Revision of the Shoulder Normalization Tests Is Required to Include Rhomboid Major and Teres Major K.A. Ginn,1 M. Halaki,2 I. Cathers2 1 Discipline of Biomedical Science, Sydney Medical School, The University of Sydney, Lidcombe, NSW 1825, Australia, 2Discipline of Exercise and Sport Science, Faculty of Health Sciences, The University of Sydney, Lidcombe, NSW, Australia Received 8 November 2010; accepted 30 May 2011 Published online 27 June 2011 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.21488 ABSTRACT: The four ‘‘Shoulder Normalization Tests’’ were found previously to be a parsimonious set of isometric tests that produce maximal voluntary isometric contractions (MVIC) in the supraspinatus, infraspinatus, subscapularis, trapezius, serratus anterior, deltoid, latissimus dorsi, and pectoralis major [Boettcher et al. (2008). J Orthop Res 26:1591–1597]. However, these tests have not been validated for rhomboid major and teres major. In the current study, these Shoulder Normalization Tests were evaluated and compared to three other tests that could possibly elicit maximum activity in rhomboid major and teres major: abduction/extension in 908 abduction; adduction at 908 abduction; and extension in 308 abduction. No statistical difference was found in the mean activation of rhomboid major and teres major in these additional MVIC tests compared to the Shoulder Normalization Tests. However, the extension MVIC test produced maxima for at least 50% of subjects in rhomboid major, teres major, and latissimus dorsi. We concluded that the original Shoulder Normalization Tests should be expanded to include the extension MVIC test. The EMG normalization reference value for any of the above muscles would be the maximum EMG level generated across these Revised Shoulder Normalization Tests. ß 2011 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 29:1846–1849, 2011. Keywords: EMG; normalization; teres major; rhomboid major; shoulder muscles Extending the work of previous studies,1,2 Boettcher et al.3 identified four maximal voluntary isometric contractions (MVIC) that maximally activated the supraspinatus, infraspinatus, subscapularis, trapezius, serratus anterior, deltoid, latissimus dorsi, and pectoralis major. They termed these isometric tests the ‘‘Shoulder Normalization Tests’’ and suggested their adoption as a standard for generating MVIC for normalization in shoulder EMG research to facilitate reliable comparison among studies and thus, to progress understanding of shoulder muscle function. Rhomboid major and teres major are two large shoulder muscles involved in positioning the scapula and moving the humerus, respectively, which were not examined by Boettcher et al.3 A standard normalization procedure for shoulder EMG that also incorporates these two muscles would enable a more comprehensive understanding of the contribution of muscle dysfunction to shoulder joint pathology. Previous EMG research compared rhomboid major activity levels during eight isometric manual muscle tests including three positions specifically aimed at eliciting maxima in rhomboid muscles: Kendall positionresisted shoulder adduction and elevation in prone lying;4 Kendall-Alternative position-resisted shoulder horizontal extension at 908 abduction in prone lying;4 and the Hislop–Montgomery position-resisted shoulder extension/adduction in prone lying with hand on sacrum.5 Results indicated that the isometric test position recommended for posterior deltoid (resisted shoulder abduction/extension in 908 of shoulder Correspondence to: K.A. Ginn (T: þ61-2-9351-9352; F: þ61-29351-9520; E-mail: karen.ginn@sydney.edu.au) ß 2011 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. 1846 JOURNAL OF ORTHOPAEDIC RESEARCH DECEMBER 2011 abduction) elicited higher activity in rhomboid major than any of the three manual test positions recommended for rhomboid muscles, although this difference was only significantly higher than the Hislop– Montgomery test position.6 There do not seem to be any EMG studies comparing teres major activity during isometric manual muscle tests. Therefore, our aim was to compare the activity levels generated in rhomboid major and teres major during the four Shoulder Normalization Tests with those generated during resisted shoulder abduction/ extension in 908 of shoulder abduction, previously recommended by Smith et al.6 as the manual muscle test to be used to produce maximal rhomboid activity for normalization purposes during kinesiologic studies, and in tests likely to generate maximum activity in teres major. The manual muscle test position for teres major recommended by Kendall et al.4 is resisted shoulder extension and adduction with the humerus in an internally rotated position. As the Shoulder Normalization Tests include a maximal isometric internal rotation test, we included maximal isometric shoulder extension and adduction tests to include all shoulder movements likely to generate maximum teres major activity. Because scapular downward rotation, produced by rhomboid