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«Dissertation zur Erlangung des akademischen Grads Dr. phil. im Fach Sportwissenschaft eingereicht am 23. September 2014 an der Kultur-, Sozial- und ...»

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Human tendon adaptation in response to

mechanical loading

Dissertation

zur Erlangung des akademischen Grads

Dr. phil.

im Fach Sportwissenschaft

eingereicht am 23. September 2014

an der Kultur-, Sozial- und Bildungswissenschaftlichen Fakultät der

Humboldt-Universität zu Berlin

von

Dipl.-Sportwiss. Sebastian Bohm

Präsident der Humboldt-Universität zu Berlin:

Prof. Dr. Jan-Hendrik Olbertz

Dekanin der Kultur-, Sozial- und Bildungswissenschaftlichen Fakultät:

Prof. Dr. Julia von Blumenthal

Gutachter:

1. Prof. Dr. Adamantios Arampatzis

2. Prof. Dr. Vasilios Baltzopoulos Tag der mündlichen Prüfung: 05. Dezember 2014 Zusammenfassung Sehnen übertragen die vom Muskel erzeugten Kräfte auf das Skelett. Die Eigenschaften der Sehne beeinflussen die Leistungen des Muskels und damit unsere alltäglichen Bewegungen sowie athletische Leistungsfähigkeiten. Weiterhin reagieren Sehnen auf mechanische Belastungen durch eine Adaptation ihrer mechanischen, morphologischen und Materialeigenschaften. Allerdings sind die Effekte spezifischer Parameter des mechanischen Dehnungsstimulus sowie allgemeiner Belastungsbedingungen auf die Sehnenanpassung nicht vollständig geklärt. Die vorliegende Arbeit vertieft den derzeitigen Kenntnisstand über die Auswirkungen mechanischer Belastungen auf die Anpassung der menschlichen Sehne.

Das adaptive Potential der Sehne wurde durch einen Vergleich der Sehneneigenschaften zwischen dem dominanten und nicht dominanten Bein, in Bezug auf seitenabhängige Belastungen, experimentell untersucht. Um den Effekt verschiedener interventionsinduzierter Belastungen auf das Ausmaß der Sehnenanpassung zu bestimmen, wurde zudem ein systematischer Literaturreview nebst Metaanalyse durchgeführt. Der Einfluss spezifischer Parameter des mechanischen Dehnungsstimulus (Rate und Dauer) auf die Sehnenanpassung wurde mittels zweier Trainingsinterventionen untersucht. Magnetresonanztomographie, Ultrasonographie und Dynamometrie dienten der Quantifizierung der Sehneneigenschaften.

Der Vergleich zwischen den Achillessehneneigenschaften des dominanten und nicht dominanten Beins zeigte einen signifikanten Unterschied des Young's Modulus (Materialeigenschaften), mutmaßlich eine Konsequenz seitenabhängiger Alltagsbelastungen beider Beine (Fußdominanz). Die Metaanalyse ermittelte hohe Effektgrößen der inkludierten Interventionen auf die mechanischen und Materialeigenschaften sowie eine niedrige Effektgröße auf die morphologische Sehnencharakteristik. Die Unterschiede in den Belastungen der einzelnen Studien hatten einen Einfluss auf die adaptiven Reaktionen, wobei hohe Intensitäten einen gesteigerten Effekt zeigten. Die beiden Interventionen belegten, dass eine hohe Dehnungsrate und eine lange Dauer keinen übergeordneten Stimulus zur Sehnenanpassung im Vergleich zu einer hohen Dehnungsmagnitude und niedrigen Dehnungsfrequenz darstellen.

Die Experimentalstudien sowie die Literaturanalyse bestätigen, dass Sehnen auf ihre mechanischen Konstellationen durch eine Adaptation ihrer Eigenschaften reagieren. Weiterhin zeigen die Ergebnisse der Querschnittstudie und Metaanalyse, dass Materialeigenschaften sensitiver gegenüber Belastungsänderungen sind und im Vergleich zur Morphologie zeitiger adaptieren. Unterschiede in den Belastungen beeinflussen dabei signifikant die Magnitude der Adaptation. Die Ergebnisse der Interventionen in Kombination mit früheren Studien lassen den Schluss zu, dass eine hohe Dehnungsmagnitude, eine adäquate Dauer und repetitive Belastung essentiell für einen effektiven Stimulus sind. Die Ergebnisse liefern wichtige Erkenntnisse bezüglich einer Verbesserung von Sehneneigenschaften im Kontext der athletischen Leistung sowie Verletzungsprävention und -rehabilitation.

