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high_intensity_shoulder_abduction_exercise_in.1
high_intensity_shoulder_abduction_exercise_in.1
ABSTRACT
BERG, O. K., F. PAULSBERG, C. BRABANT, K. ARABSOLGHAR, S. RONGLAN, N. BJØRNSEN, T. TØRHAUG, F. GRANVIKEN,
S. GISMERVIK, and J. HOFF. High-Intensity Shoulder Abduction Exercise in Subacromial Pain Syndrome. Med. Sci. Sports Exerc., Vol. 53,
No. 1, pp. 1–9, 2021. Subacromial pain syndrome (SAPS) defined as pain of nontraumatic origin localized around the acromion, is a debil-
itating, common, and often chronic condition. Among many proposed underlying causes of SAPS, hypoperfusion and hypoxic conditions in
and around the tendons may be an intrinsic cause of SAPS. Purpose: This study aimed to determine if adding high-intensity aerobic interval
training (HIIT) of the rotator cuff to usual care was feasible in SAPS and improved shoulder endurance more than usual care alone, as well as
to examine the influence on shoulder pain and disability and the response of tendinous microcirculation after HIIT. Methods: Twenty-one
subjects with chronic SAPS were randomized to two groups: experimental group (EG; n = 13) receiving HIIT in addition to treatment as usual
and control group (CG; n = 8) receiving treatment as usual. Before and after 8 wk of exercise therapy, endurance performance was assessed by
an incremental abduction exercise of the arm to exhaustion (TTE). Pain and disability was assessed by the shoulder pain and disability index
(SPADI). Contrast-enhanced ultrasound of the musculus supraspinatus and tendon was utilized to indicate tendon blood flow. RESULTS: Endurance
in the TTE test improved by an estimated 233 s more on average in EG than in CG (P = 0.001; 95% confidence interval, 102 to 363). The
SPADI score was reduced 22 points more on average in EG (P = 0.017; 95% confidence interval, −40 to −5). The change from pretest to
posttest was significant in EG for both TTE test and SPADI improvement (P < 0.001). EG also experienced less pain during exercise after
the intervention compared with CG (P < 0.001). Contrast-enhanced ultrasound indicated an increase in tendinous blood flow in EG (P = 0.019).
Conclusions: HIIT rotator cuff exercise seems to be a feasible intervention in SAPS, increasing endurance performance more than usual care alone.
Key Words: SAPS, BLOOD FLOW, ULTRASOUND, CONTRAST ENHANCED, VASCULARIZATION
C
hronic shoulder pain (duration >3 months) is a common manual labor workers requiring prolonged overhead arm posi-
musculoskeletal disorder, second only to lower back tions, or repetitive overhead sports such as swimming or volley-
pain (1). The prevalence is especially high among ball (2). Limitations in daily life are common in the patient
group, as well as sick leave due to the shoulder pain (1). Shoul-
der pain patients are characterized by reduced range of motion
Address for correspondence: Ole Kristian Berg, M.D., Faculty of Health and
Social Sciences, Molde University College, Britvegen 2, 6410 Molde, (ROM), as well as impaired muscle strength and endurance of
Norway. E-mail: olbe@himolde.no. the shoulder (3–5). Ultimately, shoulder pain may lead to dis-
Submitted for publication March 2020. ability pension at a relatively young age (6).
Accepted for publication June 2020. Attempting to define the etiology of chronic shoulder pain,
0195-9131/20/5301-0001/0 Neer (7) developed the term “shoulder impingement syndrome,”
MEDICINE & SCIENCE IN SPORTS & EXERCISE® indicating mechanical stress to the tendinous portion of the rotator
Copyright © 2020 by the American College of Sports Medicine cuff, exhibited by the acromion during lifting of the arm, as a
DOI: 10.1249/MSS.0000000000002436 mechanism responsible for shoulder pain development. However,
Copyright © 2020 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
the role of mechanical impingement as a cause of chronic intratendinous blood flow, visualized by contrast-enhanced ul-
shoulder pain is debated (8). trasound (CEUS), increases after exercise (22,23). Capillary
Mechanisms intrinsic to the tendon itself offer alternate ex- growth and tendon perfusion may be proportional to training
CLINICAL SCIENCES
planations for the development of chronic shoulder pain (9). adaptations in muscle tissue. Thus, the aim of this study was
Although no one clear pathology has been found, degeneration to investigate 1) if HIIT in addition to usual care would be fea-
of the tendons seems to be linked to changes occurring in re- sible in SAPS patients and improve rotator cuff endurance
sponse to a deficient healing response (10), possibly induced more than treatment as usual, and 2) if the HIIT group would
by hypoperfusion (11) and subsequent hypoxic triggering of have reduced pain and disability, as well as increased micro-
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cell apoptosis, inflammation, and a shift in the tendon collagen circulation in the supraspinatus tendon, more than the group
matrix toward the structurally weaker type III collagen (12). receiving treatment as usual.
