Impact of different mechanical and metabolic stimuli on the temporal dynamics of muscle strength adaptation

Journal article


Lambrianides, Y., Epro, G., Smith, K., Mileva, K., James, D. and Karamanidis, K. (2022). Impact of different mechanical and metabolic stimuli on the temporal dynamics of muscle strength adaptation. Journal of strength and conditioning research. 36 (11), pp. 3246-3255. https://doi.org/10.1519/JSC.0000000000004300
AuthorsLambrianides, Y., Epro, G., Smith, K., Mileva, K., James, D. and Karamanidis, K.
Abstract

A fundamental task in exercise physiology is to determine and ultimately improve the adaptations that take place in the human body, an integrated network of various physiological systems e.g., muscle, tendon and bone. Investigating the temporal dynamics (time-course) of adaptations in these diverse systems may help us gain new knowledge about the functioning of the neuro-motor system in healthy and pathological conditions. The aim of this review was to explore the temporal dynamics of muscular strength adaptations in studies implementing a resistance training intervention. In addition, we categorised these studies under mechanical or metabolic stimuli to identify whether certain stimuli cause faster muscle strength gains. Searches were performed using PubMed and Google Scholar databases. The review comprised 708 participants from 57 training groups within 40 studies that met the inclusion criteria. The results revealed that the mean time point of first significant increase in muscle strength of all studies was 4.3 weeks and the corresponding increase was on average about 17%. A plateau in muscle strength increase (~25%) was found to occur between weeks 8 and 12. Categorisation into stimuli groups revealed that performing training in a hypoxic environment is likely to produce a leftward shift (~25% increase at ~2.8 weeks) in the dose-response relationship compared to blood flow restriction and supplementation. However, stimuli that cause faster muscle strength gains may also induce imbalanced adaptation between the muscle and the surrounding biological structures potentially triggering a degradation in some parts of the network (i.e., leading to an increased risk of injury).

Keywordsdose-response relationship, time-related adaptive response, resistance training 
Year2022
JournalJournal of strength and conditioning research
Journal citation36 (11), pp. 3246-3255
PublisherLippincott, Williams & Wilkins
ISSN1533-4287
Digital Object Identifier (DOI)https://doi.org/10.1519/JSC.0000000000004300
Publication dates
Print01 Jul 2022
Publication process dates
Deposited28 Jun 2022
Accepted12 Apr 2022
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Epro, G, Mierau, A, McCrum, C, Leyendecker, M, Brüggemann, G-P and Karamanidis, K (2018). Retention of gait stability improvements over 1.5 years in older adults: effects of perturbation exposure and triceps surae neuromuscular exercise. Journal of Neurophysiology. 119 (6), pp. 2229-2240. https://doi.org/10.1152/jn.00513.2017
Wide-pulse, high-frequency, low-intensity neuromuscular electrical stimulation has potential for targeted strengthening of an intrinsic foot muscle: A feasibility study
James, D.C., Solan, M.C., Mileva, K.N. and James, D. (2018). Wide-pulse, high-frequency, low-intensity neuromuscular electrical stimulation has potential for targeted strengthening of an intrinsic foot muscle: A feasibility study. Journal of Foot and Ankle Research. 11. https://doi.org/10.1186/s13047-018-0258-1
Selected B vitamins and their possible link to the aetiology of age-related sarcopenia: relevance of UK dietary recommendations.
Aytekin, N, Mileva, K. and Cunliffe, AD (2018). Selected B vitamins and their possible link to the aetiology of age-related sarcopenia: relevance of UK dietary recommendations. Nutrition Research Reviews. 31 (2), pp. 104-224. https://doi.org/10.1017/S0954422418000045
The role of muscle strength on tendon adaptability in old age
Holzer, D, Epro, G, McCrum, C, Doerner, J, Luetkens, JA, Scheef, L, Kukuk, GM, Boecker, H, Mierau, A, Brüggemann, G-P, Maganaris, CN and Karamanidis, K (2018). The role of muscle strength on tendon adaptability in old age. European Journal of Applied Physiology. https://doi.org/10.1007/s00421-018-3947-3
Matching Participants for Triceps Surae Muscle Strength and Tendon Stiffness Does Not Eliminate Age-Related Differences in Mechanical Power Output During Jumping
Koenig, M, Hemmers, S, Epro, G, McCrum, C, Ackermans, TMA, Hartmann, U and Karamanidis, K (2018). Matching Participants for Triceps Surae Muscle Strength and Tendon Stiffness Does Not Eliminate Age-Related Differences in Mechanical Power Output During Jumping. Frontiers in physiology. 9, p. 1345. https://doi.org/10.3389/fphys.2018.01345
Parameters that remain consistent independent of pausing before gait-initiation during normal rise-to-walk behaviour delineated by sit-to-walk and sit-to-stand-and-walk.
