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Abstract
The aim of the present study is to: (1) induce delayed onset muscle soreness (DOMS) in the neck and shoulder muscles; (2) com-
pare the pressure pain sensitivity of muscle belly with that of musculotendinous tissue after DOMS; (3) examine the gender differ-
ences in the development of DOMS. An eccentric shoulder exercise was developed to induce DOMS on neck/shoulder muscles using
a specially designed dynamometer. Eccentric shoulder contraction consisted of 5 bouts, each bout lasted 3 min, with 3 min rest per-
iod between each bout. The right shoulder was elevating against a downward pressure force of 110% maximal voluntary contraction
force exerted by the dynamometer. Pressure pain thresholds (PPT) of 11 sites (seven sites measured were muscle belly and four sites
were myotendinous area) on neck/shoulder region were measured before, immediately after, 24 and 48 h after exercise. Pain inten-
sity, pain area and index of McGill pain questionnaire were assessed and all were increased after exercise. DOMS was induced in the
shoulder muscles. PPT was significantly decreased and reached lowest values at 24 h. The muscle belly sites are more sensitive to
pain than the musculotendinous sites. No gender differences were found in any of the parameters used to assess the development
of DOMS. DOMS did not distribute evenly in the neck/shoulder region. Soreness after exercise in the neck and shoulder seems
not to be among the conditions that produce predominant musculoskeletal pain in females.
2004 European Federation of Chapters of the International Association for the Study of Pain. Published by Elsevier Ltd. All
rights reserved.
Keywords: Pressure pain threshold; Musculotendinous site; Muscle pain; Delayed onset muscle soreness; Gender differences
1090-3801/$30 2004 European Federation of Chapters of the International Association for the Study of Pain. Published by Elsevier Ltd. All rights
reserved.
doi:10.1016/j.ejpain.2004.12.009
654 H. Nie et al. / European Journal of Pain 9 (2005) 653–660
induction of DOMS because of convenience of exercise. human quantitative experimental study was to: (1)
It has been suggested that DOMS may be a result of induce DOMS in the neck and shoulder muscles (i.e.
muscle allodynia to pressure, hence indicating neural upper, middle and lower trapezius muscle; supraspinatus;
plastic change and hyperexcitability develop and con- infraspinatus; levator scapulae; cervical muscle); (2) com-
tribute to DOMS (Barlas et al., 2000). An endogenous pare the pressure pain sensitivity of muscle belly with that
model inducing pain in the neck–shoulder region might of musculotendinous tissue after DOMS; (3) examine for
be helpful to gain knowledge about the transduction, gender differences in development of DOMS.
transmission and processing of muscle pain and to test
the efficacy of interventional studies.
With respect to the localization of DOMS in muscle, 2. Material and methods
the area of the musculotendinous attachment of quadri-
ceps muscle are thought to be the main site of pain and 2.1. Subjects
tenderness during the initial phase of DOMS (Newham
et al., 1983). The pain spreads to the centre of the muscle A total of 12 male and 12 female healthy volunteers
by 48 h (Bobbert et al., 1986). It has been found that the without musculoskeletal problems during the last 3
PPT of muscle belly in the forearm was more sensitive to months participated in the study. The average age
DOMS than adjacent musculotendinous sites (Slater (mean ± SD) was 24.6 ± 3.4 years for the males and
et al., 2003). It is therefore not known if the soreness 24.1 ± 3.6 years for the females; the average height
is distributed generally throughout the muscle or iso- (mean ± SE) was 183.3 ± 2.0 cm for the males and
lated to specific areas. 169.3 ± 2.0 cm for the females; the average weight
Women are more likely to suffer more from musculo- (mean ± SE) was 78.9 ± 3.18 kg for the males and
skeletal pain than men (Strazdins and Bammer, 2004). It 61.4 ± 3.18 kg for the females. Informed consent was
appears that women are more sensitive to pain and obtained from each subject. None had participated in
incline to report greater pain to experimental muscle weight training in the past month. The study was ap-
pain conditions (Ge et al., 2004; Riley et al., 1998). Some proved by the local ethics committee and conducted in
previous studies found no significant difference between accordance with the Declaration of Helsinki.
male and female in the sensation and development of
DOMS after high-force eccentric exercise of elbow flex- 2.2. Protocol
or (High et al., 1989; Rinard et al., 2000). Others found
females tended to report less pain at 48 h after exercise A shoulder dynamometer (Aalborg University, Aal-
than males (Dannecker et al., 2003). It is not known if borg, Denmark) was used in the present experiment.
there are gender differences in DOMS on the neck/shoul- In addition, a plastic vest was worn by the subject to
der muscles. protect the low back muscles (Fig. 1). The experiment
With a newly designed shoulder dynamometer (Mad- consisted of three sessions (i.e. in three sequential days).
eleine et al., 2004), it is possible to perform eccentric exer- The right shoulder was exercised and the left shoulder
cise in the shoulder muscles. The aim of the present acted as control side. In the first session, pressure pain
Fig. 1. The shoulder dynamometer (left) and the PPT test sites (site 1–11; description see method) on the right neck/shoulder region (right).