major, accompanies adduction, the inclusion of a separate adduction manual test had the added advantage of potentially generating maximum activity in rhomboid major. Our objective was to determine if the Shoulder Normalization Tests could be used to validly determine maximal activity in rhomboid major and teres major for the purposes of normalization of shoulder EMG, or if this recommended standard set of shoulder normalization procedures required modification to include these additional shoulder muscles. REVISED SHOULDER NORMALIZATION TESTS METHODS Subjects Fourteen subjects (6 female, 8 male, 18–49 years old (mean 22.5 years)), who had not experienced dominant shoulder pain in the past 2 years and had never sought treatment for dominant shoulder pain, participated. Subjects demonstrated normal shoulder range of motion and scapulohumeral rhythm and be pain-free on isometric internal and external rotation strength testing. Subjects were fully informed of the protocol and provided signed consent prior to participation. The study was approved by the University’s Human Research Ethics Committee. Instrumentation EMG data were collected simultaneously from 11 shoulder muscle sites using a combination of surface and indwelling electrodes: rhomboid major, teres major, supraspinatus, infraspinatus, subscapularis, upper and lower trapezius, serratus anterior, deltoid, pectoralis major, and latissimus dorsi. Surface electrodes were used to record activity in upper trapezius, middle deltoid, and pectoralis major. Before surface electrode application and with the participant seated, the skin was prepared with alcohol and an abrasive gel to reduce skin impedance. Over each muscle site, 2 surface electrodes (Red Dot, 2258, 3M, Sydney, Australia) were placed 2 cm apart parallel to the orientation of the muscle fibers. Inter-electrode resistances were always ensured to be <10 kV. Intramuscular electrodes, manufactured in our laboratory using the technique described by Basmajian and De Luca,7 were inserted into the remaining muscles.8,9 Intramuscular electrodes were used for muscles that either underlie more superficial muscles (rhomboid major, supraspinatus, subscapularis), are thin and overlie other muscles (lower trapezius, latissimus dorsi), or for muscles that shift with respect to the overlying soft tissue during shoulder movement (teres major, infraspinatus, serratus anterior). Correct indwelling electrode placement was confirmed by visual inspection of the EMG signals on a monitor during the performance of standardized submaximal tests expected to produce a large amount of activity in each muscle and compared with tests expected to generate low activity or activate surrounding muscles into which the electrode may have been incorrectly placed.3 Because of the difficulty in distinguishing between rhomboid major and lower trapezius using this method, intramuscular electrodes were inserted into these muscles using ultrasonic guidance (Mindray, DP9900). A large ground electrode (Universal Electrosurgical Pad:Split, 9160F, 3M, Sydney, Australia) was placed over the contralateral acromion and scapular spine. EMG signals were amplified and filtered (Iso-DAM 8 amplifiers, World Precision Instruments, Sarasota, FL; gain ¼ 100, bandpass between 10 and 1 kHz) before transferring to a PC with a 16 bit analog to digital converter (1401, Cambridge Electronics Design, Cambridge, UK) at a sampling rate of 2,564 Hz using Spike2 software (version 4.00, Cambridge Electronics Design). MVIC Tests Seven MVIC tests were performed in a seated position. These included shoulder abduction/extension in 908 abduction (‘‘abduction/extension’’) identified by Smith et al.6 to generate the greatest activity in rhomboid major, and the 4 Shoulder Normalization Tests as described by Boettcher et al.3: abduction at 908 with internal rotation; internal rotation in 908 1847 abduction; flexion at 1258 with scapula resistance; and horizontal adduction at 908 flexion. In addition, shoulder adduction at 908 abduction (‘‘adduction’’) and shoulder extension at 308 abduction (‘‘extension’’) were included so that all the known actions of teres major were tested. Each test lasted 5 s: 1 s to reach maximum, 3 s sustained maximum; and gradual release over the final 1 s. Each test was performed three times in random order across tests. There was a minimum rest interval of 30 s between repetitions and a minimum 1 min rest interval between each new test position. During testing, subjects could view the raw EMG signal on the computer screen, were given verbal encouragement, and were closely monitored to ensure that they did not attempt compensatory movements of the scapula or trunk. Signal and Statistical Analyses EMG signals were high pass filtered (10 Hz, dual pass 4th order Butterworth), rectified, and low pass filtered (4 Hz, dual pass 4th order Butterworth) using (Matlab version 7, The Math Works, Natick, MA). The maximum EMG (MVIC) was taken as the maximum of this rectified and filtered signal. The MVIC from abduction/extension, adduction, and