Julia K Schreiner1, Florian Recker2, Dennis Scheicht3, Pantelis Karakostas1, Jana Ziob4, Charlotte Behning5, Peter Preuss6, Peter Brossart1, Valentin S Schäfer1. 1. Clinic of Internal Medicine III, Department of Oncology, Haematology, Rheumatology and Clinical Immunology, University Hospital Bonn, Bonn, Germany. 2. Department of Obstetrics and Prenatal Medicine, University Hospital Bonn, Venusberg Campus 1, 53127 Bonn, Germany. 3. Department of Rheumatology, Porz am Rhein Hospital, Cologne, Germany. 4. Department of Dermatology and Allergy, University Hospital Bonn, Bonn, Germany. 5. Institute for Medical Biometry, Informatics and Epidemiology, University Hospital Bonn, Bonn, Germany. 6. University Sports Division, University Bonn, Bonn, Germany.
Abstract
Background: Joint effusion and enthesitis are common ultrasound findings in rheumatic diseases such as rheumatoid arthritis or spondyloarthritis. However, changes of joints and entheses were not only observed in patients but also in physically active individuals and athletes. Objectives: The purpose of this study was to evaluate joint, entheseal, bursal and tendon musculoskeletal ultrasound (MSUS) findings in large and medium joints of young healthy individuals after completing a standardised weight training. Design: This is a prospective cohort study. Methods: MSUS examinations of large- and medium-sized joints, and related entheseal sites, bursae and tendons were performed on young healthy individuals (ages 18-30 years). Before, 24 and 48 h after completing 1 h of standardised weight exercise, the subjects were evaluated by MSUS. The development of the MSUS findings and associated effects were examined using generalised linear mixed effects models. Results: In total, 51 healthy individuals (52.9% female) with a mean age of 23.7 (±2.5) years were enrolled. The results showed an increase in the number of individuals with at least one joint effusion from 37 (72.5%) before the weight training to 48 (94.1%) after 48 h. Entheses with pathologies were observed in 14 participants (27.5%) at baseline, increasing to 29 participants (56.9%) 48 h after the weight training. Biceps tendon sheath effusion was detected in 9 individuals (17.6%) prior to training, rising to 22 individuals (43.1%) after 48 h. A significant increase in the number of joints with effusion and abnormal entheses within 48 h after the weight training was indicated by the generalised linear mixed effects models. Conclusion: Within 48 h after the weight training session, a significant increase in the prevalence of joint effusion in large and medium joints and the prevalence of abnormal entheses was observed. As a result, when performing and interpreting an MSUS examination, the patient's physical activities should be taken into account.
Background: Joint effusion and enthesitis are common ultrasound findings in rheumatic diseases such as rheumatoid arthritis or spondyloarthritis. However, changes of joints and entheses were not only observed in patients but also in physically active individuals and athletes. Objectives: The purpose of this study was to evaluate joint, entheseal, bursal and tendon musculoskeletal ultrasound (MSUS) findings in large and medium joints of young healthy individuals after completing a standardised weight training. Design: This is a prospective cohort study. Methods: MSUS examinations of large- and medium-sized joints, and related entheseal sites, bursae and tendons were performed on young healthy individuals (ages 18-30 years). Before, 24 and 48 h after completing 1 h of standardised weight exercise, the subjects were evaluated by MSUS. The development of the MSUS findings and associated effects were examined using generalised linear mixed effects models. Results: In total, 51 healthy individuals (52.9% female) with a mean age of 23.7 (±2.5) years were enrolled. The results showed an increase in the number of individuals with at least one joint effusion from 37 (72.5%) before the weight training to 48 (94.1%) after 48 h. Entheses with pathologies were observed in 14 participants (27.5%) at baseline, increasing to 29 participants (56.9%) 48 h after the weight training. Biceps tendon sheath effusion was detected in 9 individuals (17.6%) prior to training, rising to 22 individuals (43.1%) after 48 h. A significant increase in the number of joints with effusion and abnormal entheses within 48 h after the weight training was indicated by the generalised linear mixed effects models. Conclusion: Within 48 h after the weight training session, a significant increase in the prevalence of joint effusion in large and medium joints and the prevalence of abnormal entheses was observed. As a result, when performing and interpreting an MSUS examination, the patient's physical activities should be taken into account.
Physical activity and its effects on joints and entheses have become one of the
topics of increasing interest among athletes and sports medicine specialists, and
within the area of rheumatology. Rheumatic diseases are known to cause inflammation,
damage and abnormalities in musculoskeletal ultrasound (MSUS) of joints, tendons and
entheses, but numerous studies show that sports exercise can cause similar changes.
Some MSUS imaging studies observed joint abnormalities in athletes and physically
active individuals. One ultrasound study reported an increased intra-tendinous flow
in the dominant patellar tendon in elite badminton players after repeated matches.
Synovitis was identified in asymptomatic professional soccer players by a
magnetic resonance imaging (MRI) study in at least one joint in 67.6% of the
examined feet.