Attempting to incorporate the wide etiology of chronic shoulder
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approximately 30° anterior in the frontal plane (scapular
plane), with the thumb pointing upward. One repetition
was conducted every 2 s, guided by a metronome configured
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to 0.5 Hz. The weight was increased from unloaded move-
ment by 250 g each minute until the subject failed to maintain
the rhythm or movement despite vocal encouragement, the
subject was able to complete 10 min of work, or pain in-
creased beyond 5 on a 0–10 visual analog scale. The cause of
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TTE test, a rest period of 10 min was given before the subjects
were seated on a chair without armrests with the affected arm
placed behind the back such that the thumb was pointing up-
ward and touching the spine approximately at L5. Using a
9-L probe with a Vivid E9 ultrasound machine (GE Healthcare,
Little Chalfont, United Kingdom), the musculus supraspinatus
and muscle tendon transition was visualized to confirm an intact
tendon. Next, a marking pen was used to index the best probe
position for visualization of the supraspinatus tendon. An ultra-
sound image of this positioning was also recorded and printed
such that the greater tuberosity and humeral head could be used
as landmarks to ensure similar probe positioning in all subse-
FIGURE 1—Elliptical ROI on supraspinatus tendon in a 15.7-s cine loop
quent scans both before and after the 8-wk intervention period. CEUS recording.
A 20–18G intravenous catheter (BD Veneflon Pro Safety;
Becton, Dickinson and Company, Franklin Lakes, NJ) was pilot on seven healthy shoulders revealed a coefficient of var-
placed by a medical professional in an antecubital vein on the iance of 4.6% for the CEUS method in our laboratory.
contralateral arm. A 1.5-mL bolus of ultrasound contrast fluid Pain and disability questionnaires. On day 2, subjects
(Optison; GE Healthcare, Chicago, IL) was injected followed submitted two self-report questionnaires designed to assess level
by a 10-mL saline flush, both at a rate of 1 mL·s−1. No subjects of pain and functional impairment related to the pain. The first
experienced adverse effects after the injections. was the shoulder pain and disability index (SPADI), which is a
Immediately after the injection, the subjects performed 3 min two-part 13-item questionnaire granting a total score between
of exercise in the same movement as for the TTE test, with a 0 and 100, where 0 is no pain/disability and 100 is worst pain/
workload corresponding to 80% of their respective pretest disability (24). A Norwegian translation of the SPADI, which
WRmax. The exercise procedure was used to increase the signal was translated according to recommended guidelines and showed
from capillaries and improve the visualization of tendon an intraclass correlation coefficient of 0.89 (95% confidence inter-
microcirculation. val (CI), 0.82–0.93), was used in the current study (25). The sec-
After the exercise, subjects reassumed the seated position ond questionnaire was the short questionnaire for surveillance of
with the arm behind their back and guided by markings on the long-standing pain, developed by the Norwegian Pain Association
skin, and the printed ultrasound image of the musculus supras- (NPA). Specifically, the three questions regarding level of pain
pinatus and tendon was visualized using the contrast harmonic were recorded from the NPA questionnaire (least, worst, and av-
mode of the ultrasound machine, with a mechanical index of erage pain of the former week). NPA was scored on a numeric
