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Pressure Pain Sensitivity Mapping in Experimentally Induced Lateral Epicondylalgia

FERNÁNDEZ-CARNERO, JOSUÉ1,2; BINDERUP, ASBJØRN T.1; GE, HONG-YOU2; FERNÁNDEZ-DE-LAS-PEÑAS, CÉSAR1,2; ARENDT-NIELSEN, LARS1; MADELEINE, PASCAL1

Medicine & Science in Sports & Exercise: May 2010 - Volume 42 - Issue 5 - p 922-927
doi: 10.1249/MSS.0b013e3181c29eab
BASIC SCIENCES

Purpose: The aim of this study was to apply topographical techniques to investigate changes in pressure pain sensitivity after induction of delayed onset muscle soreness (DOMS) in the elbow region in healthy subjects.

Methods: Pressure pain thresholds (PPT) were assessed over 12 points forming a 3 × 4 matrix (4 points in the superior part, 4 points in the middle, and 4 points in the lower part around the lateral epicondyle) over the dominant elbow in 13 healthy men, and pressure sensitivity maps were calculated. DOMS, as a model for lateral epicondylalgia (LE), was induced by repetitive high-level eccentric contractions of the wrist extensor muscles. PPT maps were assessed before, immediately after, and 24 h after eccentric exercise (DOMS).

Results: The two-way repeated-measure ANOVA detected significant differences in mean PPT for the measurement points (F = 5.96, P < 0.001), with lower PPT over the points located over the extensor carpi radialis brevis muscle. There was also a significant effect of time (F = 121.3, P < 0.001) but no time × point location interaction (F = 0.7, P = 0.8). PPT were lower 24 h after (P < 0.001) but not immediately after (P > 0.05) eccentric exercise.

Conclusions: The study provides new key information regarding mechanical pain hyperalgesia in experimentally induced LE. Topographical pressure pain sensitivity maps from the elbow region revealed heterogeneously distributed mechanical sensitivity before and during DOMS. The most sensitive localizations for PPT assessment correspond to the muscle belly of the extensor carpi radialis brevis. Our results support the implication of the extensor carpi radialis brevis muscle in LE.

1Department of Health Science and Technology, Center for Sensory-Motor Interaction (SMI), Aalborg University, Aalborg, DENMARK; and 2Department of Physical Therapy, Occupational Therapy, Physical Medicine and Rehabilitation, Universidad Rey Juan Carlos, Alcorcón, Madrid, SPAIN

Address for correspondence: Pascal Madeleine, Ph.D., Department of Health Science and Technology, Center for Sensory-Motor Interaction (SMI), Aalborg University, Fredrik Bajers Vej 7 D-3, DK-9220, Aalborg, Denmark; E-mail: pm@hst.aau.dk, URL: www.smi.hst.aau.dk.

Submitted for publication May 2009.

Accepted for publication September 2009.

Elbow injuries are frequent in sports with overhead or repetitive arm movements (20). Lateral epicondylalgia (LE) is a common elbow injury, with an annual incidence between 1% and 3% in the general population and up to 10% among women around 40 yr of age (26). LE may occur after unaccustomed or high-intensity repetitive movements such as tennis and golf. Although the pathophysiology is still unknown, there is a general agreement that the extensor carpi radialis brevis (ECRB) muscle most likely plays a relevant role in the development of LE (21). In clinical settings, patients with LE usually suffer from pain located around the elbow region and mechanical hyperalgesia in the common extensor origin (30,33). Further, most patients also report pain referring to the dorsal forearm (11).

Physical activity involving repetitive eccentric contractions leads to damage in the muscles (16,17). Delayed onset muscle soreness (DOMS), which occurs after unaccustomed eccentric exercise, allows the possibility of studying mechanisms related to elbow pain. Although the underlying mechanisms of DOMS are not completely understood, it has been suggested that soreness may be due to the damage of muscle structure during the exercise maintained by an inflammatory reaction in the muscle tissue by the release of proinflammatory substances after disruption of the muscle fibers and connective tissue after the exercise (5,9,23). In addition, it has previously been demonstrated that the effects of DOMS in the ECRB induce sensory and motor changes similar to those reported in patients with clinical LE (29). Thus, the induction of DOMS in the wrist extensor muscles can be considered as a model of LE (29).

