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FASXXX10.1177/1938640014539812Foot & Ankle SpecialistMonth XXXXvol. X / no. XFoot & Ankle Specialist

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〈 Clinical Research 〉 Plantar Flexor Muscle Architecture Changes as a Result of Eccentric Exercise in Patients With Achilles Tendinosis Abstract: Eccentric training for Achilles tendinosis (AT) has been reported to significantly improve patient symptoms. There has been no biomechanical explanation on the mechanism for specific rehabilitation technique. The purpose of this study was to determine changes in muscle architecture that occurred as a result of Achilles tendinosis injury and a subsequent eccentric rehabilitation program. Twenty-five patients (age, 53.3 ± 17.5 years) diagnosed with AT participated in 6 weeks of rehabilitation. Specific exercises for the ankle plantar flexors consisted of maximal load eccentric muscle action using 3 sets of 15 repetitions. Patients also completed a protocol for AT, which consisting of traditional rehabilitation. Medial gastrocnemius (GM) and lateral gastrocnemius (GL) muscle fascicle length and thickness were measured with ultrasound at 2-week intervals from initial treatment day to the end of 6 weeks of rehabilitation.

Matthew T. Crill, MS, MBA, PT, Gregory Berlet, MD, and Christopher Hyer, DPM, MS

this correlated with improvement in Medial gastrocnemius fascicle length a validated patient outcome scoring increased (45.1 ± 10.5 mm to 51.4 system. Further study is warranted to ± 10.5 mm; P = .22) between the determine a predictive relationship initial day of rehabilitation and after between improvement of GM fascicle 6 weeks of rehabilitation. But, GM length and outcome scores. thickness (16.3 ± 3.5 mm to 16.8 ± 2.0 mm), GL fascicle length (47.2 ± 10.0 mm to 47.1 ± 7.4 mm), and A strengthening program that GL thickness (14.9 ± 5.2 mm to 14.4 ± 2.7 mm) emphasizes eccentric muscle actions has did not change as a result of rehabilitation. been found to be particularly effective in A 6-week eccentricrelieving the symptoms of Achilles biased exercise increased the GM muscle fascicle tendinosis and hastening the return to length by 12%, but GM thickness, GL fascicle function.” length, and GL thickness did not change as a result of rehabilitation. Eccentric training for the treatment Levels of Evidence: Therapeutic, of AT is well recognized, but the Level IV: Case series mechanism of action has not been previously reported. A 6-week eccentric Keywords: muscle architecture; training protocol increased the GM eccentric training; Achilles tendinosis; muscle fascicle length by 12%, and rehabilitation; FOTO



DOI: 10.1177/1938640014539812. From OhioHealth, Columbus, Ohio, USA (MTC); and Orthopedic Foot & Ankle Center, Westerville, Ohio, USA (GB, CH). Address correspondence to: Matthew T. Crill, MS, MBA, PT, 1166 Dublin Road, Columbus, OH 43215, USA; e-mail: [email protected]. For reprints and permissions queries, please visit SAGE’s Web site at http://www.sagepub.com/journalsPermissions.nav. Copyright © 2014 The Author(s)

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Introduction Ultrasound imaging is a diagnostic tool for musculoskeletal problems and has also been used more recently to determine the in vivo behavior of muscles (Figure 1). Various aspects of muscle architecture are measured easily with ultrasound imaging such as muscle thickness, fascicle length, and pennation angle when the muscle is at rest or with activity.1 Specifically, the architectural characteristics of muscle have been shown to change substantially during muscle contraction and joint movement,2-4 in response to immobilization, aging, and strength training.5-9 Changes in muscle fascicle length after muscle-tendon complex injury and through rehabilitation have not been investigated. If the changes that occur during immobilization and strengthening in normal, healthy patients are similar to patients with muscle or tendon injury, one could suggest potential mechanisms that underlie specific rehabilitation exercises. Achilles tendinopathy is a common injury in active adults and accounts for approximately 11% of all running injuries. It is particularly prevalent in athletic and active individuals, causing functional limitations that could curtail training and participation in recreational activities for weeks to months. Weakness in the gastrocnemius muscles, rapid increases in training frequency or intensity, or decreased flexibility of the plantar flexors are all potential contributors to Achilles tendinosis.10 Rehabilitation of Achilles tendinosis involves various forms of strengthening and stretching exercises. A strengthening program that emphasizes eccentric muscle actions has been found to be particularly effective in relieving the symptoms of Achilles tendinosis and hastening the return to function.11 Several studies have shown increases in fascicle length with different resistance training protocols in healthy patients. Some have used a combination of concentric and eccentric muscle action,5,9,12 whereas others have used