I Abstract Tendons are connective tissue and transmit the force exerted by a muscle to the skeleton. The properties of tendons influence the muscle output and, therefore, affect human daily locomotion as well as athletic performances. Furthermore, tendons respond to mechanical loading by changing their mechanical, material and morphological properties. However, the effect of specific parameters of the mechanical strain stimulus as well as general loading conditions on tendon adaptation is not completely understood. The present thesis aims to deepen the current knowledge about the mechanical conditions that may affect the human tendon adaptive responses in vivo.

Tendon adaptive responses were experimentally investigated by means of a comparison of tendon properties between the non-dominant and dominant leg of normally active individuals to assess the potential effect of side-dependent loading pattern. Furthermore, a systematic literature review and meta-analysis was applied to examine the effect of various interventioninduced mechanical loading conditions on the magnitude of tendon adaptive responses. To investigate the effect of specific parameters of the mechanical strain stimulus (rate and duration) on tendon adaptation, two controlled exercise interventions (14 weeks/4 times a week) were conducted. A combination of magnetic resonance imaging, dynamometry and ultrasonography was used to assess the tendon properties in the experimental studies.

The comparison of the Achilles tendon properties between the non-dominant and dominant legs revealed a significant difference of the Young's modulus (i.e. material properties), likely a result of side-dependent daily loading pattern of both legs (i.e. foot/leg dominance).





Furthermore, the meta-analysis revealed high intervention effect sizes on the tendon mechanical and material properties and a low effect size on the morphological property. Differences in the various loading conditions between studies notably affected the tendon adaptive responses, indicating e.g. a key role of high loading intensities. The two exercise interventions showed that a higher strain rate and longer strain duration did not provide a superimposed effect for tendon adaptation compared to high strain magnitude and low strain frequency.

In conclusion, the experimental and comprehensive literature analysis approach revealed that tendons respond to their mechanical environment and adapt through alterations of their properties. As indicated by the findings of the cross-sectional study and meta-analysis, the material properties seem to be more sensitive and quicker in response to changes in the mechanical loading conditions compared to the morphological properties and that variations in the loading conditions significantly affect the magnitude of the adaptation. The results of the two interventions, in combination with earlier studies, suggest that a high strain magnitude, an appropriate strain duration and repetitive loading are essential for an effective stimulus for tendons. These findings provide valuable information with regard to the improvement of tendon properties in the context of athletic performance as well as injury prevention and rehabilitation.

IITable of contents

Zusammenfassung

Abstract

List of figures

List of tables

1. Introduction and literature review

1.1 Structure and composition of tendons

1.1.1 Tendon structure

1.1.2 Tendon composition

1.2 Tendon mechanics

1.2.1 Tendon function

1.2.2 Mechanical properties of tendons

1.2.3 Functional interaction of muscle and tendon

1.2.4 Tendon mechanical properties and locomotor performance

1.3 Tendon plasticity

1.3.1 Loading-induced tendon adaptation

1.3.2 Mechanobiology of tendons

1.3.3 Tendon adaptation to chronic mechanical loading in vivo

1.4 Methodological approaches to investigate tendon properties in vivo

1.4.1 Measurement of tendon morphological properties

1.4.2 Measurement of tendon mechanical and material properties

2. Purpose of the thesis

3. First study: "Asymmetry of Achilles Tendon Mechanical and Morphological Properties Between Both Legs"

3.1 Abstract

3.2 Introduction

3.3 Methods

3.3.1 Participants

3.3.2 Measurement of mechanical properties

3.3.3 Measurement of morphological properties

3.3.4 Statistics

3.4. Results

3.5. Discussion

3.6. Perspective

3.7. Acknowledgements

3.8. References

4. Second study: "Chronic Mechanical Loading and Tendon Adaptive Responses:

A Systematic Review and Meta-Analysis"

4.1 Abstract

4.2 Introduction

III 4.3 Methods

4.3.1 Search strategy

4.3.2 Study selection and inclusion criteria

4.3.3 Methodological quality and risk of bias

4.3.4 Data extraction

4.3.5 Statistical analysis

4.4 Results

4.4.1 Literature search

4.4.2 Description of included studies

4.4.3 Methodological quality assessment

4.4.4 Meta-analysis of intervention effects

4.5 Discussion

4.6 Conclusion

4.7 References

5. Third study: "Human Achilles Tendon Plasticity in Response to Cyclic Strain:

Effect of Rate and Duration"