We have recently reported that mechanical hyperalgesia, contrary to thermal hyperalgesia, is a characteristic of LE (13). In addition, widespread mechanical pain hypersensitivity has also been reported in unilateral LE (12). This suggests that this type of injury is characterized by deep muscle tissue hypersensitivity. Slater et al. (29) have shown that the muscle belly location has increased mechanical pain sensitivity when compared with adjacent musculotendinous sites after the induction of DOMS in the wrist extensor muscles. However, the spatial distribution of mechanical hypersensitivity in LE has not yet been studied.

The mapping of pressure pain sensitivity in the elbow will thus provide information about muscles and sites that are most likely affected in experimentally induced LE. For this purpose, we applied topographical techniques to obtain pressure pain sensitivity maps of the elbow region in healthy subjects and evaluated the changes in pressure pain sensitivity maps after the development of DOMS in the wrist extensor muscles as a model of LE (29). We hypothesized a nonuniform distribution of the pressure pain sensitivity over the elbow area. Because the ECRB seems to play a relevant role in LE, we also expected that pressure pain sensitivity of this muscle would be greater than the remaining part of the elbow region.

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MATERIALS AND METHODS

Subjects.

Thirteen healthy men (mean age = 24.3 ± 3.2 yr, body mass = 73.5 ± 13.4 kg, height = 175 ± 7 cm) with no signs or symptoms of musculoskeletal pain and who responded to a public announcement participated in the study. All subjects were right-handed. The exclusion criteria were having any complaints in the upper limb or neck in the last 12 months and regular intake of any medication. A physical examination was conducted to check that all participants had full pain-free range of elbow and wrist motion and no abnormal tenderness to palpation of soft tissues in the extensor muscles around the forearm and wrist. The study was approved by the local ethics committee (VN-2007/0019) and conducted following the Declaration of Helsinki. Informed consent was obtained from all the participants.

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Delayed onset muscle soreness (DOMS).

DOMS was induced by repeated eccentric wrist extension contractions in the dominant arm following previous guidelines (28,29). Participants were seated with their dominant forearm stabilized on a table using a vacuum pillow (Ambu, Kristianstad, Sweden). The elbow was extended and the forearm pronated. Before eccentric exercise, the maximum voluntary contraction (MVC) was recorded in static conditions. The maximum wrist extension force was measured using a piezoelectric force transducer (Kistler type 9311A, Bern, Switzerland), hooked to a strap placed on the back of the hand over the distal part of the metacarpal bones. Three trials were made to determine MVC. Participants were instructed to perform maximal wrist extension throughout the eccentric exercise period. The total exercise period was set to 25 min, divided into five bouts of 5 min. The initial exercise bout was performed at 70% MVC, and each subsequent bout was done with a 5% MVC decrement ending at 50% MVC for the final bout. Each bout was separated by a 1-min rest. The progressive decrease in the level of eccentric exercise was applied to avoid excessive fatigue after a few bouts.

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Assessment of deep tissue pain sensitivity.

Pressure pain threshold (PPT) levels were assessed using a pressure algometer at an application rate of 30 kPa·s−1 (Somedic©, Sollentuna, Sweden). The PPT was defined as the minimum pressure that evoked pain. The algometer consisted of a 1-cm2 rubber tip plunger mounted on a force transducer. PPT were measured three times for each location in random order, and the mean value was used for statistical analyses. PPT levels were assessed over 12 points forming a 3 × 4 matrix (4 points in the superior part, 4 points in the middle, and 4 points in the lower part around the lateral epicondyle) as follows: the lateral epicondyle was taken as the reference point (point 5). A line downward from the lateral epicondyle was defined as the central column of the map. In this way, three vertical points separated by 20 mm were marked (labeled 6, 7, and 8). These four points were used for defining the remaining two columns of the matrix. The remaining points were symmetrically located 20 mm anterior (points 1-4) and 20 mm posterior (points 9-12) to each respective point (Fig. 1). Points 1-4 corresponded to the anatomical location of the musculotendinous junction (point 1) and muscle belly (points 2-4) of the ECRB, points 5-8 to the anatomical projection of the musculotendinous junction (point 6) and muscle belly (points 7 and 8) of the extensor digitorum communis, and points 9-12 to the location of the musculotendinous junction (point 9) and muscle belly (points 10-12) of the extensor carpi ulnaris muscle.

