European Journal of Pain 9 (2005) 653–660 www.EuropeanJournalPain.

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Delayed onset muscle soreness in neck/shoulder muscles
Hongling Nie, Adam Kawczynski, Pascal Madeleine *, Lars Arendt-Nielsen
Laboratory for Experimental Pain Research, Center for Sensory-Motor Interaction, Aalborg University, Fredrik Bajers Vej 7D-3, DK-9220 Aalborg, Denmark Available online 2 February 2005

Abstract The aim of the present study is to: (1) induce delayed onset muscle soreness (DOMS) in the neck and shoulder muscles; (2) compare the pressure pain sensitivity of muscle belly with that of musculotendinous tissue after DOMS; (3) examine the gender differences 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 period 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 intensity, 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. Ó 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

1. Introduction Work related musculoskeletal disorders are a significant problem in the working populations (Buckle and Devereux, 2002). Musculoskeletal disorders commonly affect the neck and shoulder region with sign of muscle pain and soreness (Armstrong et al., 1993). Delayed onset muscle soreness (DOMS) which occurs after unaccustomed exercise enables to study mechanisms related to neck and shoulder pain. Previous studies show that eccentric exercise, i.e. lengthening of the contracting muscle, produces prominent soreness (Bajaj et al., 2001; Jones et al., 1987; Newham et al., 1987). Although
*

Corresponding author. Tel.: +45 96 35 88 33; fax: +45 98 15 40 08. E-mail address: pm@smi.aau.dk (P. Madeleine).

the underlying mechanisms of DOMS are not clearly understood, it has been suggested that soreness may due to the damage of muscle structure during exercise; furthermore, it may be exacerbated and maintained by the subsequently acute inflammatory reaction in muscle evoked by the release of biochemical substances after disruption of the muscle fibres and connective tissue (Armstrong, 1984; Newham et al., 1987). Delayed muscle soreness usually develops 24–48 h following exercise and is described as dull and tender (Armstrong, 1984; Armstrong et al., 1983). The sensation usually subsides within 5–7 days after exercise (Ebbeling and Clarkson, 1989). Biceps brachii (Dannecker et al., 2002; Jones et al., 1987), quadriceps femoris (Baker et al., 1997; Newham et al., 1983) and dorsal interosseous muscle (Bajaj et al., 2001) are the most targeted muscles in the

1090-3801/$30 Ó 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

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induction of DOMS because of convenience of exercise. It has been suggested that DOMS may be a result of muscle allodynia to pressure, hence indicating neural plastic change and hyperexcitability develop and contribute to DOMS (Barlas et al., 2000). An endogenous model inducing pain in the neck–shoulder region might be helpful to gain knowledge about the transduction, transmission and processing of muscle pain and to test the efficacy of interventional studies. With respect to the localization of DOMS in muscle, the area of the musculotendinous attachment of quadriceps muscle are thought to be the main site of pain and tenderness during the initial phase of DOMS (Newham et al., 1983). The pain spreads to the centre of the muscle by 48 h (Bobbert et al., 1986). It has been found that the PPT of muscle belly in the forearm was more sensitive to DOMS than adjacent musculotendinous sites (Slater et al., 2003). It is therefore not known if the soreness is distributed generally throughout the muscle or isolated to specific areas. Women are more likely to suffer more from musculoskeletal pain than men (Strazdins and Bammer, 2004). It appears that women are more sensitive to pain and incline to report greater pain to experimental muscle pain conditions (Ge et al., 2004; Riley et al., 1998). Some previous studies found no significant difference between male and female in the sensation and development of DOMS after high-force eccentric exercise of elbow flexor (High et al., 1989; Rinard et al., 2000). Others found females tended to report less pain at 48 h after exercise than males (Dannecker et al., 2003). It is not known if there are gender differences in DOMS on the neck/shoulder muscles. With a newly designed shoulder dynamometer (Madeleine et al., 2004), it is possible to perform eccentric exercise in the shoulder muscles. The aim of the present

human quantitative experimental study was to: (1) induce DOMS in the neck and shoulder muscles (i.e. upper, middle and lower trapezius muscle; supraspinatus; infraspinatus; levator scapulae; cervical muscle); (2) compare the pressure pain sensitivity of muscle belly with that of musculotendinous tissue after DOMS; (3) examine for gender differences in development of DOMS.