H. Nie et al. / European Journal of Pain 9 (2005) 653–660 655
thresholds (PPT) were measured twice from the 13 test diameter of the contact tip was 10 mm and covered with
sites. Subjects familiarized themselves with the experi- 2 mm thick rubber. A standardized speed of pressure in-
mental procedures, including the static and dynamic crease of 30 kPa/s was kept constant during pressure
contraction (abduction, flexion of upper limb and shrug) application. The pain threshold was defined when the
and pain rating procedures. perception changed from pressure to pain. The instru-
ment was calibrated at the start of each session. All
2.2.1. Exercise procedure
the measurements were performed by the same person.
The subject sat upright with both arms resting in the
The subject sat on a seat without backrest. The PPT test
neutral position. The contact point between the dyna-
sites were located and marked. PPT was measured twice
mometer and the shoulder was 3 cm medial to acro-
at each test site. The mean of two measurements at the
mion. The subject was then fixed securely to the seat
test site was considered as PPT for this site. The PPT
by Velco strips. The subject raised both shoulders in
measurement started from dominant side following the
exercise in order to minimize lateral bending. (1) The
order of site number and continuing on the non-domi-
subject elevated his shoulder as high as possible without
nant side with same order, this procedure was then re-
lateral bend, and then the height was measured as top
peated to get two measurements from each site
position. The subject lowered his shoulder as low as pos-
(Fig. 1). The PPT after exercise was normalized to
sible; the height was measured as bottom position. The
PPT before exercise by subtraction to indicate the
distance between top and bottom position was defined
change after exercise.
as the range of shoulder elevation. (2) The maximum
voluntary contraction (MVC) force was measured by
asking the subject to exert the maximal force by elevat-
2.3.1. Localization of PPT test sites
ing his shoulder in neutral position (isometric contrac-
tion) against the dynamometer for 3 s. The maximal
1. Occiput: at the suboccipital muscle insertions.
value within 3 s was computed as MVC. Three repeated
2. Cervical muscle: processus transversus C5.
measures were done to get the mean value of MVC. (3)
3. Cervical myotendinous spot: processus transversus
The shoulder eccentric exercise was conducted by asking
C7.
the subject to elevate his shoulder against the downward
4. Upper trapezius: middle point of processus spinosus
moving force of 110% MVC. The dynamometer moved
C7 and acromion.
in the previously defined range of shoulder elevation
5. Levator scapulae: 2 cm superior to the angulus supe-
during exercise. Five 3 min eccentric exercise bouts with
rior scapulae.
3 min rest in between were performed.
6. Angulus superior scapulae.
Immediately after exercise, the PPT was measured
7. 1 cm medial to the acromioclavicular joint.
again. The pain intensity for the right shoulder during
8. Supraspinatus: 3 cm superior to the middle of spina
the static and dynamic contractions was rated. The static
scapulae.
contraction included: bilateral arm abduction at 90, arm
9. Infraspinatus: 3 cm distal to the middle of spina
flexion at 90 and shrug for 30 s. The dynamic contrac-
scapulae.
tion included arm abduction from 0 to 90, arm flexion
10. Middle trapezius: middle point of processus spino-
0 to 90 and repetitive shrug for five times during 10 s.
sus T4 and medial border of spina scapulae.
The visual analogue scale (VAS) was used to rate the
11. Lower trapezius: middle point of processus spinosus
intensity of pain. The mean pain intensity ratings for sta-
T6 and medial border of spina scapulae.
tic and dynamic contractions were used in the analysis.
12. 3 cm lateral of processus L3.
The McGill pain questionnaire was completed to assess
13. Tibialis anterior: 10 cm proximal to the lower rim of
the pain quality during contraction. The pain area
patella.
in the neck/shoulder region during shoulder muscle con-
traction was drawn on the body chart.
Sites 1, 3, 6, 7 were musculotendinous sites and sites 2, 4,
In the second and third sessions, PPT, pain ratings,
5, 8 were corresponding muscle belly sites. Site 12 was
McGill pain questionnaire and pain area drawings were
measured to examine the influence of load on the lum-
assessed.
bar muscle during shoulder exercise. Site 13 was a con-
All measurements were performed before exercise
trol site for repeated measure.
