 to 5.32; p=0.008). The mean duration of symptoms was 42.7 (SD 39.4) months, with a mean VISA-P score of 58.1/100 (SD 14.9). The mean (SD) repetitions of single limb decline squats until the first onset of pain was 2.1 (1.6), with a mean reported pain of 2.4 (1.0) in the PT group (table 1). The PT group performed significantly fewer repetitions of single limb decline squats compared with controls (MD: −14.85; 95% CI −19.53 to –10.18; p<0.001), but reported pain was not different between groups.
Data for PT are presented as individual patient data in figure 2 and in online supplementary figure 1, and in summary statistics in table 2. PPT of the affected patellar tendon was significantly lower in PT compared with controls, with a mean group difference of −180.25 kPa (95% CI −317.62 to −42.89; p=0.012), adjusted for sex and age (table 2). No differences in PPT at the lateral elbow were found between PT and controls. No other QST measures were significantly different between PT and controls. Quality of life was lower in participants with PT compared with controls (MD: −0.18; 95% CI −0.23 to –0.14; p<0.001) (table 1). No group differences were seen in measures of anxiety, depression or physical activity.
Supplementary Table 1
VISA-P exhibited small to moderate correlations with anxiety (R2=0.352; p=0.012), depression (R2=0.312; p=0.020) and pain self-efficacy (R2=0. 263; p=0.035).
Thirty participants with AT (13 women (43%); mean (SD) age 45.7 (11.7) years) and 11 age-matched and sex-matched controls (five women (45%); mean (SD) age 41.0 (17.8) years) were recruited (table 1). There were no significant differences between groups for age and sex. The AT group had a significantly higher BMI than controls (MD: 4.97 kg/m2; 95% CI 2.29 to 7.65; p=0.001). BMI of ≥30 kg/m2 was observed in 37.9% of participants with AT, but in no control participants. Eighteen participants (60%) reported symptoms at the mid-Achilles’ tendon, eight (27%) at the Achilles’ insertion and four (13%) at both sites. The mean duration of symptoms was 38.6 months (SD 71.0), with an average VISA-A score of 56.8/100 (SD 17.3). The mean (SD) repetitions of single heel raises until the first onset of pain was 10.3 (8.3), with a mean reported pain of 2.9 (2.4). The AT group performed significantly fewer repetitions of single heel raises (MD: −12.22; 95% CI −16.71 to −7.74; p<0.001) and reported higher pain (MD: 1.90; 95% CI 0.14 to 3.65; p=0.035) compared with controls (table 1). No significant group differences were found on any of the QST measures over either the Achilles’ tendon or lateral elbow for AT compared with their pain-free controls (table 3). Data for AT are presented as individual patient data in figure 2 and in online supplementary figure 1. Large variability was found within the AT group for TSL, MDT, MPT and WUR. Quality of life was lower in participants with AT compared with controls (MD: −0.23; 95% CI −0.27 to –0.18; p<0.001) (table 1). No significant group differences in measures of anxiety, depression or physical activity were found in the AT group compared with controls.
There was a significant but small to moderate association between VISA-A and single heel raises (repetitions to pain onset: R2=0.377, p=0.001; pain NPRS: R2=0.270, p=0.008), quality of life scores (R2=0.224, p=0.017) and lower pain self-efficacy (R2=0.220, p=0.018). There were no significant correlations between VISA-A and physical activity levels.
AT versus PT
The PT group was significantly younger (MD: −16.20; 95% CI −21.54 to –10.86; p<0.001) and had a significantly lower BMI (MD: −2.92; 95% CI −5.45 to –0.38; p=0.025) than the AT group (table 1). In the AT group, 27.6% had a normal body mass (BMI<25), 34.5% were overweight (BMI 25–30) and 37.9% were obese (BMI≥30). In the PT group, 47.4% had a normal body mass, 36.8% were overweight and only 15.8% were obese. Quality of life of the AT group was significantly lower than the PT group (MD: 0.088; 95% CI 0.033 to 0.143; p=0.002), also after controlling for age and BMI. Higher depression scores were seen in the AT group compared with the PT group, but this was largely accounted for by age (p=0.013) after accounting for age and BMI (MD −0.186; 95% CI −1.916 to 1.544; p=0.829).
In this exploratory study we assessed the demographics, somatosensory profiles and psychological factors in relation to persistent pain in participants with PT and AT compared with pain-free controls. The data show that in our cohort of PT and AT, there is very little evidence of altered somatosensory profiles measured with QST or for psychological factors. The data show that for PT, there were altered somatosensory profiles, both a decrease in PPT and in lower limb loading pain threshold. For AT there was a reduction in lower limb loading pain threshold, and these individuals rated their pain substantially higher than the controls. The higher pain ratings at pain onset for single heel raise loading of the Achilles’ tendon infer the possibility that as well as a peripheral sensitisation there might exist some altered central pain processing (loss of descending inhibition or gain in facilitation) in AT.