2. Material and methods 2.1. Subjects A total of 12 male and 12 female healthy volunteers without musculoskeletal problems during the last 3 months participated in the study. The average age (mean ± SD) was 24.6 ± 3.4 years for the males and 24.1 ± 3.6 years for the females; the average height (mean ± SE) was 183.3 ± 2.0 cm for the males and 169.3 ± 2.0 cm for the females; the average weight (mean ± SE) was 78.9 ± 3.18 kg for the males and 61.4 ± 3.18 kg for the females. Informed consent was obtained from each subject. None had participated in weight training in the past month. The study was approved by the local ethics committee and conducted in accordance with the Declaration of Helsinki. 2.2. Protocol A shoulder dynamometer (Aalborg University, Aalborg, Denmark) was used in the present experiment. In addition, a plastic vest was worn by the subject to protect the low back muscles (Fig. 1). The experiment consisted of three sessions (i.e. in three sequential days). The right shoulder was exercised and the left shoulder 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).

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thresholds (PPT) were measured twice from the 13 test sites. Subjects familiarized themselves with the experimental procedures, including the static and dynamic contraction (abduction, flexion of upper limb and shrug) and pain rating procedures. 2.2.1. Exercise procedure The subject sat upright with both arms resting in the neutral position. The contact point between the dynamometer and the shoulder was 3 cm medial to acromion. The subject was then fixed securely to the seat by VelcoÒ strips. The subject raised both shoulders in exercise in order to minimize lateral bending. (1) The subject elevated his shoulder as high as possible without lateral bend, and then the height was measured as top position. The subject lowered his shoulder as low as possible; the height was measured as bottom position. The distance between top and bottom position was defined 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 elevating his shoulder in neutral position (isometric contraction) against the dynamometer for 3 s. The maximal value within 3 s was computed as MVC. Three repeated measures were done to get the mean value of MVC. (3) The shoulder eccentric exercise was conducted by asking the subject to elevate his shoulder against the downward moving force of 110% MVC. The dynamometer moved in the previously defined range of shoulder elevation during exercise. Five 3 min eccentric exercise bouts with 3 min rest in between were performed. Immediately after exercise, the PPT was measured again. The pain intensity for the right shoulder during the static and dynamic contractions was rated. The static contraction included: bilateral arm abduction at 90°, arm flexion at 90° and shrug for 30 s. The dynamic contraction included arm abduction from 0° to 90°, arm flexion 0° to 90° and repetitive shrug for five times during 10 s. The visual analogue scale (VAS) was used to rate the intensity of pain. The mean pain intensity ratings for static and dynamic contractions were used in the analysis. The McGill pain questionnaire was completed to assess the pain quality during contraction. The pain area in the neck/shoulder region during shoulder muscle contraction was drawn on the body chart. In the second and third sessions, PPT, pain ratings, McGill pain questionnaire and pain area drawings were assessed. All measurements were performed before exercise (pre), immediately after exercise (0 h), 24 h after exercise (24 h) and 48 h after exercise (48 h). 2.3. Pressure pain threshold (PPT) An electronic pressure algometer (SomedicÒ Algometer type 2, Sweden) was used to measure PPTs. The

diameter of the contact tip was 10 mm and covered with 2 mm thick rubber. A standardized speed of pressure increase of 30 kPa/s was kept constant during pressure application. The pain threshold was defined when the perception changed from pressure to pain. The instrument was calibrated at the start of each session. All the measurements were performed by the same person. The subject sat on a seat without backrest. The PPT test sites were located and marked. PPT was measured twice at each test site. The mean of two measurements at the test site was considered as PPT for this site. The PPT measurement started from dominant side following the order of site number and continuing on the non-dominant side with same order, this procedure was then repeated to get two measurements from each site (Fig. 1). The PPT after exercise was normalized to PPT before exercise by subtraction to indicate the change after exercise.