extension tests were compared to the MVIC obtained using the set of 4 Shoulder Normalization Tests using a single factor, 4 level repeated measures ANOVA (Statistica, version 7.1, StatSoft, Tulsa, OK) for each muscle. Since no one test maximally activated a specific muscle in all subjects, the statistical confidence of the Shoulder Normalization Tests to produce maximal activation required use of the complete set of 4 tests.3 Thus, the 4 Shoulder Normalization Tests were analyzed collectively. Significant results were accepted at p < 0.05. Tukey’s HSD post hoc test was used when significant differences were found. RESULTS The mean (standard error) MVIC EMG levels for rhomboid major and teres major for all MVIC tests are shown in Figure 1. For rhomboid major, no significant differences were found in the levels for any of the tests (F3,39 ¼ 1.28, p ¼ 0.29). For teres major, significant differences were found among tests (F3,39 ¼ 5.02, p < 0.05). Post hoc tests indicated that the EMG levels were significantly higher during the extension MVIC Figure 1. Mean (standard error) MVIC EMG levels obtained for rhomboid major and teres major during the abduction/extension, adduction, extension MVIC tests, and the Shoulder Normalisation Tests.3 Indicates significant (p < 0.05) difference between extension and abduction/extension in teres major only. JOURNAL OF ORTHOPAEDIC RESEARCH DECEMBER 2011 1848 GINN ET AL. test compared to EMG levels obtained using the shoulder adduction/extension in 908 abduction MVIC test (p < 0.05), with no significant differences (p 0.05) in EMG levels across all other MVIC tests. The number and percentage of subjects that produced a maximum EMG level for each MVIC test compared to the 4 Shoulder Normalization Tests are shown in Table 1. Although no difference was found between EMG levels among the extension test and the 4 Shoulder Normalization Tests in both rhomboid major and teres major, the extension test produced a maximum EMG in both muscles for 50% of subjects, while the 4 Shoulder Normalization Tests produced a maximum for <30% of subjects. To investigate the effects of adding the extension test to the Shoulder Normalization Tests, the number and percentage of subjects that produced a maximum during the extension MVIC test in the nine muscle sites originally tested by Boettcher et al.3 are shown in Table 2. Of these muscles, only latissimus dorsi generated maximum EMG levels in a large percentage of subjects (71%) during the extension MVIC test. DISCUSSION Our results indicate that, of the MVIC tests examined, the shoulder extension test is most likely to achieve maximal activation of both rhomboid major and teres major. For rhomboid major, this test generated high mean EMG activity that was not significantly different from that generated during the standard set of shoulder EMG normalization procedures (Shoulder Normalization Tests) recommended by Boettcher et al.3 or the abduction/extension and adduction MVIC tests. For teres major, the extension MVIC test generated significantly higher EMG activity than the abduction/extension test, but not different from that generated by the Shoulder Normalization Tests. However, a greater percentage of subjects achieved maximum rhomboid major and teres major activity during the extension MVIC test (57% and 50%, respectively) than during the Shoulder Normalization Tests (14% and 28%, respectively) or the other two MVIC tests (maximum 14% in both muscles). Because many tests generated similar high mean EMG activity in Table 1. The Number and (Percent) of Subjects That Produced Maximum EMG in Rhomboid Major and Teres Major during Each of the MVIC Tests and the Shoulder Normalization Tests3 MVIC Test Abduction/extension Adduction Extension Shoulder Normalization Tests Rhomboid Major Teres Major 2 (14%) 2 (14%) 8 (57%) 2 (14%) 2 (14%) 1 (7%) 7 (50%) 4 (28%) JOURNAL OF ORTHOPAEDIC RESEARCH DECEMBER 2011 Table 2. The Number and (Percent) of Subjects That Produced Maximum EMG during the Extension MVIC Test in the Nine Muscle Sites Previously Tested by Boettcher et al.3 Muscle Supraspinatus Infraspinatus Subscapularis Upper trapezius Lower trapezius Serratus anterior Deltoid Pectoralis major Latissimus dorsi Number of Subjects (%) 0 (0%) 1 (7%) 1 (7%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 10 (71%) many of the muscles they examined, Boettcher et al.3 used the two criteria of tests that produced significantly highest mean EMG activity and highest percentage of subjects achieving maximum activity, to determine a parsimonious, standard set of maximum tests for use in normalizing shoulder EMG data. Based on these same criteria, our study would suggest that shoulder extension performed at 308 abduction be added to the original Shoulder Normalization Tests to generate valid appropriate normalization reference values (Fig. 2). As acknowledged by Boettcher et al.,3 a standard set of maximum isometric shoulder normalization tests may not generate absolute maximum activity in all subjects; this is also true of