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Figure 1. Ultrasound imaging is a diagnostic tool for musculoskeletal problems. Various aspects of muscle architecture are measured easily with ultrasound imaging such as muscle thickness, fascicle length, and pennation angle when the muscle is at rest or with activity.

specifically eccentric training.13 Since the fascicle length and the muscle thickness are directly related to the velocity and force of muscle contraction, this study seeks to provide evidence for the changes in muscle architecture that are known to occur with injury and rehabilitation. The purpose of this study was to determine the effect of heavy load eccentric calf muscle strength training on muscle morphology and muscle performance (strength and power) in patients with chronic Achilles tendinosis.

Methods Patients Twenty-five patients (age, 53.3 ± 17.5 years) volunteered to participate in this study. All patients were diagnosed with chronic Achilles tendinosis by fellowshiptrained subspecialty foot and ankle surgeons, based on physical palpation of a bulge 2 to 4 cm from the Achilles tendon distal attachment, associated paratendonitis crepitus, pain at and proximal to the bulge, and the inability to perform 5 single leg heel raises without pain. Two patients were diagnosed with bilateral Achilles tendinosis, and therefore, 12 limbs were

used for analysis in this study. Patients in this study were enrolled between 2008 and 2011 and were treated by physical therapists in rehabilitation departments. The study was approved by the institutional review board.

Training Protocol Pretest strength measurements included manual muscle testing of the dorsiflexors and plantarflexors and ability to complete consecutive unilateral heel raises. During the study, patients completed 8 weeks of eccentric training according to the Alfredson protocol for treatment of chronic Achilles tendinosis.14 The patient stood on the edge of a step with just the forefoot on the step. Only the uninvolved extremity was used and the patient plantarflexed the ankle to raise the body. Then, the patient shifted weight to the involved side and lowered the body until the heel was below the level of the step. To ensure that no concentric loading was performed, the participant used the noninjured leg to return to the starting position. Initially, only body weight was used. After the exercise could be completed without pain or discomfort, weight was added to a backpack.14 To ensure proper technique, participants were seen by a physical therapist for regular visits (approximately 2 times per week for an average of 9 visits). In addition to the eccentric training, patients also received manual therapy and other therapeutic exercises (gentle stretching, US, and interferential electrical stimulation) as needed in the early stages of treatment. After participants were deemed compliant on exercise performance, they were discharged from physical therapy, on average, during the third or fourth week. Patients were instructed to continue exercises at home until the end of the 8 weeks.

Ultrasound Measurements Participants were seen at the initial visit, week 4, and week 8 for data collection. Medial and lateral gastrocnemius fascicle length, pennation

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angle, and muscle thickness of the affected leg were measured using ultrasound imaging. All participants were seen at the facilities by the same investigator. All measurements were taken on either a Philips HD11 or GE Logiq E Ultrasound system with a frequency of 8.0 MHz and a 3.5-cm linear transducer. The transducer was placed directly on the skin with standard US gel as the coupling agent. The patient’s muscles were relaxed with the ankle at 90o and the knee fully extended. The medial and lateral gastrocnemii were visualized and images of the muscle fascicle on a direct diagonal from the superficial fascia to deep aponeurosis were saved. All images, void of any identifiers, were measured using digital imaging software (Image J 1.43u; National Institutes of Health, Bethesda, Maryland, USA). The medial and lateral gastrocnemius muscle fascicle length and pennation angle (fascicle to superficial fascia) were measured at 2 different times and the average of these 2 measures was used for analysis. The muscle thickness was recorded as the average of 3 measures taken at the far left, center, and far right of the image, from the perpendicular of the superficial fascia to the deep aponeurosis.