Another study including professional soccer players observed one or more knee
joint lesions, such as synovitis, cartilage and meniscal lesions in all examined joints.
Polat et al.
reported a significantly higher prevalence of tendinopathy, meniscal injury
and cartilage damage in the knees of kangoo jumpers compared with the control group
by MRI imaging.Regarding different imaging approaches of the musculoskeletal system, the ultrasound
examination has earned substantial popularity due to the flexible handling and low
costs of the procedure. In the evaluation of vascular and soft-tissue changes, and
structural abnormalities of musculoskeletal conditions, grey-scale (GS) and power
Doppler (PD) ultrasound is widely applied in rheumatological practice. To ensure
comparable results, the European League Against Rheumatism (EULAR) working group for
MSUS published standardised scanning planes for the upper and lower extremity joints.
In addition, definitions for elementary lesions, such as synovitis and
enthesitis, and their scoring were published by the working group.
Reliability was demonstrated for ultrasound examinations carried out by
experienced sonographers.
Using ultrasound on a regular basis, the conflicting observations of the
impact of physical activity on MSUS results may leave the rheumatologist unsure
regarding their evaluation. In patients with or without the diagnosis of a rheumatic
disease, physical activity may alter the presentation of ultrasound results.
Therefore, the purpose of this study was to assess the development of joint,
entheseal, bursal and tendon ultrasound findings in large and medium joints of young
healthy individuals after 1 h of standardised weight training.
Methods
This prospective cohort study was approved by the local medical ethics committee of
the University Hospital Bonn (Lfd. Nr. 149/19; date: 05/07/19), and written informed
consent was obtained from every participant prior to inclusion. The Department of
Rheumatology and Clinical Immunology at the University Hospital Bonn, Germany and
the University Sports Division of the University of Bonn, Germany recruited 51
healthy individuals [27 female (52.9%) and 24 male (47.1%) individuals] to
participate in the study. Inclusion criteria were age between 18 and 30 years and
free consensus to participate. Exclusion criteria included chronic diseases
affecting the musculoskeletal system, electronic implants, cardiac arrhythmia and
current pregnancy. Individuals were selected randomly for participation. Within 48 h
in advance of the study, participants were requested to waive physical exercise and
consumption of alcohol. After signing an informed consent form, the individuals
answered a questionnaire concerning demographic data (sex, age, ethnicity,
handedness, height and weight), medical history including sport injuries, and
duration and nature of physical activity per week. The Short-Form International
Physical Activity Questionnaire (SF-IPAQ) was used to evaluate the individual
participants’ fitness level.MSUS examination was performed before (T0), 24 h (T1) and 48 h (T2) after individuals
conducted a supervised weight training. Before starting the weight training, a
bioelectrical impedance analysis (BIA) was applied to assess the participant’s body
composition.The reporting of this study conforms to the ‘EULAR recommendations for the reporting
of ultrasound studies in rheumatic and musculoskeletal diseases (RMDs).
BIA
BIA was performed using the SECA medical Body Composition Analyzer 515 (SECA GmbH
& Co. KG, Hamburg, Germany). Tetrapolar, single-frequency (5 kHz) impedance
measurements were taken to acquire fat mass (FM), fat-free mass (FFM) and
skeletal muscle mass (SMM). Values were divided by height squared creating the
fat mass index (FMI), fat-free mass index (FFMI) and skeletal muscle mass/height
(SMM/height
) for height adjustment.[10,11]
Standardised weight training
After the first MSUS examination, the individuals conducted a standardised
whole-body weight training under the guidance of board-certified fitness
trainers.The standardised weight training consisted of eight exercises (five upper body
and three lower body exercises), three sets per exercise, and a total of 24
sets. Before the workout session, a 3-min whole-body warm-up using a rowing
ergometer was mandatory and a specific warm-up set for each exercise with 50% of
predetermined training load. Training load for each exercise was determined in a
habituation training session, using the OMNI resistance exercise scale
(OMNI-RES) to target a scale value of 8 for the first set.
Exercises in the workout session were grouped into supersets for a
time-efficient training regime (Supplementary Figure 1).Based on performed repetitions and used weight, two fitness indices were
calculated. One representing upper body strength based on the training volume
(repetitions × weight) of the seated row machine and one representing lower body
strength based on the training volume of the leg press. The training volume of
the first of three training sets of both exercises was divided by the
individuals’ BMI to calculate the indices.[14-16] Representing the
individual strength, the indices allowed for a precise comparison between the
participants. For example, participants lifting heavier weight and thus have a
higher training volume reach a higher index than participants with a lower
training volume and the same BMI.
