http://informahealthcare.com/ptp ISSN: 0959-3985 (print), 1532-5040 (electronic) Physiother Theory Pract, 2014; 30(4): 282–286 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/09593985.2013.867386

RESEARCH REPORT

The influence of muscle length on one-joint shoulder internal and external rotator muscle strength Michael T. Cibulka, PT, DPT, OCS, FAPTA, Geoff Enders, DPT, Jessica Hall, DPT, Andrea Jackson, DPT, Samantha Maines, DPT, Jolyn Vonder Haar, DPT, and Jack Bennett, PT, DPT, SCS, CSCS Department of Physical Therapy, Maryville University, St. Louis, MO, USA

Abstract

Keywords

Background and purpose: Kendall suggests testing the rotator cuff muscles in their maximally shortened position, since one-joint muscles are thought to be strongest. We found little evidence to support this concept. The purpose of this study was to determine if the shoulder internal rotator (IR) and external rotator (ER) muscles are strongest when placed in their shortened length position. Methods: Fifty-three subjects participated. Glenohumeral joint internal rotation and external rotation motion was measured. Muscle strength was then tested using a hand-held dynamometer in four positions: (1) end-range ER; (2) neutral 0 ; (3) glenohumeral joint mid-range and (4) end-range IR. Data were analyzed using two repeated measures ANOVA’s. Results: The results suggest that rotator muscle strength is dependent on muscle length. IR strength was weakest at end-range IR in its shortest length; ER muscle strength was weakest at end-range ER in its shortest length. Muscle strength of the IR or ER was not significantly different when comparing neutral 0 to the mid-range position and at their most lengthened position. Conclusion: The IR and ER muscles were found to be weakest when placed in a position of shortest muscle length, while the neutral 0 and mid-range positions were the strongest positions.

External rotator, internal rotator, muscle, shoulder, strength

Weakness of the rotator cuff muscles is associated with a number of different shoulder problems (Ellenbecker and Cools, 2010; Ellenbecker and Derscheid, 1989; Jerosch, Castro, Sons, and Moersler, 1989; Seitz et al, 2011; Smith and Campbell, 1992). Therefore an evaluation of the rotator cuff muscles strength is an important part of a clinician’s plan of care. The most commonly used method to assess the strength of the rotator cuff muscles is with manual muscle testing (Hislop and Montgomery, 2007; Kendall et al, 2005). According to Kendall et al (2005), selecting the proper joint position at which to manually test a muscle is important. Not knowing which test position is strongest and which is weakest can lead to false impressions of a person’s muscle strength (a finding of a false positive or negative). According to Kendall et al (2005), the optimal test position for a one-joint muscle is at the completion of the range of motion (ROM), where it is at its shortest muscle length. Kendall et al (2005) describes one-joint muscles as Class I muscles. According to Kendall et al (2005), Class I muscles ‘‘actively shorten through range to completion of joint motion and exhibit maximal strength at completion of range (i.e. short and strong)’’. Currently no evidence shows that a one-joint muscle is strongest at its most shortened muscle length position. Placing a one-joint muscle at its shortest muscle length goes against the current thinking that a muscle would be at its weakest point of the

Address correspondence to Michael T. Cibulka, PT, DPT, OCS, FAPTA, Department of Physical Therapy, Maryville University, 650 Maryville University Drive, 5818 Marromet Ct., St. Louis, MO 63128, USA. E-mail: [email protected]

Received 31 January 2013 Revised 5 September 2013 Accepted 17 September 2013 Published online 23 December 2013