2.3.1. Localization of PPT test sites 1. Occiput: at the suboccipital muscle insertions. 2. Cervical muscle: processus transversus C5. 3. Cervical myotendinous spot: processus transversus C7. 4. Upper trapezius: middle point of processus spinosus C7 and acromion. 5. Levator scapulae: 2 cm superior to the angulus superior scapulae. 6. Angulus superior scapulae. 7. 1 cm medial to the acromioclavicular joint. 8. Supraspinatus: 3 cm superior to the middle of spina scapulae. 9. Infraspinatus: 3 cm distal to the middle of spina scapulae. 10. Middle trapezius: middle point of processus spinosus T4 and medial border of spina scapulae. 11. Lower trapezius: middle point of processus spinosus T6 and medial border of spina scapulae. 12. 3 cm lateral of processus L3. 13. Tibialis anterior: 10 cm proximal to the lower rim of patella. Sites 1, 3, 6, 7 were musculotendinous sites and sites 2, 4, 5, 8 were corresponding muscle belly sites. Site 12 was measured to examine the influence of load on the lumbar muscle during shoulder exercise. Site 13 was a control site for repeated measure.

2.3.2. Pain area drawing The human body chart consisted of the whole bodyline diagrams. The circumference of the drawing on the chart was scanned and processed (ACECAD D9000+ digitizer, Taiwan), then the area was calculated.

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2.3.3. McGill pain questionnaire (MPQ) All subjects were asked to describe the quality of pain with the validated Danish or English version of the McGill pain questionnaire (MPQ). The total pain rating index (PRI) was calculated from the rank of words chosen for the sensory, affective, evaluative and miscellaneous sub-groups (Melzack, 1975). 2.3.4. Muscle pain intensity The muscle pain intensity during shoulder muscle contraction was assessed by using the VAS. The VAS consists of a 10 cm line anchored with ‘‘no pain’’ on the left end and ‘‘extreme pain’’ on the right end. Subjects rated the perceived pain following static and dynamic contractions.

3. Statistical analysis The data are presented as mean and standard error (±SE). The MVC force was tested using one-way analysis of variance (ANOVA). The PPT data were analysed by a mixed model repeated-measures ANOVA with the within group factors: time (pre, 0, 24 and 48 h), side (exercise and control) and site (13 test sites); the between group factor: gender (male and female). The repeatedmeasures ANOVA was used to analyse PPT for the 13 test sites of the exercise side (factors: time and sites), the PRI value (factors: time and sub-group) and the pain area (factors: side and time) with genders as the between group factor. The pain intensity was analysed by Friedman test and Wilcoxon Signed Ranks Test as the post hoc test. The normalized PPT data for musculotendinous and muscle sites was evaluated by the two-way ANOVA (test sites; gender) in order to compare sensitivity 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.

effect of time: F3,66 = 4.88, P < 0.01) but not for the control side. There was no significant difference in the gender factor and interaction with other factors. PPT for the exercise side was not significantly different from the control side before exercise. PPT change for the exercise side was significantly different from the control side (time · side: F3,69 = 17.01, P < 0.001). The post hoc test showed that there was significant decrease in PPT at 24 and 48 h for the exercise side but not for the control side (SNK: P < 0.01; Fig. 2). There were significant differences between the test sites at the exercise side (main effect of site: F12,276 = 15.16, P < 0.001). Significant decrease in PPT values was found in the site 1–8 compared to pre-exercise (SNK: P < 0.05). PPT had no difference between the musculotendinous and the muscle belly sites before exercise. The normalized PPT data analysis showed that PPTs for the muscle belly sites decreased more than those for the musculotendinous sites at 24 h (ANOVA: F1,190 = 5.85, P = 0.016; Fig. 3). 4.3. Pain area There was a significant increase of pain area after exercise (24 h: 98 ± 15; 48 h: 38 ± 8 AU) (ANOVA: F2,46 = 21.06, P < 0.001) and between the exercise and the control side (24 h: 17 ± 9; 48 h: 8 ± 4 AU) (F1,23 = 49.85, P < 0.001). The post hoc test showed that there was no increase of the pain area in the control side. The pain areas of the exercise side at 0, 24 and 48 h were significantly larger than those of the control side (Fig. 4; SNK: P < 0.05). There was no significant difference between males and females.

4. Results 4.1. Maximal voluntary contraction force The MVC for males (743.2 ± 61.7 N) was significantly higher than that for females (341.2 ± 61.7 N) (ANOVA: F1,22 = 21.25, P < 0.001). There was no difference in MVC between three sessions. 4.2. Pressure pain threshold There was a significant difference between exercise and control side (ANOVA: F1,22 = 16.86, P < 0.001). There was a significant decrease of PPT after exercise, peaking at 24 h after exercise for the exercise side (main
Fig. 2. Mean PPT of eight test sites on the exercise side and the control side at before, immediately after, 24 and 48 h after exercise (n = 24, 12 male and 12 female). (*) Significant difference compared with preexercise (P < 0.05). (+) Significant difference between the exercise side and the control side (P < 0.05).