0.07. All ultrasound recordings were taken over 15.7 s using scale form 0 (no pain) to 10 (worst imaginable pain).
the cine loop mode and within 4 min of Optison injection. Training intervention. After the 2-d pretest, all subjects
Ultrasound imaging quantification and analysis was per- performed 8 wk of training in their respective groups, EG or
formed on a PC using EchoPac software (GE Healthcare, CG. Both groups received standardized usual care consisting
Chicago, IL). The software allows for analysis of selected regions of home exercises with regular follow-ups with the physio-
of interest (ROI) within which a quantification of mean signal therapists every other week on average. The main goal was to
intensity over the 15.7 cine loop can be made (dB·mm−2). A reestablish normal shoulder movement patterns through aware-
higher signal intensity signify a higher contrast detection, and ness, which the participants could transfer to daily activities. Fo-
therefore is an indication of vascularity. The ROI was placed cus was individual customized scapular stabilizing exercises,
in the area of greatest signal enhancement (Fig. 1), and the rotator cuff exercises, and pain-free ROM exercises, as previ-
width, length, and tilt of the ROI were noted, additionally an- ously described by Granviken and Vasseljen (26). CG contin-
atomical landmarks such as the greater tuberosity and humeral ued the program, and EG additionally received three sessions
head-guided placement, such that identical ROI and placement of HIIT per week. The HIIT was performed in the same move-
were used within each subject at pretest and posttest. A test–retest ment and frequency as the TTE test, with a workload
HIGH-INTENSITY SHOULDER ABDUCTION EXERCISE Medicine & Science in Sports & Exercise® 3
Copyright © 2020 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
corresponding to 80% of WRmax. Intervals lasted 4 min and groups exhibited a significant within-group increase in WRmax
were repeated four times interspaced by 3 min of active recov- from pretest to posttest (EG: 692 ± 480 to 1846 ± 857 g
ery where the subject walked leisurely on a treadmill (PPS Med, [P = 0.003] and CG: 719 ± 525 to 906 ± 533 g [P = 0.034]).
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Woodway, United Kingdom). If the subject was able to continue Shoulder pain and disability. The SPADI score (Table 2)
the final interval for one additional minute, the workload was was reduced 22 points more on average in EG (P = 0.017; 95%
increased by 250 g in the following session. Subjects reported CI, −40 to −5). The change from pretest to posttest was also sig-
pain on a scale from 0 to 10 before and during the sessions. nificant in EG (P < 0.001) but not in CG. Between groups, only
The workload was adjusted continuously to maintain pain the intensity of the least pain experienced the last week was
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lower than 5; if pain exceeded this point, the session was termi- significantly different (P = 0.045). The worst pain experienced
nated. Each completed session according to protocol was recorded. the last week showed a decreasing trend from pretest to post-
Statistical analyses. Power calculation was based on test in EG (P = 0.051). There was a significant difference be-
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TTE data from Brox et al. (27); a power of 0.8 and an α of tween groups that experienced pain during the TTE test
0.05 indicated a sample size of n = 24 to detect mean group (P < 0.001; risk difference, 66%).
differences of minimum 30 s. To assess the effect of the inter- Tendon blood flow. Signal enhancement, as a measure of
vention, analysis of covariance was applied, with outcome af- blood flow, in the supraspinatus tendon ROI measured by
ter treatment as an dependent variable, and baseline value and CEUS did not exhibit any group effect (pre: −30.5 ± 5.4
treatment group as covariates (28). IBM SPSS statistical soft- and −33.4 ± 2.8 dB·mm−2 to post: −28.3 ± 5.9 and −31.3 ±
ware (version 25) was used for statistical analysis, except for 5.1 dB·mm−2, for EG and CG, respectively). EG showed an in-
the dichotomous variable of pain during TTE where StataCorp crease in signal intensity from pretest to posttest (P = 0.019).
STATA (version 13) was used. Within-group change from pre- There was no significant change in CG.
test to posttest was assessed by Wilcoxon signed rank or the
McNemar test in the case of dichotomous variables. Differences
DISCUSSION
between group anthropometrics were assessed with two-sample
t-test. For all analyses, the level of significance was set to The main finding of this study was that 8 wk of HIIT ap-
P < 0.05. Data are presented as means ± SD in text and tables, pears to be a feasible intervention in SAPS patients and supe-
and means ± SE in figures for clarity. rior with regard to increases in shoulder endurance capacity in
the abduction exercise (TTE). Second, the participants in the
RESULTS HIIT group reported a larger reduction in pain and disability.
There was no significant improvement in CEUS after HIIT
Subject characteristics. Twenty-one subjects completed
in EG compared with CG concerning increased tendon micro-
the study (Table 1); two subjects dropped out of the study be-
circulation. However, these findings add to the understanding
tween pretesting and posttesting (one from CG and one from
of pathology and clinical treatment in SAPS, indicating that
EG). The dropouts were both for reasons unrelated to the test-
HIIT could be a relevant supplement to exercise therapy of SAPS.
ing or training. Three subjects were excluded before posttest
However, larger studies are needed to confirm the effects and
because of exclusion criteria revealed after randomization. For
mechanisms targeting hypoxia related intrinsic causes.
complete study flowchart in line with the CONSORT 2010
Shoulder endurance capacity. After 8 wk of HIIT ab-
Statement, see Figure 2 (29). One subject in CG received a
duction exercise of the arm, targeting the affected musculus
corticosteroid injection during follow up. Analysis with and
supraspinatus and tendon, TTE increased 136% in EG. This is
without this subject did not yield different findings; thus, the
higher than what has previously been reported for a similar HIIT
subject was included in the analysis. Subjects in EG completed
protocol of plantar flexion, where an increase in TTE of 42%
22 ± 3 of the planed 24 training sessions over the 8-wk interven-
was reported (18). Although at a fixed workload, O’Leary et al.
tion (92% ± 13% compliance).