Figure 2. Medial gastrocnemius fascicle length, thickness, and pennation angle. *Fascicle length is significantly greater at 8 weeks (P < .05)

Outcomes All patients were tracked using Focus on Therapeutic Outcomes (FOTO) as a general health score. Patients completed the self-reported health questionnaire at the beginning of their rehabilitation, after completing 2 weeks of supervised physical therapy visits, and at discharge. The outcome score is reported on a scale of 0 to 100 (a score of 100 equals no physical limitations).

examine multiple comparisons. An alpha level of 0.05 was considered significant. The confidence interval was set at 95%.

Results Medial Gastrocnemius

Statistical Analysis Using SPSS 17.0, a repeated-measures analysis of variance determined differences in fascicle length, muscle thickness, and pennation angle for medial and lateral gastrocnemius muscles between time 0, 4, and 8 weeks. When significant main effects were found, a Bonferroni post hoc test was used to

Fascicle length increased from the initial measurement to week 8, on average, by 6.3 mm (P < .05) (Figure 2). No significant differences were noted between initial measurements to week 4 or from week 4 to week 8 (P > .05). Pennation angle (pre, 16.1° ± 3.6°; 8 weeks, 15.7° ± 3.7°) and muscle thickness (pre, 1.6 ± 0.4 cm; 8 weeks, 1.6

± 0.4 cm) did not change significantly throughout the weeks of rehabilitation (Figure 2).

Lateral Gastrocnemius Due to technical difficulties, only 23 of the 25 data sets were included for analysis of the lateral gastrocnemius. Neither fascicle length (pre, 4.6 ± 1.0 cm; 8 weeks, 4.8 ± 0.9 cm), pennation angle (pre, 14.7° ± 2.7°; 8 weeks, 15.5° ± 3.4°), nor muscle thickness (pre, 1.5 ± 0.5 cm; 8 weeks, 1.5 ± 0.5 cm) changed over the 8 weeks of rehabilitation (Figure 3). There was a slight increase in average fascicle length of 0.2 cm at week 8, but

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Figure 3.

Figure 4.

Lateral gastrocnemius fascicle length, thickness, and pennation angle. No change in any variable with training.

Measurement of fascicle length. Ultrasound image from medial gastrocnemius.

the difference was not statistically significant (P = .426) (Figure 3).

Outcome Data The average FOTO score recorded during the initial visit was 50.2 ± 2.5. The average score after completing the training protocol was 64.3 ± 3.2. This demonstrated a 28% improvement in FOTO scores and was a statistically significant improvement.

Conclusion Several studies have determined the efficacy of an eccentric protocol to

reduce pain and improve function in patients with Achilles tendinosis.14-16 The mechanism by which this occurs is not known. What has been reflected in recent literature is the phenomenon of increased fascicle length as a result of resistance training. Several studies have reported variable significant increases in fascicle length ranging from 4.7%12 to 34%,13 with both concentric- and eccentric-biased resistance programs (traditional rehabilitation protocol) and eccentric-only protocols.5,9,12,13 These studies examined the quadriceps and hamstring muscles of healthy patients and the examiners were primarily interested in examining the relationship