Our data support a pain mechanism that is predominantly localised at the tendon. Previous work has shown that tenocytes respond to repetitive physical loading and mechanical stress of the tendon, and that these tenocytes release algogenic substances (eg, substance P).40–42 The pain expressed in our patients with persistent tendinopathies is usually experienced during or after physical loading of the tendon and not at rest without any antecedent provocative physical activity. Our findings of mechanical hyperalgesia locally at the affected tendon and reduced capacity to load the tendon (ie, reduced loading to pain onset with single limb decline squat and single heel raise) are consistent with a local sensitisation process. This local/peripheral sensitisation is plausibly related to algogenic substances released through mechanical stimulation of tenocytes.
Significantly lower PPT scores for participants with PT compared with controls, with no other differences in pain or sensory thresholds either locally or at a remote site, suggest pain in persistent PT is characterised by peripheral mechanical hyperalgesia. This corroborates with the findings in athletes with PT compared with asymptomatic controls measured on the most painful spot,11 but not with another study that reported peripheral mechanical pinprick allodynia (eg, pain from a stimulus that normally does not provoke pain) and no differences in PPT in men with PT, measured on a standardised spot.12 This, as well as the scatter in the plots of individual data (figure 2), tends to signify that there is a level of heterogeneity in the presentation of PT, which warrants further exploration.
In AT, no differences were found locally or remotely for any QST compared with controls, which concurs with findings of a recent case–control study in AT.13 The results are contradictory to a recent study that found lowered PPT on the most painful spot in participants with AT compared with controls.43 The absence of hyperalgesia found in our study may be because we performed blinded examination of PPT at a standardised location over the mid-tendon. This standardised location may not target their most painful spot, which is a significant issue if the condition is expressed predominantly as a peripheral (localised) hyperalgesia. Similar to others, we found no evidence of widespread pain as one of the features for central sensitisation by testing a remote site at the elbow in either PT or AT.13 14 These findings are different from the evidence in the upper limb.
Consistent with previous research, PT is more common in men than in women and affects a much younger population than AT.25 44 45 Earlier studies have shown that people with PT tend to be taller and heavier compared with controls,45 46 whereas people with AT are more likely to be obese.47–49 Other factors such as quality of life, obesity and depression may be more important in AT than PT44; however, the scores for quality of life and depression in this study are not outside normal range nor clinically meaningful.50 51 With regards to quality of life, the mean scores are similar to those reported by participants with persistent LE.10
Strengths of this study include the blinding of the investigator to the status of the participant’s symptoms (AT, PT, asymptomatic), comprehensive QST for both sensory and pain domains by using the full DFNS protocol, and testing of both a local and remote site to investigate possible existence of peripheral and widespread somatosensory changes. The researcher performing the QST protocol was blinded during the whole process, and all participants were measured in the same, quiet, temperature-controlled room. We also acknowledge some limitations. Due to difficulties in recruiting in a timely manner, testing was performed on only a small sample of pain-free controls, which might have limited the power for some measures. For example, a large variability in MDT at the Achilles’ tendon was observed, with several individuals showing increased thresholds (reduced perception) of mechanical stimuli. We sought to mitigate against any erroneous inferences from our data by presenting individual patient data particularly for the pain measures, which shows that it is highly likely that even with a larger sample size any differences would be small and likely not significant. Nevertheless care is required in drawing inferences from our data to the broader population due to the relatively small sample size. The QST protocol was developed for somatosensory changes in patients with neuropathic pain, both cutaneous and deep pain; future tendinopathy pain studies should focus more on deep tissue stimulation of the tendon. Notwithstanding the relatively small sample size, this study contributes meaningfully to our understanding of PT and AT, with some of the data being consistent with the findings of others, thereby supporting the veracity of inferences drawn.
It is critical to remember that the participants with tendinopathy who were included in this study did not have other musculoskeletal pain or conditions, so the results are only germane to isolated tendinopathy. Inclusion of PT and AT participants who had other areas of musculoskeletal pain or comorbidities might have resulted in different findings and conclusions.
Persistent PT and AT appear to involve predominantly a local sensitisation process with altered PPT and loading pain threshold. Little evidence was found for central sensitisation, which is in marked contrast to previous work on upper limb tendinopathy. Caution is required in drawing inferences due to small participant numbers, necessitating confirmatory replication studies.
What are the findings?
Patellar tendinopathy is characterised by lower local tendon pressure pain and tendon loading pain threshold.
Both tendinopathies express predominantly local hyperalgesia.
Evidence of central sensitisation was not supported.
How might it impact on clinical practice in the future?
Clinical tests of loading discriminate symptomatic tendinopathy from asymptomatic controls and might be useful clinically.
Treatment strategies targeting peripheral nociceptive mechanisms as opposed to central mechanisms are advocated to optimise outcomes in isolated lower limb tendinopathies.
Funding This trial was funded by the National Health and Medical Research Council (NHMRC) Program Grant (#631717). MLP is supported by the International Postgraduate Research Scholarship (IPRS)/ University of Queensland Centennial Scholarship (UQcent).
Competing interests None declared.
Patient consent No participant identifying data are included within the paper.
Ethics approval Medical Research Ethics Committee of the University of Queensland.
Provenance and peer review Not commissioned; externally peer reviewed.