(30) found TTE after 18 sessions of cycling HIIT to be increased
Shoulder endurance performance. Endurance in the
by 148%. Moreover, in that study, HIIT was found to increase is-
TTE test improved by an estimated 233 s more on average
chemic pain tolerance, whereas continuous training at moderate
in EG than in CG (P = 0.001; 95% CI, 102–363; Fig. 3). The
intensity did not improve pain tolerance. In the current study, 9
increase from pretest to posttest was significant within the inter-
of 13 subjects in the HIIT group terminated the TTE test during
vention group (P < 0.001). No change from pretest to posttest
pretest because of pain sensation exceeding 5 on the visual ana-
was observed for CG. The WRmax increased by 964 g more on
log scale, whereas only 1 subject terminated the test because of
average in EG than in CG (P = 0.003; 95% CI, 386–1543). Both
pain at posttest (Table 2). This significant reduction may be re-
TABLE 1. Subject anthropometrics. lated to increased ischemic pain tolerance after HIIT, in addition
EG (n = 13) CG (n = 8) to delayed anaerobic conditions due to improved aerobic capacity
Age, yr 47 ± 12 50 ± 14 in the trained muscles. Indeed, Beach et al. (3) demonstrated a
Sex, male/female 9/4 2/6 negative correlation between both arm external rotation and ab-
BMI, kg·m−2 29 ± 5 24 ± 2*
Symptom duration, months 38 ± 62 48 ± 53 duction endurance to shoulder pain in competitive swimmers.
Data are mean ± SD.
In line with the increase in TTE, WRmax also increased
*P < 0.05 between-group difference. more in EG than in CG. However, both groups exhibited an
Copyright © 2020 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
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FIGURE 2—Flowchart of enrollment, inclusion, allocation, follow-up, and analysis of study participants.
increase in WRmax of 167% and 26% for EG and CG, respec- cutoff at 10 min during the incremental test. No subjects in
tively. This increase in EG is higher than previous publications any group reached this ceiling at pretest. Thus, if the test had
using similar HIIT protocols to that of the current study in sin- allowed for further increase in workload, the increase and group
gle limb exercises, who report an increases of 37% and 43.9% difference may have been further amplified. This may also add
(18,19). In addition, at posttest, 7 subjects in EG reached the to the explanation of why termination due to pain was reduced
HIGH-INTENSITY SHOULDER ABDUCTION EXERCISE Medicine & Science in Sports & Exercise® 5
Copyright © 2020 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
in EG reductions in SPADI score of ~20, 27 and 31 points have
been reported after a supervised exercise for 5, 6, and 12 wk, re-
spectively (36,37). However, although the supervision may be
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Copyright © 2020 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
significant increase from pretest to posttest in EG, together with to increase. The random allocation also resulted in unbalanced
the superior effects on pain and disability, may indicate a link sex distribution between groups, which probably explains the
between SAPS severity and tendinous blood flow. Support to higher BMI in EG. Notably, there was no significant differ-
CLINICAL SCIENCES
this notion may be gleaned from other studies demonstrating ence in shoulder endurance between EG and CG at pretest, in-
reduced postexercise signal enhancement in the supraspinatus dicating that the group distributions did not influence the baseline
with age greater than 40 yr (23), and that age greater than 50 yr for our primary outcome variable. However, sex distribution may
is associated with increased risk of rotator cuff tendinopathy have influenced the response to training. Thus, while controlling
(46). However, the development of chronic SAPS seems to be for selection bias, random group differences that may influence
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complex with regard to underlying pathology, as even shoul- outcome can arise. To mitigate this effect, weighing sex in the
ders that exhibit abnormalities linked to pain and tendinopathy group distribution during randomization may be considered.
remain asymptomatic (47). Thus, it seems that SAPS consists Of notice, corticosteroid injection within 1 month before
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of an interplay of unfavorable factors, of which impaired blood pretest was an exclusion criterion in the current investigation.
