Skip to main content
Download PDF

Changes of inflammation in patients with psoriatic arthritis after high intensity interval training assessed by ultrasound and MRI, a randomized controlled trial

BMC Musculoskeletal Disorders volume 24, Article number: 743 (2023) Cite this article

Abstract

Background

In psoriatic arthritis (PsA) there is a theoretical risk of increased disease activity related to strenuous physical activity, including exercise. We evaluated the effect of high intensity interval training (HIIT) on objective measures of inflammation in PsA assessed by ultrasound (US) of peripheral joints and entheses, and by bone marrow edema (BME) on MRI of the sacroiliac joints (SIJ) and spine.

Methods

We randomly assigned 67 PsA patients to an intervention group that performed structured HIIT for 11 weeks, or to a control group instructed not to change their physical exercise habits. Outcome measures included US evaluation of the total cohort and MRI in a subgroup of 41; both assessed at 3 months. We calculated the proportions with an increased US B-mode and power-doppler (PD) signal of joints and entheses and Spondyloarthritis-Research-Consortium-of-Canada (SPARCC)-BME score of the SIJ and spine for both groups.

Results

Proportions with an increased US B-mode score of the joints were 32% and 28% in HIIT and control groups, respectively. Corresponding proportions of PD scores of the joints were 7% and 10% and PD scores of entheses were 32% and 31%.

The proportions with increased MRI BME of the SIJ were 6% in the HIIT group and 10% in the control group. Corresponding proportions were 6% and 5% for the MRI BME of the spine.

Conclusion

In PsA patients with a low to moderate disease activity, there was no clear evidence of objectively measured increased inflammation after HIIT, as evaluated by US and MRI.

Trial registration

ClinicalTrials.gov NCT02995460 (16/12/2016).

Peer Review reports

Background

Psoriatic arthritis (PsA) is an inflammatory chronic disease with diverse manifestations including peripheral arthritis, enthesitis, dactylitis and spondylarthritis [1]. PsA is commonly associated with obesity and the metabolic syndrome; these comorbidities can increase patients` risks of cardiovascular disease and mortality [2,3,4,5]. Physical exercise (defined as an activity that is planned, structured and repetitive, and that is aiming to improve or maintain one or more dimensions of physical fitness [6]) is recommended for patients with PsA especially due to the high prevalence of overweight/obesity, and the risk of comorbidities such as metabolic syndrome and cardiovascular disease [7, 8]. Further, physical exercise may be beneficial regarding disease activity in patients with arthritis [9]. This has primarily been demonstrated in ankylosing spondylitis [10] and rheumatoid arthritis [11]. However, in PsA there is a potential risk of increased disease activity, including worsening of enthesitis, after physical exercise due to excess impact loading and subsequent mechanical strain [12, 13]. It has been hypothesized that mechanical strain may be of etiologic relevance to enthesitis and arthritis, e.g., as an “internal Koebner phenomenon”. There are few data available on physical exercise in patients with PsA. However, beneficial effect has been demonstrated regarding functional capacity, general well-being, fatigue, and quality of life [14, 15]. In addition, it seems that physical exercise is well tolerated measured by disease activity markers and patient reported outcomes [14]. However, no studies have demonstrated a stable disease activity in PsA assessed by objective measurements after physical exercise. Knowledge about the effects on inflammatory activity after physical exercise in PsA is crucial to implementing optimal and appropriate recommendations.

Traditional physical examination has limitations regarding the identification of the source of musculoskeletal signs and symptoms in PsA. This relates in some measure to difficulties differentiating inflammation driven signs and symptoms from those that are non-inflammatory or related to damage [16]. Thus, evaluating the burden of enthesitis, peripheral arthritis and inflammatory back pain is challenging [17]. Ultrasonography (US) is a more sensitive tool than clinical examination for visualization of inflammatory changes in peripheral joints and entheses in patients with PsA [16]. Further, swollen joints but not tender joints are associated with arthritis assessed by US [18]. In PsA, joint tenderness has a low association with imaging signs of inflammation, particularly in patients with high self-reported pain [19].

Axial inflammation in spondyloarthritis (SpA) and PsA is traditionally evaluated by the composite scores BASDAI and ASDAS [20]. However, they are likely to be affected by peripheral disease activity as well [21]. Magnetic resonance imaging (MRI) provides the most sensitive method for detection of axial inflammation [22]. Both MRI and US have been validated as tools reliable of demonstrating inflammatory activity in PsA [23,24,25].

The aim of this study was to evaluate the impact of high intensity interval training (HIIT) on objective measures of inflammation in PsA assessed by US of peripheral joints and entheses as well as bone marrow edema (BME) in MRI of the sacroiliac joints (SIJ) and spine.