Jones, GD, James, DC, Thacker, M and Green, DA (2018). Parameters that remain consistent independent of pausing before gait-initiation during normal rise-to-walk behaviour delineated by sit-to-walk and sit-to-stand-and-walk. PLoS ONE. 13 (10). https://doi.org/10.1371/journal.pone.0205346
Positive Work Contribution Shifts from Distal to Proximal Joints during a Prolonged Run
Sanno, M, Willwacher, S, Epro, G and Brüggemann, G-P (2018). Positive Work Contribution Shifts from Distal to Proximal Joints during a Prolonged Run. Medicine and Science in Sports and Exercise. 50 (12), pp. 2507-2517. https://doi.org/10.1249/MSS.0000000000001707
Retention of improvement in gait stability over 14 weeks due to trip-perturbation training is dependent on perturbation dose
König, M, Epro, G, Seeley, J, Catalá-Lehnen, P, Potthast, W and Karamanidis, K (2018). Retention of improvement in gait stability over 14 weeks due to trip-perturbation training is dependent on perturbation dose. Journal of Biomechanics. 84, pp. 243-246. https://doi.org/10.1016/j.jbiomech.2018.12.011
Retention, savings and interlimb transfer of reactive gait adaptations in humans following unexpected perturbations
McCrum, C, Karamanidis, K, Willems, P, Zijlstra, W and Meijer, K (2018). Retention, savings and interlimb transfer of reactive gait adaptations in humans following unexpected perturbations. Communications biology. 1 (1), p. 230. https://doi.org/10.1038/s42003-018-0238-9
Deficient recovery response and adaptive feedback potential in dynamic gait stability in unilateral peripheral vestibular disorder patients.
McCrum, C, Eysel-Gosepath, K, Epro, G, Meijer, K, Savelberg, HHCM, Brüggemann, G-P and Karamanidis, K (2014). Deficient recovery response and adaptive feedback potential in dynamic gait stability in unilateral peripheral vestibular disorder patients. Physiological Reports. 2 (12), pp. 1-10. https://doi.org/10.14814/phy2.12222
Effect of long-term exercise-induced changes of the triceps surae muscle-tendon unit properties on maximal walking velocity in the elderly
Epro, G, Mierau, A, Brüggemann, G-P and Karamanidis, K (2017). Effect of long-term exercise-induced changes of the triceps surae muscle-tendon unit properties on maximal walking velocity in the elderly. 10. Jahrestagung der Deutschen Gesellschaft für Biomechanik (DGfB). Hannover, Germany 29 - 31 Mar 2017
Muscle metabolic and neuromuscular determinants of fatigue during cycling in different exercise intensity domains.
Black, MI, Blackwell, JR, Bailey, SJ, Wylie, LJ, McDonagh, STJ, Thompson, C, Kelly, J, Sumners, P, Mileva, K., Bowtell, JL and Vanhatalo, A (2017). Muscle metabolic and neuromuscular determinants of fatigue during cycling in different exercise intensity domains. Journal of Applied Physicology (1985). 122 (3), pp. 446-459. https://doi.org/10.1152/japplphysiol.00942.2016
A systematic review of gait perturbation paradigms for improving reactive stepping responses and falls risk among healthy older adults.
McCrum, C, Gerards, MHG, Karamanidis, K, Zijlstra, W and Meijer, K (2017). A systematic review of gait perturbation paradigms for improving reactive stepping responses and falls risk among healthy older adults. European Review of Aging and Physical Activity. 14, p. 3. https://doi.org/10.1186/s11556-017-0173-7
The Achilles tendon is mechanosensitive in older adults: adaptations following 14 weeks versus 1.5 years of cyclic strain exercise.