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Fig. 3. Decrease of PPT in the musculotendinous sites (site 1, 3, 6, 7) and the muscle belly sites (site 2, 4, 5, 8) at before, immediately after, 24 and 48 h after exercise (n = 24, 12 male and 12 female). (+) Significant difference between the musculotendinous sites and the muscle belly sites (P < 0.05).

4.4. McGill pain questionnaire ratings Before the exercise no pain descriptors were chosen in the MPQ. Statistical analysis showed increase in the PRI for the sub-groups (ANOVA: F3,66 = 46.29, P < 0.001; Fig. 4), time levels (F2,44 = 6.31, P < 0.01) and the interaction between PRI and the time levels (F6,132 = 4.74, P < 0.001). The PRI ratings were higher at 0 h than those at all the other times in sensory sub-group (SNK: P < 0.001). The PRI sensory ratings increased at 24 and 48 h compared to pre-exercise (SNK: P < 0.001). The PRI sensory ratings were higher than those of the affective, evaluative and miscellaneous sub-groups at all times after exercise (SNK: P < 0.001). The most chosen word was ‘‘tiring’’ (45.8% of subjects) at 0 h, ‘‘sore’’ (58.3% of subjects) at 24 h and ‘‘tender’’ (33.3%) at 48 h. There was no significant difference between males and females. 4.5. Muscle pain intensity The pain intensity significantly increased after eccentric exercise from 0 to 48 h (Friedman: v2 = 19.8, P < 0.001; Wilcoxon: P < 0.05; Fig. 4). There was no difference in the VAS score between immediately after and 24 h. The pain intensity was higher at 24 h compared with 48 h (P < 0.05). There was no significant difference between males and females. No pain sensation was reported during rest at 0, 24 and 48 h.

Fig. 4. The pain area of exercise side and control side assessed during contraction (upper), pain rating index of the McGill pain questionnaire sub-groups (middle) and mean pain intensity (VAS: 0–100 mm) during contraction (lower) at before, immediately after, 24 and 48 h after exercise (n = 24, 12 male and 12 female). (*) Significant difference compared with pre-exercise (P < 0.05). (+) Significant difference between the exercise side and the control side or between the sensory group and the other groups (P < 0.05).

5. Discussion The present study showed that DOMS could be induced specifically in the neck/shoulder region. The decrease of pressure pain threshold after exercise was prominent in muscle belly sites compared with myotendinous sites. There was no gender differences in any of

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the parameters used to assess the development of DOMS.

6. DOMS in the neck/shoulder region The PPT is an effective index in measuring the extend of muscle tenderness and validated as a diagnostic method for the musculoskeletal disorders (Madeleine et al., 1998; Nakata et al., 1993). An early subjective symptom of a pathophysiologic alteration of a skeletal muscle is increased tenderness (Mense, 1990). In the present study the PPT decreased after exercise and reached its lowest level at 24 h. Correspondingly, the PRI of MPQ, pain area and pain intensity showed maximal response. All of these data supported the conclusion that DOMS was induced and located in the neck/shoulder region. It is consistent with the previous observation that DOMS develops usually in the first 24–48 h after unaccustomed exercise (Ebbeling and Clarkson, 1989). The 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 decrease in PPT on the scapula spine, infraspinatus and lower trapezius, indicating that these muscles were probably not substantially involved under the current eccentric shoulder exercise setting. The eccentric shoulder exercise without raising arms resulted in elevation and upward rotation of scapula. The main agonist in these movements are levator scapulae and upper trapezius (Brukner and Khan, 1993) although other muscles contribute to a lower extent. The increased tenderness may due to the acute damage to the muscle fibres during exercise, causing mechanical disruption of the ultrastructural elements within the muscle fibres such as the Z-line and contractile filaments (Friden et al., 1983; Waterman-Storer, 1991). Release of the inflammatory mediators in the acute inflammation resulting from an immune response to the initial injury may sensitize muscle nociceptors and lower their threshold to mechanical stimuli leading to increased pain sensation. (Mense, 1990; Smith, 1991). Barlas et al. (2000) suggested that muscle allodynia observed in DOMS may relate to a central mechanism besides sensitization of the peripheral nociceptors. The pain following eccentric exercise was only present when the muscles were stretched or contract or palpated but not in rest. The most chosen words in the MPQ were ‘‘sore’’ and ‘‘tender’’ which in the sensory sub-group, showing the influence of DOMS was mainly on the sensation aspect of pain. This is in agreement with the observation of DOMS in the first interosseous muscle (Bajaj et al., 2001). It was found in the present study that the relatively higher PRI and pain intensity rating appeared immediately after exercise. This phenomenon also occurred in elbow flexor after eccentric contractions where most subjects reported that