Methods

Design

Results are based on analyzes of data from a study which previously has been described in detail. In short, this was a randomized controlled trial (RCT) with two parallel groups, comparing an intervention group performing HIIT three times per week for 11 weeks with a control group with no change in pre-study physical exercise habits. Randomization of the total study sample was done in three consecutive blocks. Sample size was calculated according to the primary outcome in the original study [15]. The study was conducted in compliance with the Helsinki Declaration and all the patients provided a written informed consent. The trial was approved by the regional ethics committee, REK south-east, Norway (RECnr 2012/1646).

Trial registration: NCT02995460 (16/12/2016).

Patients

Eligible patients were between ages 18–65 years and fulfilled the ClASsification for Psoriatic ARthritis (CASPAR) criteria. The exclusion criteria included: patients with inability to exercise; patients with unstable ischemic cardiovascular disease or severe pulmonary disease; an anticipated need for a change in synthetic or biologic Disease Modifying Anti Rheumatic Drugs (DMARDs) during the intervention period (a change in corticosteroid doses and intra-articular corticosteroid injections were allowed until four weeks before follow up); pregnancy, breastfeeding; and drug or alcohol addictions [15]. All the participants provided a written informed consent.

Intervention

The exercise intervention was performed as a supervised HIIT program starting with 10 min of warm up, followed by four times four minutes exercise at 85–95% of HRmax interrupted by three minutes exercise at 70% of the HRmax [26]. The supervised HIIT was performed on a stationary bicycle twice a week with an intermitting day of rest. Additionally, the participants did one self-guided HIIT a week [15].

Ultrasonography protocol

US evaluations were performed by a rheumatologist experienced in US (RST) at baseline and at 3 months follow up. The duration of each US examination was approximately 30–45 min. The sonographer was blinded with respect to group allocation at baseline but not at follow up and was aware of the clinical results at both timepoints. Brightness mode (B-mode) and Power Doppler (PD) sonography were performed at 34 mandatory joints (bilateral metacarpo-phalangeal 1–5, radio-carpal, inter-carpal, radio-ulnar, knees, talo-crural, subtalar, talo-navicular, metatarso-phalangeal 1–5) with the Norwegian ultrasonographic atlas [27] as reference and additional joints found to be swollen or tender by 66/68 joint count. Further, 10 mandatory entheses (bilateral quadriceps, proximal and distal patellar tendons, Achilles, plantar fasciae) and additionally entheses found to be tender by clinical examination of 19 other entheses (first and seventh costosternal joints, anterior superior iliac spine, iliac crest, fifth lumbar spinous process, posterior superior iliac spine, lateral and medial epicondyle, triceps, great trochanter) were scanned for PD activity [28]. B-mode and PD signals in joints and entheses were semi quantitatively graded 0–3 [27]. The US examinations were performed using a GE Logic E9 ultrasound device with two multifrequency linear transducers (4–15 MHz and 2–8 MHz).

Magnetic resonance imaging

A subset of the total study PsA cohort, including patients from the second and third randomization block, underwent MRI of the SIJ and spine at baseline, and at 3 months of follow up, at average 13 (range: 8 – 26) days after completion of the intervention. MRIs were obtained using two 1.5 T routine whole body MR scanners. A Short Tau Inversion Recovery (STIR) sequence and a T1-weighted turbo spin-echo sequence (TSE) based on a standardized protocol were applied in the semi-coronal scan plane of the SIJs and in the sagittal scan plane for the spine were used for examination of BME [29, 30].

The data on MRI spine has previously been methodologically described [31].

SPARCC scoring

A rheumatologist (RST) trained in the Spondyloarthritis Research Consortium of Canada (SPARCC) scoring methods and blinded to group allocation, timepoints and clinical outcomes, scored the STIR images of the SIJ and the spine according to the SPARCC SIJ and Spine MRI Indices for inflammation [29, 30]. In the SIJ, the six consecutive slices covering the cartilaginous part of the joints, were scored. The total maximum SPARCC score is 72 for all six slices of SIJ. For the spine, the six most abnormal disco-vertebral levels on the STIR sequence were selected. Three consecutive sagittal slices, that represent the most abnormal slices for each level, were chosen for scoring at that level. The total maximum SPARCC score is 108 for all six levels of the spine. A score less than 2 is defined as being in remission for both SIJ and Spine [32]. The minimal important change is 2,5 and 5 in SPARCC BME score for SIJ and spine, respectively [32, 33].

Statistics

Descriptive statistics are presented as mean ± SD or as median and interquartile range for non-normally distributed variables.

The difference in scores between baseline and follow up were used to classify patients as having a worse or unchanged/improved outcome in US and SPARCC BME scores. For US, a worsening was defined as an increase of one unit in B-mode or PD scores. A worsening was defined by SPARCC BME scores if scores had positive values of the minimal important change criterion or higher. The proportions with an increased US and SPARCC BME scores were calculated in percent with 95% confidence intervals (CI) for each group. Further, logistic regression analysis was performed to calculate the odds ratios (ORs) with 95% CIs for worsening in the US and SPARCC BME scores. To evaluate the actual difference in scores, the mean change between baseline and follow up was calculated for all scores in each group. Further, linear regression was performed to evaluate whether there was a difference in mean change between the groups.