Ultrasound examination
Three high-end ultrasound machines (two GE Logiq S8 machines, manufactured 2018;
one Alpinion E-CUBE 8 machine, manufactured 2019) with multifrequency linear
probes (8–15 or 6–15 MHz) operating at a frequency of 8–15 MHz (depending on the
joint) were used for every MSUS examination. The settings for PD ultrasound were
Doppler frequency of 7.7 MHz and pulse repetition frequency of 800 Hz for the GE
Logiq S8 machines and Doppler frequency of 6.0 MHz and pulse repetition
frequency of 600 Hz for the Alpinion E-CUBE 8 machine. An average GS ultrasound
gain of 50% was set. Ultrasound was performed by three board-certified
rheumatologists with 13 (P.K.), 14 (V.S.S.) and 16 (D.S.) years of ultrasound
experience [German Society for Ultrasound in Medicine (DEGUM)/European
Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB) level II
and III]. Sonographers used ultrasound presets for each joint, which were set
similarly for each device. Ultrasound presets were tested on 10 individuals
prior to the begin of the study to standardise image quality. Sonographers were
allowed to change image depth and focus point position, if necessary.The bilateral and dynamic ultrasound examination included large and medium joints
and assessment of specific entheseal sites (Figure 1). The large and medium joints
and respective entheses were chosen for examination as they are commonly
affected by rheumatological diseases such as rheumatoid arthritis or psoriatic
arthritis. In addition, these regions particularly endure mechanical stress due
to physical activity.
Figure 1.
Applied bilateral ultrasound planes of large and medium joints.
The bilateral examination comprised shoulder (q), elbow (b and c), wrist
(e, s and t), hip (g), knee (k and o) and ankle (j) joints and deltoid
muscle enthesis (m), common flexor and extensor tendon enthesis (d and
n), distal triceps tendon enthesis (r), distal quadriceps tendon
enthesis (h), proximal and distal patellar tendon enthesis (i), distal
Achilles’ tendon enthesis (u) and proximal plantar fascia enthesis (v).
The biceps tendon (a) and the extensor hallucis longus tendon (j),
tibialis posterior tendon (l), flexor digitorum longus tendon (l),
flexor hallucis longus tendon (l) and peroneus longus and brevis tendon
(p) were examined for tenosynovitis assessment. In addition, bursitis
evaluation of the trochanteric bursa (f), supra- and infrapatellar bursa
(h and i) and retrocalcaneal bursa (u) was conducted.
Applied bilateral ultrasound planes of large and medium joints.The bilateral examination comprised shoulder (q), elbow (b and c), wrist
(e, s and t), hip (g), knee (k and o) and ankle (j) joints and deltoid
muscle enthesis (m), common flexor and extensor tendon enthesis (d and
n), distal triceps tendon enthesis (r), distal quadriceps tendon
enthesis (h), proximal and distal patellar tendon enthesis (i), distal
Achilles’ tendon enthesis (u) and proximal plantar fascia enthesis (v).
The biceps tendon (a) and the extensor hallucis longus tendon (j),
tibialis posterior tendon (l), flexor digitorum longus tendon (l),
flexor hallucis longus tendon (l) and peroneus longus and brevis tendon
(p) were examined for tenosynovitis assessment. In addition, bursitis
evaluation of the trochanteric bursa (f), supra- and infrapatellar bursa
(h and i) and retrocalcaneal bursa (u) was conducted.Applied scanning planes for joint, enthesis, tendon and bursa lesions were
selected based on the Sonography of Large Joints in Rheumatology (SOLAR) score
and predefined scanning planes for the assessment of wrist and tibiotalar
joints, entheses, bursae and tendons as described before.[5,8,17] The
individuals were examined in a sitting position when the upper extremities were
assessed. Ultrasound examination of the lower extremities was carried out with
the participants lying on the examination table. The shoulder was assessed with
the elbow 90° flexed and the hand resting on the participant’s thigh in
supination. For dorsal assessment, an external rotation of the humerus was
performed with the elbow 90° flexed. The elbow was assessed in neutral position
and in 90° flexion for dorsal scans. The examination of wrist, hip and knee
joints was performed with the joints resting in neutral position.
Ankle joint assessment was carried out with the knee joint 90° flexed and
the foot positioned upright on the examination table in 20° plantar flexion. The
proximal plantar fascia entheses and distal Achilles’ tendon entheses were
assessed with the participant lying prone and the feet hanging over the end of
the examination table in active dorsiflexion.
The duration of the ultrasound examinations ranged between 30 and
60 min.Participants were assigned randomly to the sonographers at every visit. The
ultrasound images were blinded with regard to patient data and stored for future
rating. Image acquisition and rating were performed by different persons. The
rating was carried out by one of the authors (J.K.S.) together with each of the
experienced sonographers (V.S.S., P.K. and D.S.).
Ultrasound scoring of entheseal sites
The evaluation of entheseal sites was carried out according to the enthesitis
criteria defined by the Outcome Measures in Rheumatology (OMERACT) ultrasound
task force for enthesitis.The presence of enthesiophytes (step-up of the bone outline), calcification
(hyperechoic foci), erosion (step-down outline defect), thickened enthesis
(increased thickness of the insertion) and hypoechogenicity (absence of the
homogeneous fibrillar impression) was evaluated binarily (y/n), whereas
semiquantitative scoring for Doppler signal at the enthesis (< 2 mm from
cortical bone) was applied (grades 0–3).