flow and hypoxic conditions may be one. Moreover, HIIT Such treatment is common in treatment of SAPS. However, the
emerges as a relevant approach for targeting hypoxia-related immediate effects on symptoms seem to weather over time
pain in SAPS through augmenting tendon microcirculation. (51); thus, the rationale for exclusion was the possibility of pos-
Feasibility of high-intensity interval shoulder exer- itive influence on the pretest and consequently confounding of
cise in SAPS patients. Compliance with the protocol was the effect after the exercise interventions at posttest.
high at 92% ± 13%. This is in line with Granviken and Vasseljen Notably, the home-based exercise was not systematically
(26), who reported a compliance of 80% to supervised training recorded for volume comparison in the current study. Thus, we
in a group of SAPS patient. Nikander et al. (48) reported that cannot exclude that some subjects exercised more/less than
97% of subjects were able to complete an endurance training others did, and importantly if there were group differences in
program to treat neck pain in female office workers. Compli- adherence to the recommendations. Given full compliance, the
ance up to 100% has been reported in other patient groups when volume in EG would be higher because of the added HIIT. How-
applying HIIT to isolated muscle groups (18,19). The compli- ever, anecdotal comments from some subjects in the HIIT group
ance in these and our study may be enhanced because of social indicated that they felt that the sessions were exercise enough.
support offered to the subjects by researchers and therapists. Also, physiotherapists reported that subjects in both groups fre-
However, supervised training did not result in higher compli- quently complained of not adhering to the home exercise because
ance compared with unsupervised training when offered to of- of pain. Importantly the home-based exercise model does not re-
fice workers within working hours (49). Similarly, the home cord volume as a key part of the therapy; therefore, the current
exercise group in the study by Granviken and Vasseljen (26) study represents a true comparison of treatment as usual and HIIT
had a compliance of 88% versus 80% in the supervised group. in addition to treatment as usual.
The high compliance in the current study is a good indication
that the subjects tolerated the intervention. The continuous su- CONCLUSIONS
pervision of pain by the therapist, and adjustment of workload Adding HIIT abduction exercise to usual care in treatment
if indicated, was likely of importance to the compliance and of SAPS seems to be a feasible intervention that enhances shoul-
tolerance of the intervention. Thus, supervision by a therapist der endurance capacity more than home-based exercises with bi-
may be critical to achieve the effect of HIIT on SAPS observed weekly physiotherapist follow-up alone. In addition, adding HIIT
in the current study. It is possible that similar effects can be to the treatment of SAPS patients resulted in greater reductions in
obtained incorporating HIIT in a home-based program. How- pain and disability. Tendon vascularity assessed by CEUS re-
ever, the patient should be well acquainted with the pain– vealed an increased signal intensity from pretest to posttest after
workload adjustments necessary to avoid worsening symptoms. HIIT, indicating increased tendon microcirculation and oxygen
During 12 wk of conventional physiotherapy in SAPS patients, availability as a possible mechanism for the functional improve-
a mean of 2.5 sessions per week has been described (50). Al- ments, and reduction in pain. Thus, HIIT could be considered a
though slightly higher, the three sessions per week in the cur- feasible and potent approach to reduce pain and improve func-
rent study should be considered feasible in a limited time tion in conservative treatment of SAPS.
frame (8 wk) and clinical setting. The protocol is not time or
resource demanding (average session lasting ~30 min) and The authors thank all subjects who participated in the study for their
may be performed outside the clinic if required. time and contribution. A great thanks to Tor Arne Grindal for assistance in
technical issues related to ultrasound analysis. Thanks to PT Kristin
Study limitations. EG and CG ended up in a slightly Valla Stenseth and Ingunn Kregnes for assistance with the usual care.
skewed distribution after inclusion of subjects. This was due Thanks to the medical doctors at St. Olav’s University Hospital, De-
to the two randomization software programs that were used partment of Physical Medicine and Rehabilitation, for recruiting partic-
ipants. The work was funded by the Norwegian University of Science and
during the period of the study. Thus, although randomization Technology and Molde University College.
is a strength, it also caused a difference in group size. This was The authors declare no conflict of interest financial or otherwise. Re-
further augmented by those subjects dropping out of the study sults are presented clearly, honestly, and without inappropriate manip-
ulation of data, falsification, or fabrication. The results of this study do
(Fig. 1). In addition, the relatively modest sample size in this not constitute endorsement from the American College of Sports
experiment may cause a single subject’s effect on the outcome Medicine.
HIGH-INTENSITY SHOULDER ABDUCTION EXERCISE Medicine & Science in Sports & Exercise® 7
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