All statistical analyzes were conducted using StataMP 16 (16.1 Copyright 1985–2019 StataCorp LLC, StataCorp, 4905 Lakeway Drive, College Station, Texas 77,845 USA).

Results

For the US analyzes, 67 patients with PsA were included (32 in the intervention and 35 in the control groups). Recruitment, randomization and exclusions in the main study were as previously described [15]. Of the 67 patients, 10 patients dropped out before the follow up, leaving 57 patients (28 in the intervention and 29 in the control groups) for evaluation of changes in US scores. A subgroup of 41 patients (21 in the intervention and 20 in the control groups) agreed to undergo MRI of the SIJs and the spine at baseline. Four of those dropped out of the study before the MRI could be done at follow up, leaving 37 patients (17 in the intervention and 20 in the control groups) for evaluation of changes in BME scores. Overall, the included patients had a low to moderate disease activity. Baseline characteristics of the patients are presented in Table 1.

Table 1 Baseline characteristics in the intervention and control groups of patients with psoriatic arthritis
Full size table

Proportions with an increased B-mode score of the joints were 32% (95% CI, 15 to 49) in the HIIT group and 28% (95% CI, 11 to 44) in the control group. For the PD scores of the joints the proportions were 7% (95% CI, -2 to 17) and 10% (95% CI, -1 to 21) in HIIT and control groups, respectively. Further, the PD scores of entheses increased in 32% (95% CI, 15 to 49) of cases in the HIIT group and 31% (95% CI, 14 to 48) in the control group (Table 2).

Table 2 Proportions with increased B-mode and power doppler scores of joints and power doppler scores of entheses, and Odds ratio (OR) for a worsening comparing the intervention and control groups with psoriatic arthritis after the high intensity interval training
Full size table

The proportions with increased MRI BME of the SIJ were 6% (95% CI, -5 to 17) in the HIIT group and 10% (95% CI, -3 to 23) in the control group. For the MRI BME of the spine the proportions of increased scores were 6% (95% CI, -5 to 17) and 5% (95% CI, -5 to 15) in HIIT and control groups, respectively (Table 3).

Table 3 Proportions with increased bone marrow edema in MRI of the sacroiliac joints and spine, and Odds ratio (OR) for a worsening comparing the intervention and control subgroups with psoriatic arthritis after the high intensity interval training
Full size table

The changes for each individual in both groups from baseline to three months in PD of entheses and MRI BME of SIJ are illustrated in Fig. 1. In the Supplementary files, figures S 1 and S 2 are illustrations of the corresponding changes in US B-mode and PD of the joints as well as MRI BME of the spine.

Fig. 1
figure 1

Changes in US power doppler scores of the entheses and MRI-BME-SPARCC scores of the SIJ for each individual in the control and HIIT groups at baseline and 3 months. Each number at the x-axis represents individuals in a descending order according to the baseline value for each variable. In the case of a missing column, it either represents the value 0 or missing for that individual. When representing a missing value, it is noted underneath each chart. US – ultrasound, PD – power doppler, SIJ – sacroiliac joints, BME—bone marrow edema, SPARCC—Spondyloarthritis-Research-Consortium-of-Canada, HIIT—high intensity interval training, BL- baseline, 3M—3 months

Full size image

The OR for a worsening of disease activity measured by US in the B-mode and PD scores of the joints was 1.24 (95% CI, 0.40 to 3.88) and 0.67 (95% CI, 0.10 to 4.33), respectively, when comparing the HIIT group with the control group (Table 2). The OR for a worsening in PD score of entheses was 1.05 (95% CI, 0.34 to 3.22) comparing the HIIT group to the controls.

The OR for worsening in MRI assessed BME was 0.56 (95% CI, 0.05 to 6.51) for the SIJs and 1.19 (95% CI, 0.07 to 20.54) for the spine, comparing the HIIT group to controls (Table 3).

The differences in mean changes of the scores were -0.18 (95% CI, -2.61 to 2.25) for US B-mode of joints; 0.53 (95% CI, -1.23 to 2.29) for US PD of joints; -0.10 (95% CI, -0.80 to 0.60) for US PD of entheses; 0.23 (95% CI, -0.94 to 1.39) for BME in SIJ; 3.51 (95% CI, -2.83 to 9.85) for BME in the spine; comparing the HIIT group with the control group.

Discussion

In this RCT, there was no clear evidence of an increased risk of inflammation after three months of HIIT, evaluated by objective measures such as US of the peripheral joints and entheses, as well as by MRI BME of the SIJ and spine, comparing the HIIT group with controls.