length–tension curve (Taylor and Rudel, 1970). The length– tension curve proposes that a muscle during an isometric contraction will exert less tension when it is in its maximally shortened or lengthened position (Gordon, Huxley, and Julian, 1966a,b; Williams and Goldspink, 1978), due to overlapping or overextending of muscle sarcomeres. Therefore, according to the length–tension curve, the shoulder internal rotator (IR) and external rotator (ER) muscles should likely be strongest at their resting length which is at the mid or neutral 0 test position. Lieber (2010), however, states there is little scientific basis for using the concept of the length–tension curve for determining at what joint angle muscle exerts its maximum isometric force. Thus we really have no evidence to support that a single joint position yields maximal muscle strength on a muscle test. Numerous studies have examined the shoulder rotator cuff muscles isokinetically; so far no studies have compared isometric IR and ER muscle strength when the IR and ER muscles are placed in their fully shortened and lengthened position (Andrade Mdos et al, 2010; Byram et al, 2010). Jenp, Malanga, Growney, and An (1996) examined isometric shoulder ER and IR muscle strength using a Cybex II dynamometer in 20 subjects. The strength of the IR and ER muscles were tested at neutral 0 and in their lengthened position but were not tested in their shortest muscle length position. The IR muscles were tested at only half their range of internal rotation (e.g. 45 ), likewise the ER muscles were tested at half of their range of external rotation (e.g. 45 ). Riemann, Davies, Ludwig, and Gardenhour (2010) tested IR and ER muscle strength in three different shoulder positions (prone at 90 , neutral, and 30 of abduction, scaption and diagonal). The purpose of their study was to see if strength differences existed for the different shoulder positions, however they did not assess

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Introduction

History

One-joint shoulder internal and external rotator muscle strength

DOI: 10.3109/09593985.2013.867386

rotator cuff muscle strength based on muscle length. Therefore no studies have yet to examine the isometric strength of the shoulder IR and ER muscles across the full range of muscle length. The purpose of this study was to assess the influence muscle length has on muscle strength of the one-joint shoulder IR and ER muscles and to determine which, if any, is the strongest test position. We wanted to see if, according to Kendall et al (2005), the IR and ER muscles would be strongest at the end-range joint positions where the IR and ER muscles are maximally shortened ‘‘short and strong’’.

Methods Subjects This study was approved by the Maryville University Institutional Review Board. Fifty-three subjects were used from a sample of convenience from Maryville University students and the Greater St. Louis area. The sample consisted of 12 males and 41 females age 18–65 (mean age: 24.1; SD: 9.2). Forty-nine subjects were right-hand dominant and four left-hand dominant. Subjects were asked to wear non-restrictive clothing with access to the shoulder (i.e. a loose fitting t-shirt). Exclusion criteria included: previous shoulder surgery in the past 3 years; shoulder pain; neck pain; arm pain; unable to tolerate the supine position; history of chronic shoulder dislocations or current pregnancy. Procedure Subjects all signed an informed consent form, filled out a questionnaire to assess if they were eligible for the study, and were then assigned a research subject number. The subject number was used to determine which muscle group would be tested first at each position; even number subjects had the ER muscles tested first, and odd numbers had the IR muscles tested first. Next, subjects randomly drew one of two index cards to determine whether the right or left arm was tested to prevent the problem of double dipping. All together 28 right shoulders and 25 left shoulders were tested. Subjects then selected four cards, each with a testing position on it (end-range IR, end-range ER, midrange and neutral), to randomize the testing position order. A 12-in plastic universal goniometer was used to measure passive shoulder IR and ER range of motion (ROM); standard error of the measure for a universal goniometer is 5 (Vermeulen et al, 2005; Wikholm and Bohannon, 1991). The ROM of shoulder (glenohumeral) rotation was measured by performing passive IR and ER with the subject lying supine on a treatment table. Subjects were first passively moved through their available shoulder rotation ROM prior to the ROM measurements, this was performed primarily to assess the subject’s ability to relax. During ROM measures pressure was applied to the anterior (caracoid process) shoulder to prevent substitutions while the glenohumeral joint was rotated into the direction of IR or ER until a firm end feel was met. A firm end feel represents the end ROM for muscles, capsules or ligaments. The goniometer was aligned as follows: the axis at the olecranon process; the stationary arm was Figure 1. Operational definitions of the four different test positions.