FIGURE 1

FIGURE 1

Averaged PPT over the 12 points were interpolated using an inverse distance weighted interpolation (27) for graphical purposes to have a topographical reading of the PPT level distribution over the region. The inverse distance weighted interpolation consists of computing PPT values of unknown locations by summarizing the known PPT values and weight them according to their distance to the unknown location (7). Topographical pressure pain sensitivity maps were assessed before, immediately after, and 24 h after the eccentric exercise using pressure algometry. In addition, the differences in PPT immediately after and 24 h after the exercise with respect to the before exercise values were calculated to compare changes over time.

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Statistical analysis.

Data were analyzed with the SPSS© version 14.0 (SPSS Inc., Chicago, IL). Data are expressed as means, standard deviation, and 95% confidence interval. MVC and topographical pressure pain sensitivity maps over the elbow region were calculated with a one-way ANOVA. A two-way repeated-measure ANOVA with time (before, immediately after, and 24 h after exercise) and point (from 1 to 12) as within-subject factors was used to assess changes in PPT due to DOMS. Post hoc comparisons were performed with the Bonferroni test. The statistical analysis was conducted at 95% confidence level, and a P < 0.05 was considered statistically significant.

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RESULTS

MVC were significantly lower at 24 h after exercise compared with before exercise (F = 8.2, P < 0.05), respectively, 227.6 ± 45.1 versus 260.0 ± 39.2 N.

The ANOVA detected significant differences in mean PPT for the measurement points (F = 5.96, P < 0.001). Post hoc comparisons revealed 1) lower PPT over points 2-4 (ECRB muscle) when compared with PPT over points 10-12 (extensor carpi ulnaris muscle, P < 0.01); 2) PPT over point 5 (lateral epicondyle) was higher (P < 0.05) than PPT over point 3 (muscle belly of the ECRB muscle); and 3) lower PPT over points 7 and 8 (extensor digitorum communis muscle) compared with PPT over points 11-12 (P < 0.05) (Table 1, Fig. 2A).

TABLE 1

TABLE 1

FIGURE 2

FIGURE 2

The two-way repeated-measure ANOVA revealed a significant effect for time (F = 121.3, P < 0.001) but no time × point interaction (F = 0.7, P = 0.8). Post hoc test revealed that PPT were lower 24 h (P < 0.001, Fig. 2C) but not immediately (P > 0.05, Fig. 2B) after the eccentric exercise (Table 1) in all the assessed points (Fig. 3).

FIGURE 3

FIGURE 3

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DISCUSSION

The study provides new key information regarding mechanical pain hyperalgesia in experimentally induced LE and demonstrated that mechanical sensitivity is heterogeneously distributed over the wrist extensor muscles prior and during DOMS. We also found that the most sensitive localizations for PPT assessment were found in points corresponding to the muscle belly of the ECRB.

The significant increase in pressure pain sensitivity, that is, hyperalgesia observed 24 h after the eccentric exercise and strength loss in the current study, confirmed the presence of DOMS in line with previous studies (9,19,24). These results also correspond to the report that DOMS is found to develop gradually over a period of 24-48 h (3,4). The hyperalgesia observed could be due to the acute damage to the muscle fibers during exercise, causing mechanical disruption of the ultrastructural elements within the muscle fibers such as the Z-line and contractile filaments (9,16,17). The release of inflammatory mediators can sensitize muscle nociceptors and lower their threshold to mechanical stimuli, leading to increased pain sensation (25). This is being disputed by Yu et al. (34) and Malm et al. (22), who did not find disruption of the myofibrillar apparatus in the human muscle and found no evidence for a skeletal muscle inflammation. These results are supported by a recent study providing evidence of a lack of muscle inflammation and a more potent role of the extracellular matrix in relation to DOMS (9).