It is crucial to implementing recommendations on physical activity and exercise to be aware of potentially harmful effects of this activity on inflammation in PsA. It has been hypothesized that mechanical stress in an inflammatory environment can promote the onset of enthesitis [34]. Animal models mimicking human PsA, suggests deleterious effects of biomechanical stress on Achille’s tendon insertion generating local inflammation and an excess of bone formation [12]. Results from similar studies in patients with PsA are contradictory. One study suggests an association between physical exercise and structural damage to the Achilles tendon but did not show associated inflammation [35]. Further, this study found no association between clinical enthesitis and achilles enthesitis defined by US in patients with PsA. In another study, PsA patients reporting regular physical activity did not have an increased risk of enthesitis evaluated by US. However, the patients who reported avoidance of any physical activity had less enthesis inflammation assessed by US [36].

In healthy individuals, both at low activity and after physical activity, US findings of active inflammation at the lower limb entheses have been observed [37,38,39]. However, one study found that patients with SpA have a significantly higher degree of enthesitis evaluated by US compared to active athletes [40]. This could be explained by a greater ability to reverse inflammation induced by mechanical stress in healthy individuals [41]. Thus, it seems reasonable to propose a systematic rest before US evaluation of enthesis after physical activity [40].

Reducing the inflammatory environment with treatments could reduce the risk of enthesitis. Thus, it seems rational for patients to be in remission before starting any vigorous physical activity. Properly adapted and supervised exercise could also minimize this risk [14].

In our study, we did not evaluate for structural changes. However, the proportions with an increase of inflammation in the entheses were equal in both groups. This could be due to a low to minimal disease activity at baseline due to good medical treatment, thus protecting the patients from a flare after the HIIT. Also, the HIIT exercise was performed on a stationary bicycle that minimizes the mechanical stress to lower limbs and back. Finally, the timing of the US evaluation after the HIIT could be of importance as it was performed 1–2 weeks after the last HIIT.

Only a few studies have evaluated the impact of physical activity on joint inflammation in PsA [14, 42]. In our main study we observed a stable DAS44 and pain score after HIIT assuming a non-deleterious impact on joint inflammation [15]. These findings are supported by the US results in our present study although the proportion with an increase in US B-mode was slightly higher in the HIIT group. However, the proportion with an increase in US PD was lower in the HIIT group compared to controls.

MRI BME in spine and SIJ are not unique findings in PsA and SpA. MRI BME in the SIJ is frequently seen in other conditions as well, such as in patients with nonspecific back pain and in healthy subjects such as athletes and military recruits. And especially in postpartum women with buttock/pelvic pain a positive MRI BME in SIJ has been observed [43, 44]. Mechanical strain can provoke BME in SIJ in healthy individuals. However, in a large cross-sectional study self-reported physical activity of more than 2 h per week did not increase MRI BME of neither SIJ nor spine [44]. Still, it was found that a high BMI is associated with an increased risk of BME. In SpA and PsA, clinical studies indicate a beneficial effect of physical exercise on axial inflammation evaluated by BASDAI and ASDAS-CRP [42, 45].

Our patients with PsA had a low degree of BME in both the SIJ and spine at baseline and they had a moderate axial inflammation measured by ASDAS-CRP. Further, only 15% were HLA B27 positive. The axial phenotype of PsA is associated with HLA B27 [46]. Still, one study found that only 25%-30% with axial involvement in PsA are HLA B27 positive [47]. However, the lower proportion of HLA B27 positive PsA patients in our study may indicate that only a minority of the patients had an axial phenotype of PsA and thus explain the stable degree of BME after HIIT. We observed a smaller proportion with an increase in MRI BME of the SIJ in the HIIT group compared to controls.

A strength of this study was the randomized and longitudinal design. Further, the use of objective evaluation of inflammation by US and MRI covering both the peripheral joints, entheses and axial skeleton, is reflecting the whole specter of potential regions with inflammation in PsA. Also, the MRI reader was blinded to group allocation, timepoint and clinical outcomes. The chosen mode of intervention, the HIIT, is a standardized method of physical exercise and may be a more reliable measure of physical exercise compared to self-report of activity.

Adherence is a major barrier to interventions such as physical activity. However, the dropout rate was only 6–7% in both groups making the risk estimates more reliable. We have no information about the activity of the control group. However, the VO2 max (an objective measure of cardiorespiratory fitness) capacity increased significantly in the HIIT group compared to controls, indicating that the HIIT group did more physical exercise compared to controls, data not shown [48].

Other limitations to this study imply the small sample size, especially regarding the subset of participants with MRI in which only two thirds of the study cohort are included. Accordingly, the CIs are wide, which may imply a lack of power to observe small changes and making the proportions and risk estimates imprecise.

Further, the sonographer was not blinded to group allocation and clinical scores at follow up and US findings were not confirmed by another sonographer. However, previous studies in US found a good interrater reliability among skilled sonographers [49] and using a standardized protocol as in this study, facilitates the accuracy [28].