(pre), immediately after exercise (0 h), 24 h after exercise
(24 h) and 48 h after exercise (48 h).
2.3.2. Pain area drawing
2.3. Pressure pain threshold (PPT) The human body chart consisted of the whole body-
line diagrams. The circumference of the drawing on the
An electronic pressure algometer (Somedic Algom- chart was scanned and processed (ACECAD D9000+
eter type 2, Sweden) was used to measure PPTs. The digitizer, Taiwan), then the area was calculated.
656 H. Nie et al. / European Journal of Pain 9 (2005) 653–660
2.3.3. McGill pain questionnaire (MPQ) effect of time: F3,66 = 4.88, P < 0.01) but not for the con-
All subjects were asked to describe the quality of pain trol side. There was no significant difference in the gen-
with the validated Danish or English version of the der factor and interaction with other factors. PPT for
McGill pain questionnaire (MPQ). The total pain rating the exercise side was not significantly different from
index (PRI) was calculated from the rank of words cho- the control side before exercise. PPT change for the exer-
sen for the sensory, affective, evaluative and miscella- cise side was significantly different from the control side
neous sub-groups (Melzack, 1975). (time · side: F3,69 = 17.01, P < 0.001). The post hoc test
showed that there was significant decrease in PPT at 24
2.3.4. Muscle pain intensity and 48 h for the exercise side but not for the control side
The muscle pain intensity during shoulder muscle (SNK: P < 0.01; Fig. 2). There were significant differ-
contraction was assessed by using the VAS. The VAS ences between the test sites at the exercise side (main
consists of a 10 cm line anchored with ‘‘no pain’’ on effect of site: F12,276 = 15.16, P < 0.001). Significant de-
the left end and ‘‘extreme pain’’ on the right end. Sub- crease in PPT values was found in the site 1–8 compared
jects rated the perceived pain following static and dy- to pre-exercise (SNK: P < 0.05). PPT had no difference
namic contractions. between the musculotendinous and the muscle belly sites
before exercise. The normalized PPT data analysis
showed that PPTs for the muscle belly sites decreased
3. Statistical analysis more than those for the musculotendinous sites at 24 h
(ANOVA: F1,190 = 5.85, P = 0.016; Fig. 3).
The data are presented as mean and standard error
(±SE). The MVC force was tested using one-way analy- 4.3. Pain area
sis of variance (ANOVA). The PPT data were analysed
by a mixed model repeated-measures ANOVA with the There was a significant increase of pain area after
within group factors: time (pre, 0, 24 and 48 h), side exercise (24 h: 98 ± 15; 48 h: 38 ± 8 AU) (ANOVA:
(exercise and control) and site (13 test sites); the between F2,46 = 21.06, P < 0.001) and between the exercise and
group factor: gender (male and female). The repeated- the control side (24 h: 17 ± 9; 48 h: 8 ± 4 AU)
measures ANOVA was used to analyse PPT for the 13 (F1,23 = 49.85, P < 0.001). The post hoc test showed that
test sites of the exercise side (factors: time and sites), there was no increase of the pain area in the control side.
the PRI value (factors: time and sub-group) and the pain The pain areas of the exercise side at 0, 24 and 48 h were
area (factors: side and time) with genders as the between significantly larger than those of the control side (Fig. 4;
group factor. The pain intensity was analysed by Fried- SNK: P < 0.05). There was no significant difference be-
man test and Wilcoxon Signed Ranks Test as the post tween males and females.
hoc test. The normalized PPT data for musculotendi-
nous and muscle sites was evaluated by the two-way
ANOVA (test sites; gender) in order to compare sensi-
tivity of different site to DOMS and gender differences.
The Student–Newman–Keuls (SNK) test was used as
the post hoc test in case of significant factors. P < 0.05
was considered significant.