between muscle strength/cross-sectional area (CSA) and muscle architecture. Our aim was to determine if the same architectural changes would occur in an injury model, with patients participating in rehabilitation for a common muscletendon complex injury. The results indicate that medial gastrocnemius fascicle length increases as a result of eccentric training, despite Achilles tendinosis injury (Figure 4). The increase in fascicle length after 8 weeks of eccentric exercise in our study suggests an increase of sarcomeres in series. This increase of sarcomeres in series has been shown in other studies to cause a rightward shift in the muscle fascicle length-tension curve.17 Although strength was not investigated in this study, a hypothetical rightward shift of the curve has great implications for use with an injury model. If a previously injured muscle was able to operate over a greater range of the length-tension curve, it could result in prevention of subsequent injuries due to the muscle’s ability to generate greater torques at more extreme ranges of motion, where injuries typically occur.18 Again, this premise is purely speculative, as range of motion and strength were not investigated in our study. Fascicle length changes were of primary concern in this study; however, it is necessary to highlight that no other measured variables significantly changed. Other studies investigating muscle architectural changes have seen concomitant increases in pennation angle and or muscle thickness/CSA. Interesting enough, the studies that have seen significant changes in pennation angle

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and/or muscle thickness alongside increases in fascicle length used some form of concentric/eccentric muscle contraction combination in the training method.5,6,9,12 Potier, Alexander, and Seynnes13 used an eccentric-biased training protocol and saw results similar to ours. In their study, 8 weeks of eccentric training of the biceps femoris resulted in a 34% increase in fascicle length without any changes in pennation angle. It is theoretically possible that a significant increase in fascicle length with eccentric training could extend the inter-aponeurosis distance, lengthening the whole muscle; whereas, with concentric training, other architectural adaptations to the muscle are made to accommodate an increased fascicle length.13 Alternatively, our results could differ from other studies because of discrepancies in the methods used to measure fascicle length. Previous studies have measured the angle of the muscle fascicle to the deep aponeurosis,5,9,12 and we arbitrarily chose to measure the superficial angle because it was more consistent in its orientation and clarity. It is possible that the choice to use the superficial rather than the deep angle is the reason that we did not see changes in pennation angle. In addition, recent evidence suggests that foot position during heel raise exercises can selectively train the medial or lateral gastrocnemius muscle.19 It is possible that our patients were completing the heel raise exercises with the foot in an externally rotated position, which has significantly greater medial gastrocnemius muscle activation as compared to lateral gastrocnemius. Because we did not control for a neutral foot position during exercises, this could be a possible explanation for the differential response between the medial and lateral gastrocnemii. Another variable of interest in studies examining muscle architecture changes is training duration. The variation in length of resistance training programs in studies that hypothesize an increase in muscle fascicle length can range from as few as 5 weeks to as great as 52 weeks. What seems to be emerging in these studies is

that a shorter training duration is more conducive to increases in fascicle length. Seynnes, de Boer, and Narici9 saw increases in fascicle length in as little as 10 days and a significant increase of 9.9% by the end of their study, 5 weeks in total. Similarly, Blazevich et al6 saw significant increases in fascicle length at the end of 5 weeks and no further improvement with 5 additional weeks of resistance training. The results of this study and Potier et al13 seem to echo this result, with significant increases in fascicle length seen with an 8-week eccentric-biased rehabilitation program. This is promising for future research with injury models, if the implication is that less time is needed for injury rehabilitation with good functional outcomes. Several limitations exist in this study. We chose to allow for bilateral lower extremity injuries; therefore, there were no control measures of the uninjured side. In addition, our sample size was small even with efforts to increase participants by using patients with bilateral injuries. Finally, there was no assessment of patient compliance after discharge from physical therapy. Patients were seen every 2 weeks and asked about completion of exercises, but there is no way to determine if patients were performing the required number of eccentric lowering exercises at home. We also planned to compare an eccentric protocol to a traditional rehabilitation program in the same patient population to determine if our research will corroborate the results of other studies with the same resistance training method, but using an injury model rather than healthy participants. So far, it has been difficult to ethically justify such a protocol because of the significant functional improvements seen with an eccentric-biased rehabilitation program. In conclusion, irrespective of the limitations associated with this study, significant results were still evident. The data presented in this study indicate that medial gastrocnemius muscle fascicles increase in length as a result of training, which could lead to a rightward shift in

the length tension curve and possibly prevent future muscular injuries. Furthermore, more controlled studies are necessary to determine the relationship between strength, range of motion, and muscle architecture and to compare results between completion of eccentric and concentric exercises in this patient population.