perpendicular to the floor and the moving arm was aligned with the ulna using the ulnar styloid process for reference. A towel roll was placed under the subject’s distal humerus so it was parallel to the surface. Goniometric measures for IR and ER were read and the ROM documented by a neutral observer. Intraclass correlation coefficients were established from the first consecutive 15 subjects. The ICC (3,1) for both IR and ER was found to be high, ICC ¼ 0.99 [95% CI: 0.97–0.99]. IR and ER strength was measured with a hand-held dynamometer (HHD) by performing a ‘‘make’’ test of the IR and ER muscles with the subject lying supine. The ‘‘make’’ test using a HHD has previously been demonstrated with an ICC of 0.91 (Vermeulen et al, 2005). Subjects were examined using four different test positions: (1) end-range ER; (2) neutral 0 ; (3) a mid-range position and (4) end-range IR (Figure 1). The endrange IR and ER positions consisted of the end of the subjects available ROM in each direction without scapular or trunk substitutions. End-range IR represents glenohumeral rotation so that the subject’s forearm was placed vertical or perpendicular to the anatomical axis of the body. We also included a mid-range test position. We calculated a mid-range test position based on the concept that a one-joint muscle length and ROM are the same (Kendall et al, 2005). The normal ROM of motion in the shoulder is 70 of IR and 90 of ER (Clarkson, 2000), however variation exists, so we calculated the mid-range position by adding ER and IR ROM and then divided the sum by 2 to give a total range of glenohumeral rotation. The total range of glenohumeral rotation was then subtracted from the largest ROM value found for either IR or ER. For example, if the participant has 70 of IR and 90 of ER, the sum would be 160 . The total range of rotation 160 is then divided by 2 which equals 80 . The 80 is then subtracted from 90 (the largest ROM value found for ER). This resulted in a mid-range position of 10 of ER (Figure 1). A description of the 53 subjects ROM is displayed in Table 1. IR and ER strength was measured with a HHD by performing a bilateral ‘‘make’’ test of the IR and ER muscles while the participant was in the supine position. This test differs from a ‘‘break’’ test in that there is no intention of breaking the muscle contraction by the tester. While supine the subject was manually placed, according to their range, in each of the four different test positions prior to strength testing. The HHD was held stationary 3 cm proximal to the ulnar styloid process, and in the center of the subject’s forearm, while a slight pressure was used to stabilize the anterior shoulder to prevent scapular substitution. All subjects were instructed to slowly increase their force into the HHD until a maximum contraction was achieved. This maximum contraction was held for 3 s, and was then reduced. The intention of the test was for subjects to ‘‘make’’ a maximal muscle contraction, not to ‘‘break’’ the contraction by applying an additional overwhelming force in the opposite direction. Each subject had IR and ER strength measurements taken twice at each testing position, and the same muscle group was never assessed consecutively. To insure data were taken unbiased the measures were read and recorded by a separate observer.

Midrange position at 10° End Range ER Position at 90°

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Neutral Position at 0° End Range IR Position at 70°

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Physiother Theory Pract, 2014; 30(4): 282–286

Table 1. Descriptive statistics for our 53 subjects range of motion (in degrees).

ER ROM IR ROM Total ROM

Minimum

Maximum

Mean

SD

60 19 103

112 89 188

90.6 55.7 146.3

12.3 17.1 17.4

Table 2. ICCs for IR and ER muscle testing.

External rotator muscles Internal rotator muscles

End-range IR

Neutral

Mid-range

End-range ER

0.980 0.990

0.987 0.978

0.979 0.984

0.952 0.991

The reliability of the ‘‘make’’ tests for the first 15 subjects IR and ER muscles for each of the different test positions was very high (Table 2). Minimal detectable change (MDC95) was determined for IR muscle (1.5 kg) and for ER muscle force (1.4 kg) using the formula MDC95 ¼ SEM  1.96  ˇ2.

Figure 2. ER muscle strength in kilogram at different shoulder joint positions (ER muscles shortest in ER).

Data analysis Descriptive statistics were used to calculate means and confidence intervals for IR and ER muscle strength and to assess both samples for normality using SPSS version 16.0. Data were first checked for normality using the Shapiro–Wilk and Kolmogorov– Smirnov tests as well as assessing kurtosis and skewness. Two different repeated measure ANOVA’s were used, one to compare IR, and the other to compare ER muscle strength at the four different test positions. A post hoc Bonferroni adjustment was performed to adjust for alpha inflation when performing multiple tests. Findings were considered significant at p50.05.