The external validity may be questioned as patients volunteering to this kind of activity may not previously have experienced axial or entheses inflammation to a higher degree, as that might have prevented them from attending.

Conclusion

In PsA patients with a low to moderate disease activity, there was no clear evidence of an increased risk of objectively measured inflammation evaluated by US and MRI after HIIT, comparing the intervention group to controls. This supports that HIIT is safe in PsA without increasing disease activity, at least in patients with a low to moderate disease activity.

Availability of data and materials

The data from the current study can be made available upon request to the corresponding author and after approved application to the ethics committee.

Abbreviations

PsA:

Psoriatic Arthritis

HIIT:

High Intensity Interval Training

BME:

Bone Marrow Edema

US:

Ultrasonography

SIJ:

Sacroiliac Joint

PD:

Power Doppler

SPARCC:

Spondyloarthritis-Research-Consortium-of-Canada

MRI:

Magnetic Resonance Imaging

SpA:

Spondyloarthritis

BASDAI:

Bath Ankylosing Spondylitis Disease Activity Index

ASDAS:

Ankylosing Spondylitis Disease Activity Score

RCT:

Randomized Controlled Trial

CASPAR:

ClASsification for Psoriatic ARthritis

DMARDs:

Disease Modifying Anti Rheumatic Drugs

HRmax:

Heartrate maximum

B-mode:

Brightness mode

STIR:

Short Tau Inversion Recovery

TSE:

Turbo spin-echo

OR:

Odds ratio

VO2max:

Maximal oxygen uptake

References

  1. Coates LC, Helliwell PS. Psoriatic arthritis: state of the art review. Clin Med (Lond). 2017;17(1):65–70.

    PubMed  Google Scholar 

  2. Gladman DD, Ang M, Su L, Tom BD, Schentag CT, Farewell VT. Cardiovascular morbidity in psoriatic arthritis. Ann Rheum Dis. 2009;68(7):1131–5.

    CAS  PubMed  Google Scholar 

  3. Eder L, Wu Y, Chandran V, Cook R, Gladman DD. Incidence and predictors for cardiovascular events in patients with psoriatic arthritis. Ann Rheum Dis. 2016;75(9):1680–6.

    PubMed  Google Scholar 

  4. Gulati AM, Semb AG, Rollefstad S, Romundstad PR, Kavanaugh A, Gulati S, et al. On the HUNT for cardiovascular risk factors and disease in patients with psoriatic arthritis: population-based data from the Nord-Trondelag Health Study. Ann Rheum Dis. 2016;75(5):819–24.

    CAS  PubMed  Google Scholar 

  5. Polachek A, Touma Z, Anderson M, Eder L. Risk of Cardiovascular morbidity in patients with psoriatic arthritis: a meta-analysis of observational studies. Arthritis Care Res. 2017;69(1):67–74.

    Google Scholar 

  6. Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43(7):1334–59.

    PubMed  Google Scholar 

  7. Lubrano E, Spadaro A, Parsons WJ. Rehabilitation in psoriatic arthritis. J Rheumatol. 2009;83:81–2.

    Google Scholar 

  8. Rausch Osthoff AK, Niedermann K, Braun J, Adams J, Brodin N, Dagfinrud H, et al. 2018 EULAR recommendations for physical activity in people with inflammatory arthritis and osteoarthritis. Ann Rheum Dis. 2018;77(9):1251–60.

    PubMed  Google Scholar 

  9. Sveaas SH, Smedslund G, Hagen KB, Dagfinrud H. Effect of cardiorespiratory and strength exercises on disease activity in patients with inflammatory rheumatic diseases: a systematic review and meta-analysis. Br J Sports Med. 2017;51(14):1065–72.

    PubMed  Google Scholar 

  10. Pecourneau V, Degboe Y, Barnetche T, Cantagrel A, Constantin A, Ruyssen-Witrand A. Effectiveness of exercise programs in ankylosing spondylitis: a meta-analysis of randomized controlled trials. Arch Phys Med Rehabil. 2018;99(2):383-9 e1.

    PubMed  Google Scholar 

  11. Metsios GS, Kitas GD. Physical activity, exercise and rheumatoid arthritis: Effectiveness, mechanisms and implementation. Best Pract Res Clin Rheumatol. 2018;32(5):669–82.

    PubMed  Google Scholar 

  12. Jacques P, Lambrecht S, Verheugen E, Pauwels E, Kollias G, Armaka M, et al. Proof of concept: enthesitis and new bone formation in spondyloarthritis are driven by mechanical strain and stromal cells. Ann Rheum Dis. 2014;73(2):437–45.

    PubMed  Google Scholar 

  13. McGonagle DG, Helliwell PS, Douglas V. Enthesitis in Psoriatic Disease. Dermatology (Basel, Switzerland). 2012;225:100–9.