the shoulder extension MVIC test recommended above for use in normalizing activity in teres major and rhomboid major. There may be other tests not examined in this study that may generate absolute maximum activity in rhomboid major and teres major in a larger percentage of subjects than the recommended shoulder extension MVIC test. However, we would agree with Boettcher et al.3 that the advantage of adopting a standard set of tests as soon as possible to make comparisons between future shoulder EMG studies more reliable outweighs these limitations. Our results suggest that the shoulder extension at 308 abduction MVIC test needs to be added to the 4 Shoulder Normalization Tests3 to have a high likelihood of achieving maximal activation in rhomboid major and teres major. The extension MVIC test also has the benefit of achieving similarly high levels of latissimus dorsi activity as the Shoulder Normalization Tests but with 70% of the cohort examined in this study achieving maximum latissimus dorsi activity during this test. Boettcher et al.3 also found that latissimus dorsi activity was not significantly different from its maximum level of activation during a similar isometric extension test as we examined. Therefore, because the extension MVIC test is necessary to reliably achieve maximum activity levels in rhomboid major and teres major, and because it is likely to achieve absolute maximum activity levels in latissimus REVISED SHOULDER NORMALIZATION TESTS 1849 individuals. Therefore, similar to the recommendations of Boettcher et al.3 the normalization reference level for each of these muscles should be taken as the maximum level of activation generated across all five Revised Shoulder Normalization Tests. In conclusion, our results indicate that the original standard shoulder normalization procedures3 should be expanded to include the isometric extension test performed at 308 abduction. These Revised Shoulder Normalization Tests thus include: abduction at 908 with internal rotation; internal rotation in 908 abduction flexion at 1258 with scapula resistance; horizontal adduction at 908 flexion; and extension at 308 abduction. This set of tests: will be able to reliably generate maximal activity in more shoulder muscles than the original Shoulder Normalization Tests; is more likely to generate maximal activity in latissimus dorsi than the original Shoulder Normalization Tests; and is still few in number to minimize subject fatigue. The recommended Revised Shoulder Normalization Tests builds on the rigorous examination of shoulder normalization tests by Boettcher et al.3 to provide a standard set of normalization procedures for use in EMG studies. REFERENCES Figure 2. The extension MVIC test: subject seated with the arm at 308 abduction, elbow fully extended, and thumb toward the body; arm extended as resistance applied over the distal forearm. dorsi in a higher percentage of subjects than the Shoulder Normalization Tests, we would recommend that the extension MVIC test be added. This set of five Revised Shoulder Normalization Tests still satisfies the criterion of being small in number to reduce the likelihood of fatigue during subject preparation, while enabling standardized, reliable normalization of EMG data recorded from more shoulder muscles than the original Shoulder Normalization Tests. As demonstrated previously3,10 and supported by our results, maximum activity in many shoulder muscles may be generated from many isometric tests in different 1. Ekstrom R, Soderberg G, Donatelli R. 2005. Normalization procedures using maximum voluntary isometric contractions for serratus anterior and trapezius muscles during surface EMG analysis. J Electromyogr Kinesiol 15:418–428. 2. Kelly B, Kadrmas W, Kirkendall D, et al. 1996. Optimal normalisation tests for shoulder muscle activation: An electromyographic study. J Orthop Res 14:647–653. 3. Boettcher C, Ginn K, Cathers I. 2008. Standard maximum isometric voluntary contraction tests for normalizing shoulder muscle EMG. J Orthop Res 26:1591–1597. 4. Kendall F, McCreary E, Provance P, et al. 2005. Muscles: Testing and function with posture and pain. 327–328 pp. 5. Hislop H, Montgomery J. 2002. Muscle testing and function, 7th ed. Philadelphia: WB Saunders. 467 p. 6. Smith J, Padgett D, Kaufman K, et al. 2004. Rhomboid muscle electromyography activity during 3 different manual muscle tests. Arch Phys Med Rehab 85:987–992. 7. Basmajian J, De Luca C. 1985. Muscles alive: Their functions revealed by electromyography, 5th ed. Baltimore: Williams & Wilkins Co. 561 p. 8. Geiringer S. 1994. Anatomic localization for needle electromyography. Philadelphia: Mosby; 153 p. 9. Kadaba M, Cole A, Wooten M, et al. 1992. Intramuscular wire electromyography of the subscapularis. J Orthop Res 10:394–397. 10. Chopp J, Fischer S, Dickerson C. 2010. On the feasibility of obtaining multiple muscular maximal voluntary excitation levels from test exertions: A shoulder example. J Electromyogr Kinesiol 20:896–902. JOURNAL OF ORTHOPAEDIC RESEARCH DECEMBER 2011