Ultrasound scoring of joints, tendons and bursae
Joint effusion and synovial hyperperfusion of the joints were evaluated by GS and
PD mode using a semiquantitative score (grades 0–3).[19,20] Binary (y/n) evaluation
of the presence of bursal or tendon sheath effusion and hyperperfusion was
carried out. Effusion was defined as hypo-to anechoic area within the joint
capsule, bursa or tendon sheath. Doppler signals were evaluated for the
assessment of hyperperfusion.
Statistical analysis
For statistical analysis, SPSS statistical software, version 27.00 (IBM, Armonk,
NY, USA) and R statistical software (Version 4.0.3; R Foundation for Statistical
Computation, Vienna, Austria) were used. Absolute and relative frequencies are
presented for describing categorial variables. Mean standard deviation and
ranges were calculated for continuous data. The development of ultrasound
findings from baseline to follow-up at 24 and 48 h after the weight training and
effects on the development were analysed using generalised linear mixed effects
models. As the number of joints with effusion and entheses with pathologies are
count measurements, a Poisson distribution with a logarithmic link function was
used. To account for repeated measurements within an individual, these were
included in the model as a random effect. The time in days was included as a
fixed effect. Further independent variables, such as age, sex, hours of physical
activity per week, BMI, FMI, FFMI, SMM/height
, upper and lower body fitness indices were evaluated in separate models.
As it was assumed that the influence of these variables might be time-dependent,
a fixed term and a slope term (interaction with time) were included in the
model. The analyses were carried out on a patient level and thus findings in all
joints were summed. Missing values in the outcome were imputed by last value
carried forward. Missing values in risk factors and covariates were not imputed.
Significance level of all exploratory analyses was 0.05. Also,
p-values were not adjusted for multiple testing.
Inter- and intrareader reliability
For reliability analysis, the three sonographers (P.K., D.S. and V.S.S.) involved
in the study rated 100 stored ultrasound images of two participants. The scoring
was repeated after 24 h to assess the intrareader reliability. Joint effusion,
hyperperfusion and entheseal pathology were evaluated binarily (y/n) in GS and
PD images.
Inter-reader agreement was determined by calculating Cohen’s kappa for
each pair, based on their first image evaluation. Kappa values of less than 0.0
were considered poor, 0–0.20 slight, 0.21–0.40 fair, 0.41–0.60 moderate,
0.61–0.80 substantial and 0.81–1.0 almost perfect agreement.
Results
Population characteristics
This study comprised the examination of 51 healthy individuals with a mean age of
23.65 ± 2.46 (range: 19–30) years. Most of the participants were Caucasian
(94.1%), two individuals were African (3.9%) and one South American (2.0%). The
participants had a mean BMI of 22.54 ± 3.07 (range:
18.61–36.55) kg/m2. The BIA revealed a mean FMI, mean FFMI and SMM/height
of 4.38 ± 1.77, 18.16 ± 2.51 and 8.59 ± 1.55 kg/m2,
respectively. The mean hours of physical activity per week were 4.78 ± 3.02
(range: 1.00–15.00) h. Although the participants were asked not to perform any
physical activity 48 h prior the study, two individuals reported medium level of
physical activity. According to the results of the SF-IPAQ, 56.9% of the
individuals (n = 29) performed high-level, 31.4%
(n = 16) moderate-level and 11.8% (n = 6)
low-level physical activity. Visiting a fitness centre on a regular basis was
stated by 33 participants (64.7%). The fitness indices of the upper and lower
body were calculated with a mean of 0.88 ± 0.62 and 3.90 ± 1.12, respectively.Two individuals did not complete the last follow-up examination due to a common
cold. Seven values of both fitness indices and one value of physical activity
per week were missing.
Development of joint effusion
The number of individuals with joint effusion in at least one joint increased
from 37 individuals (72.5%) at T0 to 45 individuals (88.2%) at T1 and to 48
individuals (94.1%) at T2 after the weight training. The mean number of joints
affected by effusion was 1.49 at T0, 2.82 at T1 and 4.16 at T2.Predominantly, joint effusion was evaluated grade I. At T1, 12 joints (8.3%) and
at T2, 19 joints (8.8%) exhibited grade II effusion. Grade III effusion was
detected in only one joint at T2 (0.5%).At T1, 10 individuals (19.6%) presented with effusion in one joint, whereas in 8
individuals (15.7%), two joints with effusion were observed. In 10 individuals
(19.6%), effusion in three joints was detected. The maximum number of joints
with effusion was eight and was observed in one case (2.0%). At T2, joint
effusion in one and two joints was observed in two (3.9%) and five cases (9.8%),
respectively. Overall, 14 individuals (27.5%) presented with effusion in three
joints. The highest number of affected joints was nine and was detected in one
case (Figure 2).
Figure 2.
Number of joints with effusion per individual at baseline, after 24 and
48 h.