    PubMed  Google Scholar 

  14. Kessler J, Chouk M, Ruban T, Prati C, Wendling D, Verhoeven F. Psoriatic arthritis and physical activity: a systematic review. Clin Rheumatol. 2021;40(11):4379–89.

  15. Thomsen RS, Nilsen TIL, Haugeberg G, Bye A, Kavanaugh A, Hoff M. The impact of high intensity interval training on disease activity and patient disease perception in patients with psoriatic arthritis: A randomized controlled trial. Arthr Care Res. 2018;71(4):530–7.

  16. Wiell C, Szkudlarek M, Hasselquist M, Moller JM, Vestergaard A, Norregaard J, et al. Ultrasonography, magnetic resonance imaging, radiography, and clinical assessment of inflammatory and destructive changes in fingers and toes of patients with psoriatic arthritis. Arthritis Res Ther. 2007;9(6):R119.

    PubMed  PubMed Central  Google Scholar 

  17. Watad A, Eshed I, McGonagle D. Lessons learned from imaging on enthesitis in psoriatic arthritis. Isr Med Assoc J. 2017;19(11):708–11.

    PubMed  Google Scholar 

  18. Hammer HB, Michelsen B, Sexton J, Haugen IK, Provan SA, Haavardsholm EA, et al. Swollen, but not tender joints, are independently associated with ultrasound synovitis: results from a longitudinal observational study of patients with established rheumatoid arthritis. Ann Rheum Dis. 2019;78(9):1179–85.

    PubMed  Google Scholar 

  19. Felbo SK, Wiell C, Ostergaard M, Poggenborg RP, Boyesen P, Hammer HB, et al. Do tender joints in active psoriatic arthritis reflect inflammation assessed by ultrasound and magnetic resonance imaging? Rheumatology (Oxford, England). 2021;61(2):723–33.

  20. Kilic G, Kilic E, Nas K, Karkucak M, Capkin E, Dagli AZ, et al. Comparison of ASDAS and BASDAI as a measure of disease activity in axial psoriatic arthritis. Clin Rheumatol. 2015;34(3):515–21.

    PubMed  Google Scholar 

  21. Tucker LJ, Coates LC, Helliwell PS. Assessing disease activity in psoriatic arthritis: a literature review. Rheumatol Ther. 2019;6(1):23–32.

    PubMed  Google Scholar 

  22. Puhakka KB, Jurik AG, Egund N, Schiottz-Christensen B, Stengaard-Pedersen K, Van Overeem Hansen G, et al. Imaging of sacroiliitis in early seronegative spondylarthropathy. Assessment of abnormalities by MR in comparison with radiography and CT. Acta Radiol. 2003;44(2):218–29.

    PubMed  Google Scholar 

  23. Poggenborg RP, Ostergaard M, Terslev L. Imaging in psoriatic arthritis. Rheum Dis Clin North Am. 2015;41(4):593–613.

    PubMed  Google Scholar 

  24. Felbo SK, Terslev L, Ostergaard M. Imaging in peripheral and axial psoriatic arthritis: contributions to diagnosis, follow-up, prognosis and knowledge of pathogenesis. Clin Exp Rheumatol. 2018;36 Suppl 114(5):24–34.

    PubMed  Google Scholar 

  25. Aydin SZ, Mathew AJ, Koppikar S, Eder L, Ostergaard M. Imaging in the diagnosis and management of peripheral psoriatic arthritis. Best Pract Res Clin Rheumatol. 2020;34(6):101594.

    PubMed  Google Scholar 

  26. Helgerud J, Hoydal K, Wang E, Karlsen T, Berg P, Bjerkaas M, et al. Aerobic high-intensity intervals improve VO2max more than moderate training. Med Sci Sports Exerc. 2007;39(4):665–71.

    PubMed  Google Scholar 

  27. Hammer HB, Bolton-King P, Bakkeheim V, Berg TH, Sundt E, Kongtorp AK, et al. Examination of intra and interrater reliability with a new ultrasonographic reference atlas for scoring of synovitis in patients with rheumatoid arthritis. Ann Rheum Dis. 2011;70(11):1995–8.

    PubMed  Google Scholar 

  28. Michelsen B, Diamantopoulos AP, Hammer HB, Soldal DM, Kavanaugh A, Haugeberg G. Ultrasonographic evaluation in psoriatic arthritis is of major importance in evaluating disease activity. Ann Rheum Dis. 2016;75(12):2108–13.

    PubMed  Google Scholar 

  29. Maksymowych WP, Inman RD, Salonen D, Dhillon SS, Krishnananthan R, Stone M, et al. Spondyloarthritis Research Consortium of Canada magnetic resonance imaging index for assessment of spinal inflammation in ankylosing spondylitis. Arthritis Rheum. 2005;53(4):502–9.