Results The data were found to be normally distributed for both the IR and ER muscle force. Both IR and ER repeated measure ANOVA’s had a significant Mauchley’s test for sphericity so we used the Huynh–Feldt correction for testing the main effects. Both of the repeated measure ANOVA’s showed that significant differences do exist between the four positions for ER muscle force (F ¼ 118.2; p50.01) and for IR muscle force (F ¼ 45.8; p50.01). Post hoc analysis showed that significant differences do not exist between neutral and mid-range positions for both IR and ER muscle forces. Significant differences do exist between the shortened length and mid-position for both IR and ER muscles. Significant differences also existed between the shortened and neutral 0 position for both IR and ER muscles. Finally differences existed between shortened and lengthened position for both IR and ER muscles (Figures 2 and 3; Table 3).

Discussion The results of this study showed that both the IR and ER muscles of the shoulder are weakest when tested in their maximally shortened position. This position is one in which the shoulder (glenohumeral) joint was full externally rotated for the ER muscles and internally rotated for the IR muscles (Figures 2 and 3). This finding differs from Kendall et al (2005) who proposed that one-joint muscles, when maximally shortened, will produce their optimal strength at the completion of their range. Our results also agree with the findings of Jenp, Malanga, Growney, and An (1996) who found that the shoulder IR and ER muscles were nearly equal in strength when comparing the

Figure 3. IR muscle strength in kilogram at different shoulder joint positions (IR muscles shortest in IR). Table 3. Mean IR and ER muscle strength in kilograms with 95% CIs. Muscle group IR ER

End-range IR

Neutral 0

Mid-range

End-range ER

6.0 [5.3–6.7] 9.2 [8.1–10.3] 9.7 [8.6–10.8] 9.0 [7.6–10.4] 9.1 [7.9–10.3] 10.8 [9.7–11.9] 10.9 [9.9–11.9] 4.3 [3.8–4.7]

mid-range and neutral position to a position where the ER and IR muscles were maximally lengthened. The data also suggest that the mid-range and neutral 0 position are likely near the resting muscle length of the IR and ER muscles. Resting muscle length is the position where muscle develops its maximum isometric tension (force). Hislop and Montgomery (2007) described the reason for testing single joint muscles at the end of the range is ‘‘to allow for consistency of procedure rather than to select the estimated midrange position’’. According to Leiber (2010) and Lieber and Shoemaker (1992), there is virtually no evidence to support that a single joint position yields maximal muscle strength on a muscle test. Leiber (2010); Lieber and Boakes (1988a,b); Lieber and Shoemaker (1992) and Mai and Lieber (1990) also claimed that recent animal studies suggest that muscle force is often at its maximum at the extreme end of the range of motion. Our results also show that there may not be a single best position to assess muscle strength, however some positions are better than others.