Epro, G, Mierau, A, Doerner, J, Luetkens, J, Scheef, L, Kukuk, G, Boecker, H, Maganaris, C, Brüggemann, G-P and Karamanidis, K (2017). The Achilles tendon is mechanosensitive in older adults: adaptations following 14 weeks versus 1.5 years of cyclic strain exercise. Journal of Experimental Biology. 220 (Pt 6), pp. 1008-1018. https://doi.org/10.1242/jeb.146407
Muscle and tendon adaptation in young and older adult athletes: A combined longitudinal and cross sectional investigation
Koenig, M, Epro, G, McCrum, C, Ackermans, TMA, Schade, F and Karamanidis, K (2017). Muscle and tendon adaptation in young and older adult athletes: A combined longitudinal and cross sectional investigation. 10. Jahrestagung der Deutschen Gesellschaft für Biomechanik. Hannover 29 - 31 Mar 2017
Simplified triceps surae muscle volume assessment in the elderly
Epro, G, Koenig, M, Mersmann, F, Arampatzis, A and Karamanidis, K (2017). Simplified triceps surae muscle volume assessment in the elderly. 10. Jahrestagung der Deutschen Gesellschaft für Biomechanik (DGfB). Hannover, Germany 29 - 31 Mar 2017
Associations Between Bipedal Stance Stability and Locomotor Stability Following a Trip in Unilateral Vestibulopathy
McCrum, C, Eysel-Gosepath, K, Epro, G, Meijer, K, Savelberg, HHCM, Brüggemann, G-P and Karamanidis, K (2017). Associations Between Bipedal Stance Stability and Locomotor Stability Following a Trip in Unilateral Vestibulopathy. Journal of applied biomechanics. 33 (2), pp. 112-117. https://doi.org/10.1123/jab.2016-0004
Age-related differences in drop-jump performance are eliminated by matching triceps surae muscle strength and Achilles tendon stiffness.
Koenig, M, Hemmers, S, McCrum, C, Epro, G, Ackermans, TMA, Hartmann, U and Karamanidis, K (2017). Age-related differences in drop-jump performance are eliminated by matching triceps surae muscle strength and Achilles tendon stiffness. 2017 BASES Biomechanics Interest Group (BIG) Meeting, Portsmouth. Portsmouth 19 - 19 Apr 2017
The effect of habitual athletics training on muscle and tendon adaptation in young and older elite athletes.
Koenig, M, Epro, G, McCrum, C, Bädorf, M, Schade, F and Karamanidis, K (2017). The effect of habitual athletics training on muscle and tendon adaptation in young and older elite athletes. 2017 BASES Biomechanics Interest Group (BIG) Meeting, Portsmouth. Portsmouth 19 - 19 Apr 2017
Effect Of Triceps Surae Muscle-Tendon Unit Mechanical Properties On Gait Stability And Adaptability In Older Female Adults
Epro, G, McCrum, C, Mierau, A, Leyendecker, M, Brüggemann, G-P and Karamanidis, K (2017). Effect Of Triceps Surae Muscle-Tendon Unit Mechanical Properties On Gait Stability And Adaptability In Older Female Adults. BASES Biomechanics Interest Group (BIG) Meeting 2017. Portsmouth, UK 19 - 19 Apr 2017
Achilles tendon is mechanosensitive in old adults: a 1.5 year resistance training intervention
Epro, G, Mierau, A, Doerner, J, Luetkens, J, Scheef, L, Kukuk, G, Boecker, H, Maganaris, C and Karamanidis, K (2017). Achilles tendon is mechanosensitive in old adults: a 1.5 year resistance training intervention. BASES Biomechanics Interest Group (BIG) Meeting 2017. Portsmouth, UK 19 - 19 May 2017
Matching triceps surae muscle strength and tendon stiffness eliminates age-related differences in drop-jump performance
Koenig, M, Hemmers, S, McCrum, C, Epro, G, Ackermans, TMA, Hartmann, U and Karamanidis, K (2017). Matching triceps surae muscle strength and tendon stiffness eliminates age-related differences in drop-jump performance. 35th International Conference on Biomechanics in Sports. Cologne 14 - 18 Jun 2017
Muscle-tendon adaptation monitoring in elite athletes: Preliminary results from a longitudinal investigation
Epro, G, Koenig, M, McCrum, C, Baedorf, M, Schade, F and Karamanidis, K (2017). Muscle-tendon adaptation monitoring in elite athletes: Preliminary results from a longitudinal investigation. 35th Conference of the International Society of Biomechanics in Sport. Cologne, Germany 14 - 18 Jun 2017
Loading rate and contraction type effects on the human Achilles tendon force-elongation relationship
McCrum, C, Oberländer, KD, Epro, G, Krauss, P, Reeves, N and Karamanidis, K (2017). Loading rate and contraction type effects on the human Achilles tendon force-elongation relationship. 22nd Annual Congress of the European College of Sport Science. Essen, Germany 05 - 08 Jul 2017
Monitoring muscle-tendon adaptation in elite athletes: Preliminary data from a 1-year longitudinal investigation
Koenig, M, Epro, G, McCrum, C, Bädorf, M, Schade, F and Karamanidis, K (2017). Monitoring muscle-tendon adaptation in elite athletes: Preliminary data from a 1-year longitudinal investigation. 22nd annual Congress of the European College of Sport Science (ECSS). Essen 05 - 08 Jul 2017
Achilles tendon mechanosensitivity is preserved in old age: In vivo evidence from a 1.5 years long resistance training intervention
Epro, G, Mierau, A, Doerner, J, Luetkens, J, Scheef, L, Kukuk, G, Boecker, H, Maganaris, C, Brüggemann, G-P and Karamanidis, K (2017). Achilles tendon mechanosensitivity is preserved in old age: In vivo evidence from a 1.5 years long resistance training intervention. 22nd annual Congress of the European College of Sport Science. Essen, Germany 05 - 08 Jul 2017
Loading rate and contraction duration effects on in vivo human Achilles tendon mechanical properties.