the actual induction procedure produced more pain than 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 might due to the small range of shoulder motion and small load during pain measurement. The range of the shoulder eccentric exercise is not as large as that of the biceps brachii or quadriceps femoris. The change of muscle length was therefore small. It is believed that the extent of muscle injury due to eccentric exercise is related more to the muscleÕs change in length rather than the amount of force generated by the muscle (Lieber and Friden, 1993). Eccentric exercise performed at longer muscle lengths causes more damage to the muscle than at shorter muscle lengths (Child et al., 1998; Newham et al., 1988). The pain intensity measured without load on the shoulder may diminish the pain sensation because pain after DOMS is obvious during muscle contraction. The lack of changes in MVC may due to the synergetic effect of shoulder muscles (Halder et al., 2000).

7. Different sensitivity of muscle and myotendinous site to DOMS It is, to date, not clear whether the eccentric exercise produces muscle damage and soreness uniformly over the muscle or in the specific area of the muscle, due perhaps to susceptible weaker structural components (Baker et al., 1997). In the present study, it was found that the PPTs for the muscle belly sites decreased more than the myotendinous sites after exercise. The results are in contrast to those of Newham et al. (1983) where the initial tenderness was primarily located at the distal, medial and lateral parts of the quadriceps, but at peak intensity of soreness the muscle-tendon region was not more prone to soreness than others muscle sites. Cleak and Eston (1992) reported that tenderness at the proximal myotendinous junction of the biceps was significantly less than the distal myotendinous junction and at the mid belly after strenuous eccentric exercise (Cleak and Eston, 1992). Baker et al. (1997) reported that the pressure pain tolerance of myotendinous sites was lower than that of the muscle belly in the same quadriceps femoris after eccentric down-hill running. Compared to the pressure pain tolerance before the exercise, the pressure pain tolerance decreased more in the muscle belly site than in the myotendinous site when DOMS reached the peak levels. The present results may due to the discrete damage of eccentric exercise to the myotendinous part and muscle belly. It has been found that even in one muscle suffering from DOMS the decrease of pain threshold was not distributed evenly (Weerakkody et al., 2001), suggesting that the foci of damage underlying the soreness were discrete and separated by regions of the uninjured muscle.

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8. Sex difference in DOMS In the present study, no gender differences was found in change of PPT, pain intensity rating, PRI of McGill pain questionnaire and pain area. Previous studies showed equivocal results with respect to sex difference in DOMS. There was no difference between genders in the soreness rating for eccentric exercise of the leg (High et al., 1989; MacIntyre et al., 2000) and the elbow flexors (Poudevigne et al., 2002; Rinard et al., 2000). Another study found that females reported less pain than males at 48 h after eccentric resistance exercise (Dannecker et al., 2003). The differences in the pain intensity rating between men and women may be due to different dependent variables (soreness or pain) and different time periods of data collection (Dannecker et al., 2003). Although different methodologies were used in those studies, most of them tailored the exercise intensity to personal maximum contraction strength level as done in the present study. Therefore the damage to the muscle after the exercise was likely to be similar between men and women in the present study. The lack of difference in decrease of PPT reflected that the tenderness of muscle after DOMS was induced similarly in men and women. These results were in agreement with results of previous studies (Dannecker et al., 2003). The present study used a novel apparatus to induce DOMS in the neck/shoulder region and the results indicated that males and females were equally susceptible to the exercise-induced muscle damage in the neck/shoulder muscles. The mechanisms underlying DOMS might be different from that of chronic musculoskeletal pain in the neck/shoulder region where females have a higher prevalence of chronic pain. Too low pain intensity evolved by DOMS in the present study might be an alternative reason for the lack of gender differences. The present endogenous model might in the future provide quantitative data regarding the efficacy of intervention studies.

Acknowledgement This work was financially supported by Norma og Frode S. Jacobsens Fond.

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