Development of joint effusion from baseline (T0)
to 24 h (T1) and 48 h (T2) following weight training.
Number of joints with effusion per individual at baseline, after 24 and
48 h.Development of joint effusion from baseline (T0)
to 24 h (T1) and 48 h (T2) following weight training.Synovial hyperperfusion was not detected at T0.
At T1, hyperperfusion was observed in four joints with effusion (2.8%)
and two joints without effusion (0.4%). Then, 48 h after the weight training,
hyperperfusion was detected in a total of two joints, one with simultaneous
joint effusion (0.5%) and one without (0.3%). An erosion was observed in the
knee of one individual (2.0%) at T0.The elbow joint showed the highest number of effusions at T1, with a total of 40
joints in 28 individuals (54.9%), which was followed by the wrist joint with 48
joints in 32 individuals (62.7%) at T2. The wrist was also the joint with the
highest number of individuals showing bilateral joint effusion (Figures 3 and 4).
Figure 3.
Ultrasound images of common joint and tendon effusions.
Ultrasound images of the wrist and elbow joint, and the biceps tendon,
which were the most commonly affected structures. (a) Longitudinal
section of the wrist joint (radio-carpal) displaying grade II effusion –
1: distal radius, 2: lunate bone, 3: capitate bone, 4: fourth extensor
compartment; (b) anterior longitudinal humeroulnar scan of the elbow
joint with grade I effusion – 5: humerus, 6: coronoid process of the
ulna; (c) anterior longitudinal scan of the biceps tendon displaying
tendon sheath effusion – 7: humerus, 8: biceps tendon.
Figure 4.
Development of elbow and wrist joint effusion within 48 h after the
weight training.
Ultrasound images of the elbow (a, c, e) and wrist joint (b, d, f) before
as well as 24 and 48 h after the weight training are displayed. (a)
Anterior longitudinal humeroulnar scan of the elbow joint without joint
effusion examined before the weight training; (b) longitudinal section
of the wrist joint (radio-carpal) without joint effusion before the
weight training; (c) anterior longitudinal humeroulnar scan of the elbow
joint of the same participant as in A, displaying grade I joint effusion
after 24 h; (d) longitudinal section of the wrist joint (radio-carpal)
of the same participant as in (b), presenting with grade I joint
effusion after 24 h; (e) the same participant as in (a) and (c) examined
48 h after the weight training displaying grade I joint effusion; (f)
the same participant as in (b) and (d) examined after 48 h presenting
with grade II joint effusion; 1: humerus, 2: coronoid process of the
ulna, 3: distal radius, 4: lunate bone, 5: capitate bone, 6: fourth
extensor compartment.
Ultrasound images of common joint and tendon effusions.Ultrasound images of the wrist and elbow joint, and the biceps tendon,
which were the most commonly affected structures. (a) Longitudinal
section of the wrist joint (radio-carpal) displaying grade II effusion –
1: distal radius, 2: lunate bone, 3: capitate bone, 4: fourth extensor
compartment; (b) anterior longitudinal humeroulnar scan of the elbow
joint with grade I effusion – 5: humerus, 6: coronoid process of the
ulna; (c) anterior longitudinal scan of the biceps tendon displaying
tendon sheath effusion – 7: humerus, 8: biceps tendon.Development of elbow and wrist joint effusion within 48 h after the
weight training.Ultrasound images of the elbow (a, c, e) and wrist joint (b, d, f) before
as well as 24 and 48 h after the weight training are displayed. (a)
Anterior longitudinal humeroulnar scan of the elbow joint without joint
effusion examined before the weight training; (b) longitudinal section
of the wrist joint (radio-carpal) without joint effusion before the
weight training; (c) anterior longitudinal humeroulnar scan of the elbow
joint of the same participant as in A, displaying grade I joint effusion
after 24 h; (d) longitudinal section of the wrist joint (radio-carpal)
of the same participant as in (b), presenting with grade I joint
effusion after 24 h; (e) the same participant as in (a) and (c) examined
48 h after the weight training displaying grade I joint effusion; (f)
the same participant as in (b) and (d) examined after 48 h presenting
with grade II joint effusion; 1: humerus, 2: coronoid process of the
ulna, 3: distal radius, 4: lunate bone, 5: capitate bone, 6: fourth
extensor compartment.The wrist joint showed the greatest increase in the number of affected joints at
T2, ranging from 18 joints at T0 to 48 joints at T2. The hip had the lowest
number of effusion joints at all time periods (Table 1).
Table 1.
Development of joint effusion within 48 h.