McCrum, C, Oberländer, KD, Epro, G, Krauss, P, James, DC, Reeves, N and Karamanidis, K (2017). Loading rate and contraction duration effects on in vivo human Achilles tendon mechanical properties. Clinical Physiology and Functional Imaging. 38 (3), pp. 517-523. https://doi.org/10.1111/cpf.12472
Locomotor stability and adaptation during perturbed walking across the adult female lifespan.
McCrum, C, Epro, G, Meijer, K, Zijlstra, W, Brüggemann, G-P and Karamanidis, K (2016). Locomotor stability and adaptation during perturbed walking across the adult female lifespan. Journal of Biomechanics. 49 (7), pp. 1244-1247. https://doi.org/10.1016/j.jbiomech.2016.02.051
Use of a Lucas-Kanade-Based Template Tracking Algorithm to Examine In Vivo Tendon Excursion during Voluntary Contraction Using Ultrasonography.
Karamanidis, K, Travlou, A, Krauss, P and Jaekel, U (2016). Use of a Lucas-Kanade-Based Template Tracking Algorithm to Examine In Vivo Tendon Excursion during Voluntary Contraction Using Ultrasonography. Ultrasound in Medicine and Biology. 42 (7), pp. 1689-1700. https://doi.org/10.1016/j.ultrasmedbio.2016.02.019
Visual and proprioceptive contributions to postural control of upright stance in unilateral vestibulopathy.
Eysel-Gosepath, K, McCrum, C, Epro, G, Brüggemann, G-P and Karamanidis, K (2016). Visual and proprioceptive contributions to postural control of upright stance in unilateral vestibulopathy. Somatosensory and Motor Research. 33 (2), pp. 72-78. https://doi.org/10.1080/08990220.2016.1178635
Sit-to-walk and sit-to-stand-and-walk task dynamics are maintained during rising at an elevated seat-height independent of lead-limb in healthy individuals
Jones, GD, James, DC, Thacker, M, Jones, EJ and Green, DA (2016). Sit-to-walk and sit-to-stand-and-walk task dynamics are maintained during rising at an elevated seat-height independent of lead-limb in healthy individuals. Gait and Posture. 48 (July), pp. 226 - 229. https://doi.org/10.1016/j.gaitpost.2016.06.005
Sit-to-stand-and-walk from 120% knee height: A novel approach to assess dynamic postural control independent of lead-limb
Jones, GD, James, DC, Thacker, M and Green, DA (2016). Sit-to-stand-and-walk from 120% knee height: A novel approach to assess dynamic postural control independent of lead-limb. Journal of Visualized Experiments. 2016 (114). https://doi.org/10.3791/54323
Matching participants for triceps surae mechanical properties eliminates age-related differences in drop jump performance
Koenig, M, Hemmers, S, McCrum, C, Epro, G, Ackermans, TMA, Hartmann, U and Karamanidis, K (2016). Matching participants for triceps surae mechanical properties eliminates age-related differences in drop jump performance. 11th Joint Conference on Motor Control & Learning, Biomechanics & Training of the German Society of Sports Sciences. Darmstadt, Germany 28 - 30 Sep 2016
Aging and the effects of a half marathon on Achilles tendon force-elongation relationship.