We have recently demonstrated the utility of multiple site recordings for PPT mapping leading to a new imaging modality of muscle pain sensitivity (1,14,15,31). The technique enables visualization of nonuniform muscle pressure pain sensitivity as reported in chronic headaches (14,15) and musculoskeletal pain (18,24). The current study is the first one investigating topographical pressure pain sensitivity maps in a common region of sports injuries, that is, the elbow. Moreover, it confirmed that this new imaging technique provides pertinent information of the muscle sensitivity to pressure pain. As hypothesized, a nonuniform distribution of the pressure pain sensitivity over the elbow region was found to be in line with the results obtained from the triceps muscle (32). Moreover, a general hyperalgesia developed over the entire region was found 24 h after eccentric exercise. Barlas et al. (6) suggested that muscle hyperalgesia observed in DOMS may relate to central and peripheral sensitization mechanisms. Indeed, both peripheral and central mechanisms have been identified for the explanation of LE symptoms (11,12), supporting the concept that DOMS can be used for experimentally induced LE. The results of the PPT changes showed that there was a similar drop in absolute PPT for all points because of DOMS. This further underlined that the DOMS model induced mechanical hyperalgesia in a large area of the elbow. Future studies integrating topographical pressure pain sensitivity maps of the elbow region in patients with LE are warranted.

At baseline, the most sensitive PPT locations found over the elbow region were the points corresponding to the muscle belly of the ECRB muscle. Moreover, the ECRB was still most sensitive to pressure pain in the presence of DOMS compared with the extensor digitorum communis and extensor carpi ulnaris muscles. This underlines the primordial role of this muscle in LE sensory changes and motor deficit (8). In line with our study, Slater et al. (29) found that the ECRB muscle belly was the most sensitive site to pressure pain compared with the origin of the extensor digitorum communis muscle, the radioulnar joint, and the radial head after the induction of DOMS in the wrist extensors. However, the latter study only assessed five points around the elbow region and did not include the musculotendinous part of the ECRB muscle. In addition, Slater et al. (28) also reported that LE patients showed significant bilateral hyperalgesia at the ECRB muscle during and after experimental muscle pain compared with no pain and healthy controls, again supporting the role of this muscle in LE etiology. The results of the current study support that pressure pain sensitivity is intrinsically higher in the ECRB, which may explain why this muscle is hyperalgesic and of extreme importance in elbow injuries.

Higher pressure pain sensitivity was also found in the muscle belly sites compared with musculotendinous sites. This can be explained by the differences in muscle thickness as the underlying bone structures in the tendon areas can provide a more resistive force against the pressing force and result in generally higher PPT compared with muscle belly sites (1). Another explanation could be the difference in density and function of group III and IV nociceptors in muscle tendon and belly (2). Site dependency has also been reported in the presence of DOMS in the quadriceps muscle, with greater decreases in PPT in the distal region of the muscle, probably attributable to variations in the morphological and architectural characteristics of the muscle (19). Longitudinal studies should investigate if eccentric contractions of the wrist extensor muscles may be related to the development or prevention of LE. For instance, isokinetically adapted eccentric training has been reported to decrease pain intensity in patients with chronic lateral epicondylar tendinopathy (10), suggesting that training and rehabilitation programs of the elbow region could include a sufficient eccentric component.

Finally, we should recognize some limitations of this study. First, we did not include a control group, and only healthy subjects took part in the study. Therefore, our results cannot be extrapolated to patients with LE. It would be interesting to investigate if the application of DOMS has similar effects in an LE patient population. Second, our conclusions were largely based on the assumption that the assessed points correspond to different anatomical landmarks, that is, muscle belly or musculotendinous junction of the ECRB or extensor digitorum communis muscle. Nevertheless, this method of mapping has not yet been validated with respect to these anatomical landmarks. New studies validating the anatomical projection of the mapping point used in the current study are now needed.

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CONCLUSION

The present study demonstrated heterogeneous distribution of pressure pain sensitivity over the extensor muscles prior and during DOMS induced in the elbow region. Further, the most sensitive localizations for PPT assessment corresponded to the muscle belly of the ECRB. Our results support the role of the ECRB muscle in LE. Further studies are needed to assess the potential beneficial effect of eccentric exercise in training and rehabilitation programs of the elbow region.

The authors are grateful to Afshin Samani for his help during data collection and processing.

All authors disclose any financial and personal relationships with other people or organizations that could inappropriately influence their work.

The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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Keywords:

PRESSURE PAIN THRESHOLD; TOPOGRAPHICAL MAPS; DELAYED-ONSET MUSCLE SORENESS; MECHANICAL HYPERALGESIA

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