Influence of muscle fatigue on the pedaling kinetic and kinematics in different cycling protocols: a scoping review

Influência da fadiga muscular sobre a cinética e cinemática de pedalada em diferentes protocolos de ciclismo: uma revisão de escopo

Influencia de la fatiga muscular en la cinética y cinemática de pedaleo en diferentes protocolos de ciclismo: una revisión del alcance

Fábio J. Lanferdini Marco A. Vaz About the authors

ABSTRACT

The aim of this study was to review the literature on the effects of muscle fatigue generated by different cycling protocols, on the kinetics and kinematics of the crank cycle. Twenty-two studies were included in the review. The establishment of the fatigue processes caused an increase in the resulting and effective forces (all tests), together with the pedaling efficiency (incremental and constant tests). In addition, fatigue caused joint changes in the lower limbs (increased range of motion in the ankle and reduced contribution to total torque) in different cycling tests. Therefore, these pedaling strategies may be related to the maintenance of muscle work to postpone the cyclists’ exhaustion.

Keywords:
Cycling; Fatigue; Crank forces; Kinematics

RESUMO

O objetivo deste estudo foi revisar a literatura sobre os efeitos da fadiga muscular gerada por diferentes protocolos de ciclismo, sobre a cinética e cinemática do ciclo de pedalada. Vinte e dois estudos foram incluídos na revisão. A instauração dos processos de fadiga provocou aumento das forças resultante e efetiva (todos os testes), em conjunto com a eficiência de pedalada (testes incremental e constante). Além disso, a fadiga provocou mudanças articulares dos membros inferiores (aumento da amplitude articular do tornozelo e redução da sua contribuição para o torque total), em diferentes testes de ciclismo. Estas estratégias de pedalada podem estar relacionadas à manutenção do trabalho muscular para postergar a exaustão dos ciclistas.

Palavras-chave:
Ciclismo; Fadiga; Forças na pedalada; Cinemática

RESUMEN

El objetivo de este estudio fue revisar la literatura sobre los efectos de la fatiga muscular generada por diferentes protocolos de ciclismo, sobre la cinética y cinemática del ciclo de pedaleo. Veintidós estudios se incluyeron en la revisión. El establecimiento de los procesos de fatiga provocó un aumento de las fuerzas resultantes y efectivas (todas las pruebas), junto con la eficiencia del pedaleo (prueba incremental y constante). Además, la fatiga provocó cambios articulares en los miembros inferiores (mayor rango de movimiento en el tobillo y menor contribución al torque total) en diferentes pruebas de ciclismo. Estas estrategias de pedaleo pueden estar relacionadas con el mantenimiento del trabajo muscular para posponer el agotamiento de los ciclistas.