DOI: 10.3109/09593985.2013.867386

One-joint shoulder internal and external rotator muscle strength

Strength production for the IR and ER muscles was weakest in the maximally shortened position, while the neutral and mid-range positions were both near the peak of isometric muscle force production (Figures 2 and 3). Therefore the IR and ER are best tested for their maximum strength in the mid-range or neutral 0 test position. While numerous studies have previously been performed on the isometric force production of muscle most have been performed on the elbow flexors and extensors and knee flexors and extensor muscles (Cahalan, Johnson, and Chao, 1991; Campney and Wehr, 1965; Haffajee, Moritz, and Svantesson, 1972; Knapik, Wright, Mawdsley, and Braun, 1983; Lindahl, Movin, and Ringqvist, 1969; Scudder, 1980; Singh and Karpovich, 1966; Williams and Stutzman, 1959). Williams and Stutzman (1959) studied isometric force production on a number of different muscles. They found that most isometric force showed a continuous drop in strength from the elongated to the shortened position in most of the muscles they studied. However in some they noted a plateau or leveling off of force production. Knapik, Wright, Mawdsley, and Braun (1983) examined four different muscle groups (knee extensors, knee flexors, elbow flexor and elbow extensors) and found generally an ‘‘inverted U-shaped curve’’ for isometric peak torque with the greatest force production in mid-range and the least force production where muscle was in its most shortened length. Our data were in line with Knapik, Wright, Mawdsley, and Braun (1983) finding of an inverted ‘‘Ushaped’’ curve with a steeper ascending curve when the rotators were at their shortest length and a flatter descending curve when the rotator muscles were lengthened (Figures 2 and 3). Williams and Stutzman (1959) report that during an isometric muscle contraction muscle contracts with more force when fully elongated and force decreases as the muscle is shortened. Although we noted a large decrease in force production in both the IR and ER muscles when fully shortened compared to the maximally lengthened position muscles in the fully shortened position also had significantly less force when compared to the neutral 0 and mid-range positions both statistically and by more than the minimal detectable change amount (1.4 kg for ER and 1.5 kg for IR) (Figures 2 and 3). The length–tension curve of muscle is only valid for isometric contractions and cannot be used for isotonic or isokinetic contractions; this is because the length–tension curve was determined under constant length (Lieber, 2010) and isotonic and isometric contractions have changing length. Also the length– tension curve was derived from isolated muscle fibers not for the entire muscle. Muscle length is defined as the distance from origin of the proximal to the insertion of the distal fiber, while fibers length is the length of just the muscle itself (Lieber, 2010). Thus fiber length and muscle length are never the same because of the addition of connective tissue (e.g. tendon). Also pennate and other muscles that are twisted or angled do not follow the entire length of the muscle. The rotator cuff muscles are somewhat linear and have less connective tissue when compared to the semitendinosus muscle, so that they likely behave similar to the expectations of the length–tension curve. Our results agree with this, with the least force generated in the shortest length position, the most in the mid-range, and with force decreasing as the rotators are fully lengthened. The shoulder abducted at 90 position is the best position for isolating the one-joint rotator cuff muscles as a group. EMG analysis shows that testing the rotator cuff muscles at 0 of abduction results in contraction of the pectoralis major and latissimus dorsi muscles during IR and the posterior deltoid during ER (Dark, Ginn, and Halaki, 2007). However, for isolating

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individual rotator cuff muscles, like the supraspinatus, other positions are more advantageous, like the full or empty can positions (Brookham, McLean, and Dickerson, 2010). Our sample of convenience had more females than males. To make sure gender differences did not exist in our results we also performed separate repeated measure ANOVA’s on males and females and found the same results as we did with both groups combined. Another possible limitation is the strength of the muscle tester; a couple of the subjects were able to over-power the muscle tester during testing which could have resulted in an inaccurate measure of muscle strength. Wikholm and Bohannon (1991) determined that tester strength makes a difference when using a HHD to measure muscle strength; stronger testers consistently measured greater forces than weaker testers when assessing the same muscle group. Future studies should include a larger sample of subjects including more males, and older individuals. Also subjects with shoulder problems should be compared to a group of healthy individuals to identify discrepancies in strength at specific parts of the shoulder rotation ROM. Another desirable study would be to establish if similar results are found using a ‘‘break’’ test, since this is the traditional manual muscle testing procedure. A major impetus for this study came from our experience manual muscle testing shoulders in the clinic; we often found weakness of the shoulder ER muscles when testing at the end of full shoulder ER. A future study comparing the results of HHD to manual muscle tests of the shoulder would be interesting. Another future study that would be clinically interesting is to compare our manual muscle tests positions with the 30–30–30 positions. Knowing that different shoulder test positions can influence muscle strength of the rotator cuff muscles is important when selecting the proper test position for a patient. Since the IR and ER muscles were found to be weakest in their maximally shortened position, clinicians must consider this to avoid finding a false weakness when muscle testing. Conversely this information can also help clinicians when assessing patients where a mismatch between the therapist and patient exists, understanding the weaker test position when muscle testing the rotator cuff muscles can help reduce the findings of a false negative test result. Finally knowing where the IR and ER muscles are weakest and strongest within the shoulder ROM can also give clinician’s important information when prescribing different types of exercises for the rotator cuff muscles.

Declaration of interest The authors report no declaration of interest.

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The influence of muscle length on one-joint shoulder internal and external rotator muscle strength.

Kendall suggests testing the rotator cuff muscles in their maximally shortened position, since one-joint muscles are thought to be strongest. We found...
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