Joint
Time
Right side, n (%)
Left side, n (%)
Both sides, n (%)
No effusion, n (%)
Shoulder
T0
4 (7.8)
1 (2.0)
0 (0.0)
46 (90.2)
T1
3 (5.9)
5 (9.8)
3 (5.9)
40 (78.4)
T2
9 (17.6)
9 (17.6)
6 (11.8)
27 (52.9)
Elbow
T0
2 (3.9)
7 (13.7)
7 (13.7)
35 (68.6)
T1
4 (7.8)
12 (23.5)
12 (23.5)
23 (45.1)
T2
5 (9.8)
12 (23.5)
14 (27.5)
20 (39.2)
Wrist
T0
6 (11.8)
6 (11.8)
3 (5.9)
36 (70.6)
T1
7 (13.7)
8 (15.7)
11 (21.6)
25 (49.0)
T2
10 (19.6)
6 (11.8)
16 (31.4)
19 (37.3)
Hip
T0
0 (0.0)
1 (2.0)
0 (0.0)
50 (98.0)
T1
2 (3.9)
6 (11.8)
2 (3.9)
41 (80.4)
T2
6 (11.8)
4 (7.8)
4 (7.8)
37 (72.5)
Knee
T0
7 (13.7)
5 (9.8)
1 (2.0)
38 (74.5)
T1
4 (7.8)
10 (19.6)
2 (3.9)
35 (68.6)
T2
7 (13.7)
10 (19.6)
12 (23.5)
22 (43.1)
Ankle
T0
2 (3.9)
5 (9.8)
4 (7.8)
40 (78.4)
T1
7 (13.7)
7 (13.7)
5 (9.8)
32 (62.7)
T2
9 (17.6)
7 (13.7)
9 (17.6)
26 (51.0)
Number of participants presenting with and without joint effusion in
the respective joint detected by ultrasound at baseline (T0),
24 h (T1) and 48 h (T2) after the weight training.
Development of joint effusion within 48 h.Number of participants presenting with and without joint effusion in
the respective joint detected by ultrasound at baseline (T0),
24 h (T1) and 48 h (T2) after the weight training.
Development of entheseal pathology
Overall, 14 individuals (27.5%) presented with entheseal pathology in at least
one enthesis at T0, 24 individuals (47.1%) at T1 and 29 individuals (56.9%) at
T2. The mean number of entheses with abnormal findings per individual increased
from 0.37 at T0 to 1.02 at T1 and 1.12 at T2.
The only entheseal pathology observed at T1 and T2 was
hyperperfusion.At T1, 10 individuals (19.6%) showed hyperperfusion in one entheseal site. Seven
(13.7%) and three cases (5.9%) presented with hyperperfusion in two and three
entheses, respectively. In one case (2.0%), the maximum number of entheseal
sites with hyperperfusion identified was six.Hyperperfusion was observed in one and two entheseal sites in 11 individuals
(21.6%) and in three entheseal sites in 6 individuals (11.8%) at T2. There was
no hyperperfusion in four or five entheses, although one individual (2.0%) had
six entheseal locations with hyperperfusion. Predominantly, grade I
hyperperfusion was observed. Grade II hyperperfusion was observed in one
entheseal site at T1 (1.9% of entheseal sites with pathologies), whereas four
entheseal sites showed grade II hyperperfusion at T2 (7.0% of entheseal sites
with pathologies). A grade III hyperperfusion could not be detected at any time
point during the study.The entheseal site most affected by pathologies at T1 was the common flexor
tendon enthesis of the forearm regarding 12 entheseal sites in 11 individuals
(21.6%). The deltoid muscle insertion showed the highest number of entheses with
hyperperfusion overall, with a total number of 13 entheses in 12 individuals
(23.5%) at T2 (Figure
5). It was detected on the left side in two cases (3.9%) on the right
side in nine cases (17.6%) and on both sides in one case (2.0%). The highest
increase in affected entheses was also seen in the deltoid muscle enthesis from
three entheses at baseline to six entheses at T1 to 13 entheses at T2.
Figure 5.
Development of entheseal hyperperfusion by anatomical localisation.
The development of entheseal pathologies by anatomical localisation at T0 (baseline),
T1(after 24 h), and T2 (after 48 h) is displayed.
EN = enthesis.
Development of entheseal hyperperfusion by anatomical localisation.The development of entheseal pathologies by anatomical localisation at T0 (baseline),
T1(after 24 h), and T2 (after 48 h) is displayed.
EN = enthesis.
Factors associated with the number of joints with effusion and entheses with
pathologies
The generalised linear mixed effects models showed a significant increase in the
number of joints with effusion and entheses with pathologies per individual with
time after the weight training, p < 0.001,
Exp(b) = 1.63, 95% CI [1.45, 1.84] and
p < 0.001, Exp(b) = 1.58, 95% CI [1.27,
1.97].A significant association between the FMI and the overall number of joints with
effusion was detected when including all individuals,
p = 0.049, Exp(b) = 0.87, 95% CI [0.76, 1.00].