    PubMed  Google Scholar 

  30. Maksymowych WP, Inman RD, Salonen D, Dhillon SS, Williams M, Stone M, et al. Spondyloarthritis research Consortium of Canada magnetic resonance imaging index for assessment of sacroiliac joint inflammation in ankylosing spondylitis. Arthritis Rheum. 2005;53(5):703–9.

    PubMed  Google Scholar 

  31. Chronaiou I, Giskeodegard GF, Neubert A, Hoffmann-Skjostad TV, Thomsen RS, Hoff M, et al. Evaluating the impact of high intensity interval training on axial psoriatic arthritis based on MR images. Diagnostics (Basel). 2022;12(6):1420.

  32. van den Berg R, de Hooge M, Bakker PA, van Gaalen F, Navarro-Compan V, Fagerli KM, et al. Metric Properties of the SPARCC Score of the Sacroiliac Joints - Data from Baseline, 3-month, and 12-month Followup in the SPACE Cohort. J Rheumatol. 2015;42(7):1186–93.

    PubMed  Google Scholar 

  33. Maksymowych WP, Lambert RG, Brown LS, Pangan AL. Defining the minimally important change for the spondyloarthritis research consortium of Canada spine and sacroiliac joint magnetic resonance imaging indices for ankylosing spondylitis. J Rheumatol. 2012;39(8):1666–74.

    PubMed  Google Scholar 

  34. Kehl AS, Corr M, Weisman MH. Review: Enthesitis: new insights into pathogenesis, diagnostic modalities, and treatment. Arthr Rheumatol (Hoboken, NJ). 2016;68(2):312–22.

    Google Scholar 

  35. Michelsen B, Diamantopoulos AP, Soldal DM, Hammer HB, Kavanaugh A, Haugeberg G. Achilles enthesitis defined by ultrasound is not associated with clinical enthesitis in patients with psoriatic arthritis. RMD Open. 2017;3(2):e000486.

    PubMed  PubMed Central  Google Scholar 

  36. Wervers K, Herrings I, Luime JJ, Tchetverikov I, Gerards AH, Hazes JMW, et al. Association of physical activity and medication with enthesitis on ultrasound in psoriatic arthritis. J Rheumatol. 2019;46(10):1290–4.

  37. Di Matteo A, Filippucci E, Cipolletta E, Martire V, Jesus D, Musca A, et al. How normal is the enthesis by ultrasound in healthy subjects? Clin Exp Rheumatol. 2020;38(3):472–8.

    PubMed  Google Scholar 

  38. Meric JC, Grandgeorge Y, Lotito G, Pham T. Walking before an ultrasound assessment increases the enthesis score significantly. J Rheumatol. 2011;38(5):961.

    PubMed  Google Scholar 

  39. Proft F, Grunke M, Reindl C, Schramm MA, Mueller F, Kriegmair M, et al. The influence of long distance running on sonographic joint and tendon pathology: results from a prospective study with marathon runners. BMC Musculoskelet Disord. 2016;17:272.

    PubMed  PubMed Central  Google Scholar 

  40. Lanfranchi MA, Leluc O, Tavano A, Wormser C, Morange S, Chagnaud C, et al. Are Ultrasound Findings Similar in Patients with Axial Spondyloarthritis and in Athlete Entheses? J Rheumatol. 2017;44(5):609–12.

    PubMed  Google Scholar 

  41. Malliaras P, Chan O, Simran G, Martinez de Albornoz P, Morrissey D, Maffulli N. Doppler ultrasound signal in Achilles tendinopathy reduces immediately after activity. Int J Sports Med. 2012;33(6):480–4.

    CAS  PubMed  Google Scholar 

  42. Roger-Silva D, Natour J, Moreira E, Jennings F. A resistance exercise program improves functional capacity of patients with psoriatic arthritis: a randomized controlled trial. Clin Rheumatol. 2018;37(2):389–95.

    PubMed  Google Scholar 

  43. Seven S, Ostergaard M, Morsel-Carlsen L, Sorensen IJ, Bonde B, Thamsborg G, et al. Magnetic resonance imaging of lesions in the sacroiliac joints for differentiation of patients with axial spondyloarthritis from control subjects with or without pelvic or buttock pain: a prospective, cross-sectional study of 204 participants. Arthr Rheumatol (Hoboken, NJ). 2019;71(12):2034–46.

    Google Scholar 

  44. Baraliakos X, Richter A, Feldmann D, Ott A, Buelow R, Schmidt CO, et al. Which factors are associated with bone marrow oedema suspicious of axial spondyloarthritis as detected by MRI in the sacroiliac joints and the spine in the general population? Ann Rheum Dis. 2020;80(4):469–74.

  45. Sveaas SH, Bilberg A, Berg IJ, Provan SA, Rollefstad S, Semb AG, et al. High intensity exercise for 3 months reduces disease activity in axial spondyloarthritis (axSpA): a multicentre randomised trial of 100 patients. Br J Sports Med. 2019;54(5):292–7.