5.1 Abstract

5.2 Introduction

5.3 Methods

5.3.1 Subjects

5.3.2 Exercise interventions

5.3.3 Achilles tendon morphological properties

5.3.4 Achilles tendon mechanical and material properties

5.3.5 Statistics

5.4 Results

5.4.1 Intervention 1: Effect of strain rate

5.4.2 Intervention 2: Effect of strain duration

5.5 Discussion

5.6 Funding

5.7 Conflict of interest

5.8 References

6. Main findings and conclusions

6.1 Practical implications

6.1.1 Training for the improvement of tendon properties

6.1.2 Methodological considerations

6.2 Limitations

6.3 New questions and future lines of research

References

Acknowledgements

Eidesstattliche Erklärung/Statutory Declaration

–  –  –

Fig. 1.1 Schematic illustration of the multi-unit hierarchical structure of the tendon................2 Fig. 1.2 Schematic stress-strain and force-elongation relationship.

Fig. 1.3 Force-length relation of a sarcomere and sarcomere lengths during ankle bending, jumping, walking and pedaling, indicating that the tendon compliance allows the muscle fibres to contract around the plateau region of the sarcomer force-length curve (except pedaling) and, thus, enhances the force potential

Fig. 1.4 Mechanical tendon-aponeurosis properties in relation to (A) running economy and (B) athletic activity level, respectively.

Fig. 1.5 Schematic illustration of a possible mechanism for loading-induced collagen synthesis

Fig. 1.6 Intervention-induced adaptations of the Achilles tendon related to the strain frequency.

Fig. 1.7 Measurement of the tendon morphological properties (i.e. length and cross-sectional area (C)) by means of sagittal (A) and transverse (B) magnetic resonance images exemplary for the free Achilles tendon.

Fig. 1.8 Ultrasound images of the patellar (A) and Achilles (B) tendon during rest (upper) and ramped maximum voluntary contraction (deeper) with an exemplary corresponding tendon force-elongation curve (C)

Fig. 3.1 Transversal (A) and sagittal (B) magnetic resonance images of free Achilles tendon (AT) were used to investigate the morphological AT properties, i.e.

length and cross-sectional area along its length (C)

Fig. 3.2 Achilles tendon force-elongation relationship (every 100 N) and Achilles tendon stress-strain relationship (every 1 MPa) (mean ± standard error of mean) of the non-dominant and dominant leg during maximum voluntary contraction.

Fig. 3.3 Cross-sectional area (CSA) values (mean ± standard error of mean) of the free Achilles tendon from the non-dominant and dominant leg at every 10 % of tendon length (n = 36).

–  –  –

Fig. 3.5 Bland and Altman plots depicting the agreement of the non-dominant (ND) and dominant (D) leg.

Fig. 4.1 Flowchart of the systematic review process

Fig. 4.2 Forest plot for the meta-analysis.

Fig. 5.1 Loading profiles of the reference protocol (4 repetitions of 3 s loading, 3 s relaxation), the high strain rate protocol (72 one-legged jumps) and the long strain duration protocol (1 repetition of 12 s loading) of the two interventions performed for 5 sets on 4 days per week for 14 weeks, featuring similar exercise volume (integral of the plantar flexion force over time).

Fig. 5.2 Sagittal (A) and transverse (B) magnetic resonance images of free Achilles tendon (AT) were used to investigate the morphological AT properties (i.e., length and cross-sectional area (CSA), C)..

Fig. 5.3 Mean stiffness values and standard error of mean (error bars) of the Achilles tendon before (Pre-exercise) and after (Post-exercise) the intervention 1 featuring the reference and high strain rate protocol as well as for the control group.

Fig. 5.4 Mean cross-sectional area (CSA) and standard error of mean (error bars) of the Achilles tendon in 10 % intervals of the tendon length before (Preexercise) and after (Post-exercise) intervention 1 featuring the reference and high strain rate protocol, respectively

Fig. 5.5 Mean stiffness values and standard error of mean (error bars) of the Achilles tendon before (Pre-exercise) and after (Post-exercise) the intervention 2 featuring the reference and long strain duration protocol as well as for the control group.

Fig. 5.6 Mean cross-sectional area (CSA) and standard error of mean (error bars) of the Achilles tendon in 10 % intervals of the tendon length before (Preexercise) and after (Post-exercise) intervention 2 featuring the reference and long strain duration protocol, respectively.

VIList of tables

Tab. 3.1 Investigated parameters (mean ± standard deviation) of the non-dominant and dominant leg and the corresponding correlation coefficient (r) between sides (n = 36).

Tab. 4.1 Criteria of the methodological quality

Data extraction from the included studies



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