Ackermans, TMA, Epro, G, McCrum, C, Oberländer, KD, Suhr, F, Drost, MR, Meijer, K and Karamanidis, K (2016). Aging and the effects of a half marathon on Achilles tendon force-elongation relationship. European Journal of Applied Physiology. 116 (11-12), pp. 2281-2292. https://doi.org/10.1007/s00421-016-3482-z
Age-related differences in drop jump performance are eliminated when triceps surae mechanical properties are matched
Koenig, M, Hemmers, S, McCrum, C, Epro, G, Ackermans, TMA, Hartmann, U and Karamanidis, K (2016). Age-related differences in drop jump performance are eliminated when triceps surae mechanical properties are matched. Dutch Society for Movement Sciences (VvBN) PhD Day 2016. Maastricht 09 - 09 Nov 2016
The biomechanical characteristics of wearing FitFlop™ sandals highlight significant alterations in gait pattern: a comparative study.
James, DC, Farmer, LJ, Sayers, JB, Cook, DP and Mileva, K. (2015). The biomechanical characteristics of wearing FitFlop™ sandals highlight significant alterations in gait pattern: a comparative study. Clinical Biomechanics. 30 (4), pp. 347-354. https://doi.org/10.1016/j.clinbiomech.2015.02.016
47 An acute session of high-frequency, low-intensity, wide-pulse electrical stimulation evokes fatigue adaptations in an intrinsic foot muscle
James, DC, Mileva, K. and Solan, MC (2015). 47 An acute session of high-frequency, low-intensity, wide-pulse electrical stimulation evokes fatigue adaptations in an intrinsic foot muscle. British Journal of Sports Medicine. 49 (Suppl). https://doi.org/10.1136/bjsports-2015-095573.47
Low-frequency accelerations over-estimate impact-related shock during walking.
James, DC, Mileva, K. and Cook, DP (2014). Low-frequency accelerations over-estimate impact-related shock during walking. Journal of Electromyography and Kinesiology. 24 (2), pp. 264-270. https://doi.org/10.1016/j.jelekin.2013.12.008
Effect of exercise-induced enhancement of the leg-extensor muscle-tendon unit capacities on ambulatory mechanics and knee osteoarthritis markers in the elderly.
Karamanidis, K, Oberländer, KD, Niehoff, A, Epro, G and Brüggemann, G-P (2014). Effect of exercise-induced enhancement of the leg-extensor muscle-tendon unit capacities on ambulatory mechanics and knee osteoarthritis markers in the elderly. PLoS ONE. 9 (6). https://doi.org/10.1371/journal.pone.0099330
Experimental evidence of the tonic vibration reflex during whole-body vibration of the loaded and unloaded leg
Zaidell, L., Mileva, K., Sumners, D.P. and Bowtell, J. (2013). Experimental evidence of the tonic vibration reflex during whole-body vibration of the loaded and unloaded leg. PLoS ONE. 8 (12), p. e85247. https://doi.org/10.1371/journal.pone.0085247
Effect of Hypohydration on Peripheral and Corticospinal Excitability and Voluntary Activation
Bowtell, JL, Avenell, G, Hunter, SP and Mileva, K. (2013). Effect of Hypohydration on Peripheral and Corticospinal Excitability and Voluntary Activation. PLoS ONE. 8 (10), p. e77004. https://doi.org/10.1371/journal.pone.0077004
Repeated sprint training in normobaric hypoxia
Cooke, K, Galvin, HM, Sumners, DP, Mileva, K. and Bowtell, JL (2013). Repeated sprint training in normobaric hypoxia. British Journal of Sports Medicine. 47, pp. i74-i79. https://doi.org/10.1136/bjsports-2013-092826
Wide-pulse electrical stimulation to an intrinsic foot muscle induces acute functional changes in forefoot-rearfoot coupling behaviour during walking.
James, D.C., Chesters, T., Sumners, D.P., Cook, D.P., Green, D.A. and Mileva, K. (2012). Wide-pulse electrical stimulation to an intrinsic foot muscle induces acute functional changes in forefoot-rearfoot coupling behaviour during walking. International Journal of Sports Medicine. 34 (5), pp. 438-443. https://doi.org/10.1055/s-0032-1321893
Coefficient of cross correlation analysis of kinematics during walking barefoot and in Vibram FiveFingers®
James, DC and Cook, D (2011). Coefficient of cross correlation analysis of kinematics during walking barefoot and in Vibram FiveFingers®. Footwear Science. 3 (SUP 1), pp. S79-S81. https://doi.org/10.1080/19424280.2011.575401