  46. Jadon DR, Sengupta R, Nightingale A, Lindsay M, Korendowych E, Robinson G, et al. Axial disease in psoriatic arthritis study: defining the clinical and radiographic phenotype of psoriatic spondyloarthritis. Ann Rheum Dis. 2017;76(4):701–7.

    PubMed  Google Scholar 

  47. Coates LC, Baraliakos X, Blanco FJ, Blanco-Morales EA, Braun J, Chandran V, et al. The phenotype of axial spondyloarthritis: is it dependent on HLA-B27 status? Arthritis Care Res. 2021;73(6):856–60.

    CAS  Google Scholar 

  48. Thomsen RS, Nilsen TIL, Haugeberg G, Bye A, Kavanaugh A, Hoff M. Effect of high-intensity interval training on cardiovascular disease risk factors and body composition in psoriatic arthritis: a randomised controlled trial. RMD Open. 2018;4(2):e000729.

    PubMed  PubMed Central  Google Scholar 

  49. Ficjan A, Husic R, Gretler J, Lackner A, Graninger WB, Gutierrez M, et al. Ultrasound composite scores for the assessment of inflammatory and structural pathologies in Psoriatic Arthritis (PsASon-Score). Arthritis Res Ther. 2014;16(5):476.

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the department of rheumatology at St. Olavs Hospital for the contribution in recruiting patients to the main trial. The participating patients also deserve our gratitude.

Funding

Open access funding provided by Norwegian University of Science and Technology No specific funding was received from any public, commercial or not-for-profit organization to carry out the work described in this article. Dr. Ruth Thomsen acknowledges the grant from the Norwegian ExtraFoundation for Health and Rehabilitation and Central Norway Regional Health Authority. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Department of Neuromedicine and Movement Science, NTNU, Faculty of Medicine, Norwegian University of Science and Technology, Post Box 8905, N-7491, Trondheim, Norway

    Ruth Stoklund Thomsen, Glenn Haugeberg & Mari Hoff

  2. Department of Circulation and Medical Imaging, NTNU, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology, Trondheim, Norway

    Ruth Stoklund Thomsen & Beathe Sitter

  3. Department of Rheumatology, St Olavs Hospital, Trondheim University Hospital, Trondheim, Norway

    Ruth Stoklund Thomsen & Mari Hoff

  4. Department of Public Health and Nursing, NTNU, Norwegian University of Science and Technology, Trondheim, Norway

    Tom Ivar Lund Nilsen

  5. Department of Anaesthesia and Intensive Care, St Olavs Hospital, Trondheim University Hospital, Trondheim, Norway

    Tom Ivar Lund Nilsen

  6. Division of Rheumatology, Department of Internal Medicine, Hospital of Southern Norway Trust, Kristiansand, Norway

    Glenn Haugeberg

  7. Division of Rheumatology, Allergy, and Immunology, School of Medicine, University of California, San Diego, USA

    Arthur Kavanaugh

  8. Copenhagen Center for Arthritis Research (COPECARE), Center for Rheumatology and Spine Disease, Rigshospitalet, Denmark

    Susanne Juhl Pedersen

Authors
  1. Ruth Stoklund Thomsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tom Ivar Lund Nilsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Glenn Haugeberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Beathe Sitter
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arthur Kavanaugh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Susanne Juhl Pedersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mari Hoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

RST: conception and design of the trial, performing the trial, statistical analyses and interpretation of the data, preparing tables and figures, writing. TILN: statistical analyses and interpretation of the data, preparing tables and figures, writing. AK, GH, SJP, BS: interpretation of the data, writing. MH: conception and design of the trial, interpretation of the data, writing. All authors reviewed the manuscript. The author(s) read and approved the final manuscript.

Corresponding author

Correspondence to Ruth Stoklund Thomsen.

Ethics declarations

Ethics approval and consent to participate

The study was conducted in compliance with the Helsinki Declaration and all the patients provided a written informed consent. The trial was approved by the Norwegian Regional Committee for Medical and Health Research Ethics, REK south-east (RECnr 2012/1646).

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1:

Figure S1. Changes in US B-mode and power doppler scores of the joints for each individual in the control and HIIT groups at baseline and 3 months.

Additional file 2:

Figure S2. Changes in MRI BME SPARCC scores of the spine for each individual in control and HIIT groups at baseline and 3 months.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thomsen, R.S., Nilsen, T.I.L., Haugeberg, G. et al. Changes of inflammation in patients with psoriatic arthritis after high intensity interval training assessed by ultrasound and MRI, a randomized controlled trial. BMC Musculoskelet Disord 24, 743 (2023). https://doi.org/10.1186/s12891-023-06871-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12891-023-06871-3

Keywords

BMC Musculoskeletal Disorders

ISSN: 1471-2474

Contact us