4. Results
5. Discussion
crease of pressure pain threshold after exercise was
The present study showed that DOMS could be in- prominent in muscle belly sites compared with myoten-
duced specifically in the neck/shoulder region. The de- dinous sites. There was no gender differences in any of
658 H. Nie et al. / European Journal of Pain 9 (2005) 653–660
the parameters used to assess the development of the actual induction procedure produced more pain than
DOMS. the delayed soreness (Barlas et al., 2000). This increased
pain may attribute to fatigue induced by the exercise
(Barlas et al., 2000). The relative low pain intensity
6. DOMS in the neck/shoulder region might due to the small range of shoulder motion and
small load during pain measurement. The range of the
The PPT is an effective index in measuring the extend shoulder eccentric exercise is not as large as that of the
of muscle tenderness and validated as a diagnostic method biceps brachii or quadriceps femoris. The change of
for the musculoskeletal disorders (Madeleine et al., muscle length was therefore small. It is believed that
1998; Nakata et al., 1993). An early subjective symptom the extent of muscle injury due to eccentric exercise is re-
of a pathophysiologic alteration of a skeletal muscle is lated more to the muscleÕs change in length rather than
increased tenderness (Mense, 1990). In the present study the amount of force generated by the muscle (Lieber and
the PPT decreased after exercise and reached its lowest Friden, 1993). Eccentric exercise performed at longer
level at 24 h. Correspondingly, the PRI of MPQ, pain muscle lengths causes more damage to the muscle than
area and pain intensity showed maximal response. All at shorter muscle lengths (Child et al., 1998; Newham
of these data supported the conclusion that DOMS et al., 1988). The pain intensity measured without load
was induced and located in the neck/shoulder region. on the shoulder may diminish the pain sensation because
It is consistent with the previous observation that pain after DOMS is obvious during muscle contraction.
DOMS develops usually in the first 24–48 h after unac- The lack of changes in MVC may due to the synergetic
customed exercise (Ebbeling and Clarkson, 1989). The effect of shoulder muscles (Halder et al., 2000).
significant decreases of PPTs were found in 8 of 11 test
sites situated on the upper and middle trapezius, levator
scapulae and supraspinatus muscles. There was no de- 7. Different sensitivity of muscle and myotendinous site to
crease in PPT on the scapula spine, infraspinatus and DOMS
lower trapezius, indicating that these muscles were prob-
ably not substantially involved under the current eccen- It is, to date, not clear whether the eccentric exercise
tric shoulder exercise setting. The eccentric shoulder produces muscle damage and soreness uniformly over
exercise without raising arms resulted in elevation and the muscle or in the specific area of the muscle, due per-
upward rotation of scapula. The main agonist in these haps to susceptible weaker structural components (Ba-
movements are levator scapulae and upper trapezius ker et al., 1997). In the present study, it was found
(Brukner and Khan, 1993) although other muscles con- that the PPTs for the muscle belly sites decreased more
tribute to a lower extent. The increased tenderness may than the myotendinous sites after exercise. The results
due to the acute damage to the muscle fibres during are in contrast to those of Newham et al. (1983) where
exercise, causing mechanical disruption of the ultra- the initial tenderness was primarily located at the distal,
structural elements within the muscle fibres such as the medial and lateral parts of the quadriceps, but at peak
Z-line and contractile filaments (Friden et al., 1983; intensity of soreness the muscle-tendon region was not
Waterman-Storer, 1991). Release of the inflammatory more prone to soreness than others muscle sites. Cleak
mediators in the acute inflammation resulting from an and Eston (1992) reported that tenderness at the proxi-
immune response to the initial injury may sensitize mus- mal myotendinous junction of the biceps was signifi-
cle nociceptors and lower their threshold to mechanical cantly less than the distal myotendinous junction and
stimuli leading to increased pain sensation. (Mense, at the mid belly after strenuous eccentric exercise (Cleak
1990; Smith, 1991). Barlas et al. (2000) suggested that and Eston, 1992). Baker et al. (1997) reported that the
muscle allodynia observed in DOMS may relate to a pressure pain tolerance of myotendinous sites was lower
central mechanism besides sensitization of the peripheral than that of the muscle belly in the same quadriceps
nociceptors. The pain following eccentric exercise was femoris after eccentric down-hill running. Compared
only present when the muscles were stretched or con- to the pressure pain tolerance before the exercise, the
tract or palpated but not in rest. The most chosen words pressure pain tolerance decreased more in the muscle
in the MPQ were ‘‘sore’’ and ‘‘tender’’ which in the sen- belly site than in the myotendinous site when DOMS
sory sub-group, showing the influence of DOMS was reached the peak levels. The present results may due
mainly on the sensation aspect of pain. This is in agree- to the discrete damage of eccentric exercise to the myo-
ment with the observation of DOMS in the first interos- tendinous part and muscle belly. It has been found that
seous muscle (Bajaj et al., 2001). It was found in the even in one muscle suffering from DOMS the decrease of
present study that the relatively higher PRI and pain pain threshold was not distributed evenly (Weerakkody
intensity rating appeared immediately after exercise. et al., 2001), suggesting that the foci of damage underly-
This phenomenon also occurred in elbow flexor after ing the soreness were discrete and separated by regions
eccentric contractions where most subjects reported that of the uninjured muscle.
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