In a sensitivity analysis, one outlier with a considerable higher FMI
(11.71 kg/m2) compared with the mean (4.38 kg/m2) was
excluded. After exclusion, no significant effect of the FMI was observed
anymore, p = 0.211, Exp(b) = 0.91, 95% CI
[0.79, 1.05]. No significant association between age, sex, hours of physical
activity per week, BMI, FFMI, SMM/height
, upper or lower body fitness indices and the overall number of joints
with effusion was spotted.Hours of physical activity per week had a significant association with the
overall number of entheses with pathologies, p = 0.031,
Exp(b) = 0.84, 95% CI [0.73, 0.98], but when adjusting for
this variable, no effect of the time on the number of entheses with pathologies
was observed anymore. No significant association between age, sex, BMI, FMI,
FFMI, SMM/height
, upper, or lower body fitness indices and the overall number of entheses
with pathologies was noticed. None of the interaction terms between time and
other independent variables showed a significant association with the number of
entheses with pathologies or number of joints with effusion.No significant association between the development of the numbers of joints with
effusion or entheses with pathologies and age, sex, hours of physical activity
per week, BMI, FMI, FFMI, SMM/height
, upper or lower body fitness indices was noted (Supplementary Table 1).
Development of tendon and bursal ultrasound findings
The highest number of tendon abnormalities was observed in the biceps tendon.
Overall, 9 cases (17.6%) showed tendon sheath effusion at baseline, which
increased to 16 cases (31.4%) at T1 and 22 cases (43.1%) at T2. Hyperperfusion
of the biceps tendon was noted in one case at T1 (2.0%) without tendon sheath
effusion and in six participants (11.8%) at T2, of which four cases (7.8%)
presented with simultaneous tendon sheath effusion. The retrocalcaneal bursa
showed the highest number of bursal effusions as observed at baseline, at T1 and
T2 in 9 (17.6%), 12 (23.5%), and 11 (21.6%) cases, respectively (Supplementary Table 2). Hyperperfusion of the bursae or tendons
except for the biceps tendon was not observed in any case.The intrareader reliability analysis showed an excellent agreement for all
raters, reaching a mean kappa value of 0.954. Inter-reader reliability results
for the pair V.S.S./P.K. demonstrated substantial agreement
[K = 0.745, asymptotic standard error
(se) = 0.123]. An almost perfect agreement was observed for the
pairs V.S.S./D.S. (K = 0.886, se = 0.080) and
D.S./P.K. (K = 0.854, se = 0.102).
Discussion
The aim of this study was to analyse MSUS findings after 1 h of sex adjusted weight
training in terms of joint effusions, entheseal, tendons and bursal pathology in
young healthy individuals. According to our results, entheseal hyperperfusion,
observed in 56.86% (n = 29) after 48 h and joint effusion observed
in 94.12% (n = 48) after 48 h increase significantly after weight
training and thus should be interpreted with caution in the respective patient
population. In addition, biceps tendon abnormalities and effusion of the
retrocalcaneal bursa were observed in 47.1% (n = 24) and 21.6%
(n = 11) 48 h after the weight training.The mean number of joints with effusion increased from 1.49 at baseline to 2.82 after
24 h and 4.16 after 48 h. The development of joint effusion in relation to physical
activity has been studied before with varying results, largely focusing on
professional athletes. Hohmann et al.
did not detect any changes in MRI images of the hips and knees of eight
marathon runners before and after the race. Another study evaluated the knee and
ankle joints of 105 marathon runners by ultrasound observing no development or
changes in joint effusion of both joints.
Yet, in both studies, highly trained athletes were expected to undergo
frequent and high-level training in advance of the race. This may also have
influenced the results in addition to the marathon. In fact, Major and Helms
observed abnormalities in 74% of the knees of professional basketball players
by MRI during their preseason physical examination and reported a percentage of knee
joint effusion of 35%. Nevertheless, no information was given regarding physical
activity right before conducting the MRI examination.However, an influence of physical activity on joint findings was also observed in
normal volunteers. Stehling et al.
studied knee abnormalities in an asymptomatic, middle-aged population using
MRI and their association to physical activity assessed by the Physical Activity
Scale for Elderly (PASE). They described a significantly higher prevalence of knee
joint effusion, cartilage, ligament, meniscus abnormalities and bone marrow edema
pattern in participants with a higher PASE.In addition to an increased number of joints with effusion, we also found a
significantly increased number of entheses with hyperperfusion per participant after
weight training. Our results are supported by a recent study evaluating enthesitis
of the Achilles and patellar tendon, and the lateral humeral epicondyles in 32
badminton players before and after an hour of training. The researchers noted a
significantly higher PD score following training, indicating that mechanical stress
promotes entheseal hyperperfusion. However, the examination was performed directly
after the training and thus, no information was obtained on how long this
hyperperfusion lasted.
According to our results, the number of entheses displaying hyperperfusion
increases during the 48-h period. Alternatively, another study comparing the Madrid
Sonographic Enthesis Index (MASEI) scores of athletes and non-athlete controls
failed to detect a significant difference between the athletes and non-athletes.
However, they did not evaluate the direct effect of a training session but defined
‘athletes’ as individuals performing more than 6 h of physical activity per week and
required the non-athlete controls to perform less than an hour of physical activity
per week.