References 1. Kubo K, Kanehisa H, Azuma K, et al. Muscle architectural characteristics in women aged 20-79 years. Med Sci Sports Exerc. 2003;35:39-44. 2. Chleboun GS, Busic AB, Graham KK, Stuckey HA. Fascicle length change of the human tibialis anterior and vastus lateralis during walking. J Orthop Sports Phys Ther. 2007;37:372-379. 3. Chleboun GS, France AR, Crill MT, Braddock HK, Howell JN. In vivo measurement of fascicle length and pennation angle of the human biceps femoris muscle. Cells Tissues Organs. 2001;169:401-409. 4. Ito M, Kawakami Y, Ichinose Y, Fukashiro S, Fukunaga T. Nonisometric behavior of fascicles during isometric contractions of a human muscle. J Appl Physiol (1985). 1998;85:1230-1235. 5. Alegre LM, Jimenez F, Gonzalo-Orden JM, Martin-Acero R, Aguado X. Effects of dynamic resistance training on fascicle length and isometric strength. J Sports Sci. 2006;24:501-508. 6. Blazevich AJ, Gill ND, Bronks R, Newton RU. Training-specific muscle architecture adaptation after 5-wk training in athletes. Med Sci Sports Exerc. 2003;35:2013-2022. 7. Kawakami Y, Akima H, Kubo K, et al. Changes in muscle size, architecture, and neural activation after 20 days of bed rest with and without resistance exercise. Eur J Appl Physiol. 2001;84:7-12. 8. Narici MV, Maganaris CN, Reeves ND, Capodaglio P. Effect of aging on human muscle architecture. J Appl Physiol (1985). 2003;95:2229-2234. 9. Seynnes OR, de Boer M, Narici MV. Early skeletal muscle hypertrophy and architectural changes in response to highintensity resistance training. J Appl Physiol (1985). 2007;102:368-373. 10. Chang HJ, Burke AE, Glass RM. Achilles tendinopathy. JAMA. 2010;303:188. 11. Mafi N, Lorentzon R, Alfredson H. Superior short-term results with eccentric calf muscle training compared to concentric

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training in a randomized prospective multicenter study on patients with chronic achilles tendinosis. Knee Surg Sports Traumatol Arthrosc. 2001;9:42-47. 12. Blazevich AJ, Cannavan D, Coleman DR, Horne S. Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol (1985). 2007;103:1565-1575. 13. Potier TG, Alexander CM, Seynnes OR. Effects of eccentric strength training on biceps femoris muscle architecture and knee joint range of movement. Eur J Appl Physiol. 2009;105:939-944.

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14. Alfredson H, Pietila T, Jonsson P, Lorentzon R. Heavy-load eccentric calf muscle training for the treatment of chronic achilles tendinosis. Am J Sports Med. 1998;26:360-366.

17. Reeves ND, Narici MV, Maganaris CN. In vivo human muscle structure and function: adaptations to resistance training in old age. Exp Physiol. 2004;89:675-689.

15. Kingma JJ, De Knikker R, Wittink HM, Takken T. Eccentric overload training in patients with chronic achilles tendinopathy: a systematic review. Br J Sports Med. 2007;41:e3.

18. Morgan DL, Allen DG. Early events in stretch-induced muscle damage. J Appl Physiol (1985). 1999;87:2007-2015.

16. Maffulli N, Walley G, Sayana MK, Longo UG, Denaro V. Eccentric calf muscle training in athletic patients with achilles tendinopathy. Disabil Rehabil. 2008;30:1677-1684.

19. Riemann BL, Limbaugh GK, Eitner JD, Lefavi RG. Medial and lateral gastrocnemius activation differences during heel-raise exercise with three different foot positions. J Strength Cond Res. 2011;25:634-639.

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Plantar flexor muscle architecture changes as a result of eccentric exercise in patients with Achilles tendinosis.

Eccentric training for Achilles tendinosis (AT) has been reported to significantly improve patient symptoms. There has been no biomechanical explanati...
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