We observed the highest increase in individuals with entheseal hyperperfusion
at the deltoid muscle insertion. Another localisation of entheses that could have
been expected to be increasingly affected due to mechanical load is the lower
extremity. A significant increase in proximal patellar tendon entheses with
hypervascularity was previously observed in runners after performing a marathon.
In our study, the number of individuals with pathologies of entheses located
at the lower extremities was overall lower than those of the upper extremity. The
number of individuals with pathologies of the distal patellar entheses even
decreased from 6 (11.8%) to 5 (9.8%) after 48 h. This could be due to the fact that
a marathon strains the lower extremity joints more vigorously than does a weight
training session. Furthermore, a majority of the participants
(n = 30; 58.8%) stated that they perform endurance training on a
regular basis, which strenuously involves the lower extremity and may lead to
another conclusion: Wervers et al.
suggested that entheses adapt to a regular level of physical activity and
respond to a change in physical activity. Our data support this hypothesis as we
found that individuals performing weekly physical activity to a greater extent had
lower numbers of pathological entheses independently of the examination time. This
finding indicates a habituation process towards physical activity in highly trained
individuals. In patients with axial spondyloarthritis, a randomised controlled trial
showed a significant reduction of disease activity (symptoms and inflammation) after
3 months of high-intensity physical training.
However, the role of physical activity in pathophysiology and treatment of
spondyloarthritis is still not entirely understood.
As a result, our findings may not only be applicable in healthy individuals
but also in rheumatological patients; however, further studies including patients
are required to obtain deeper insights of their ultrasound presentation after
physical activity.Our study has limitations. We only observed a time frame until 48 h after the weight
training. Considering the number of entheses with pathologies and joints with
effusion still increasing within 2 days, a longer observation period might be better
to fully assess the development of the ultrasound findings. The fact that we did not
include a control group also represents a limitation to our study. In addition, we
asked the participants not to perform any physical activity within 48 h, and based
on our results, this period may not have been long enough. For further
investigation, we would recommend a longer renunciation of any physical activity by
the participants involved, which would however not be a real-life setting any
more.
Conclusion
According to our results, the prevalence of joint effusion in large and medium joints
and the prevalence of abnormal entheses increase significantly within 48 h after a
1-h weight training session. In addition, biceps tendon abnormalities and effusion
of the retrocalcaneal bursa were observed in a notable part of the study population
after 48 h. As a result, the patient’s physical activities should be considered when
performing and interpreting an MSUS examination in clinical practise as they may
alter the ultrasound findings.Click here for additional data file.Supplemental material, sj-docx-1-tab-10.1177_1759720X221111610 for Changes in
ultrasound imaging of joints, entheses, bursae and tendons 24 and 48 h after
adjusted weight training by Julia K. Schreiner, Florian Recker, Dennis Scheicht,
Pantelis Karakostas, Jana Ziob, Charlotte Behning, Peter Preuss, Peter Brossart
and Valentin S. Schäfer in Therapeutic Advances in Musculoskeletal Disease
Authors: R N Baumgartner; K M Koehler; D Gallagher; L Romero; S B Heymsfield; R R Ross; P J Garry; R D Lindeman Journal: Am J Epidemiol Date: 1998-04-15 Impact factor: 4.897
Authors: Marina Backhaus; Peter V Balint; George A Bruyn; Robin Christensen; Philip G Conaghan; Ricardo J O Ferreira; Juan Luis Garrido-Castro; Francis Guillemin; Hilde Berner Hammer; Désirée van der Heijde; Annamaria Iagnocco; Marion C Kortekaas; Robert Bm Landewé; Peter Mandl; Esperanza Naredo; Wolfgang A Schmidt; Lene Terslev; Caroline B Terwee; Ralf Thiele; Félicie Costantino; Loreto Carmona; Maarten Boers; Maria-Antonietta D'Agostino Journal: Ann Rheum Dis Date: 2021-01-22 Impact factor: 19.103
Authors: Wolfgang Hartung; Herbert Kellner; Johannes Strunk; Horst Sattler; Wolfgang A Schmidt; Boris Ehrenstein; Martin Fleck; Marina Backhaus Journal: Arthritis Care Res (Hoboken) Date: 2012-05 Impact factor: 4.794
Authors: J K Schreiner; D Scheicht; P Karakostas; F Recker; J Ziob; C Behning; P Preuss; P Brossart; V S Schäfer Journal: Scand J Rheumatol Date: 2021-12-14 Impact factor: 3.641
Authors: Alexander K Scheel; Kay-Geert A Hermann; Elke Kahler; Daniel Pasewaldt; Jacqueline Fritz; Bernd Hamm; Edgar Brunner; Gerhard A Müller; Gerd R Burmester; Marina Backhaus Journal: Arthritis Rheum Date: 2005-03
Authors: Fabian Proft; Mathias Grunke; Christiane Reindl; Markus A Schramm; Felix Mueller; Maximilian Kriegmair; Jan Leipe; Peter Weinert; Hendrik Schulze-Koops; Matthias Witt Journal: BMC Musculoskelet Disord Date: 2016-07-11 Impact factor: 2.362