Palabras clave:
Ciclismo; Fatiga; Fuerzas en pedalear; Cinemática

INTRODUCTION

Fatigue can be defined as the inability to maintain strength or power output (PO) for the crank cycle (Rattey et al., 2006Rattey J, Martin PG, Kay D, Cannon J, Marino FE. Contralateral muscle fatigue in human quadriceps muscle: evidence for a centrally mediated fatigue response and cross-over effect. Pflugers Arch. 2006;452(2):199-207. http://dx.doi.org/10.1007/s00424-005-0027-4. PMid:16365782.
http://dx.doi.org/10.1007/s00424-005-002...
). Currently, two types of fatigue have been evidenced in the practice of endurance sports, peripheral fatigue [Catastrophic Model (Amann et al., 2013Amann M, Venturelli M, Ives SJ, McDaniel J, Layec G, Rossman MJ, et al. Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output. J Appl Physiol. 2013;115(3):355-64. http://dx.doi.org/10.1152/japplphysiol.00049.2013. PMid:23722705.
http://dx.doi.org/10.1152/japplphysiol.0...
)] and central fatigue [Central Governor Model (Noakes, 2007Noakes TD. The central governor model of exercise regulation applied to the marathon. Sports Med. 2007;37(4-5):374-7. http://dx.doi.org/10.2165/00007256-200737040-00026. PMid:17465612.
http://dx.doi.org/10.2165/00007256-20073...
)]. Central fatigue is related to a reduction of muscle activation (reduction in firing frequency and/or number of activated motor units) for the same force demand (Bigland-Ritchie and Woods, 1984Bigland-Ritchie B, Woods JJ. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve. 1984;7(9):691-9. http://dx.doi.org/10.1002/mus.880070902. PMid:6100456.
http://dx.doi.org/10.1002/mus.880070902...
). The main factors of central fatigue origin are related to muscle inhibition (reduction in the ability to activate all motor units and consequent reduction in the muscle strength production), which imposes an exercise intensity reduction by the central nervous system in order to avoid musculoskeletal injuries. Peripheral fatigue is observed both by maintaining the force produced with a concomitant muscle activation increase, or by reducing the force generated with a reduction in muscle activation during time-to-exhaustion (TTE) protocols (Amann et al., 2013Amann M, Venturelli M, Ives SJ, McDaniel J, Layec G, Rossman MJ, et al. Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output. J Appl Physiol. 2013;115(3):355-64. http://dx.doi.org/10.1152/japplphysiol.00049.2013. PMid:23722705.
http://dx.doi.org/10.1152/japplphysiol.0...
; Millet and Lepers, 2004Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med. 2004;34(2):105-16. http://dx.doi.org/10.2165/00007256-200434020-00004. PMid:14965189.
http://dx.doi.org/10.2165/00007256-20043...
). In addition, Ulmer (1996)Ulmer H-V. Concept of an extracellular regulation of muscular metabolic rate during heavy exercise in humans by psychophysiological feedback. Experientia. 1996;52(5):416-20. http://dx.doi.org/10.1007/BF01919309. PMid:8641377.
http://dx.doi.org/10.1007/BF01919309...
proposed a theoretical model of a control system for optimization of performance during heavy exercise (e.g., cycling). The model is based on a standard feedback control loop, in which the efferent signals contain information on motion, force or PO, time, and muscular metabolism, which determine muscle metabolic rate and exercise intensity. Afferent signals send feedback information from chemoreceptors and mechanoreceptors, which may be used to alter or modify movement and force of PO to optimize performance (Lambert et al., 2005Lambert EV, St Clair Gibson A, Noakes TD. Complex systems model of fatigue: integrative homoeostatic control of peripheral physiological systems during exercise in humans. Br J Sports Med. 2005;39(1):52-62. http://dx.doi.org/10.1136/bjsm.2003.011247. PMid:15618343.
http://dx.doi.org/10.1136/bjsm.2003.0112...
). Furthermore, afferent information include biomechanical feedback for optimizing the 'somatosensory' control, beyond the metabolic feedback parameters, for optimizing the metabolic control (optimal adjustment of energy consumption), and cyclists need such feedback, assuming that they possessed an extracellular feedback control system for optimal adjustment of metabolic rate (Ulmer, 1996Ulmer H-V. Concept of an extracellular regulation of muscular metabolic rate during heavy exercise in humans by psychophysiological feedback. Experientia. 1996;52(5):416-20. http://dx.doi.org/10.1007/BF01919309. PMid:8641377.
http://dx.doi.org/10.1007/BF01919309...
); Figure 1.

Figure 1
Ulmer’s hypothetical model of a control system for optimization of performance during exercise (e.g., cycling). The left panel shows simple feedback control of the motor system by the central nervous system (CNS). The right panel shows an integrative control system for optimization of performance where there are a number of different levels of control in the CNS and peripheral physiological systems (Adapted from Lambert et al., 2005Lambert EV, St Clair Gibson A, Noakes TD. Complex systems model of fatigue: integrative homoeostatic control of peripheral physiological systems during exercise in humans. Br J Sports Med. 2005;39(1):52-62. http://dx.doi.org/10.1136/bjsm.2003.011247. PMid:15618343.
http://dx.doi.org/10.1136/bjsm.2003.0112...
; and Ulmer, 1996Ulmer H-V. Concept of an extracellular regulation of muscular metabolic rate during heavy exercise in humans by psychophysiological feedback. Experientia. 1996;52(5):416-20. http://dx.doi.org/10.1007/BF01919309. PMid:8641377.
http://dx.doi.org/10.1007/BF01919309...
).

Looking in more detail at cycling, the PO produced during pedaling is the most used measure to represent the fatigue processes’ onset in TTE (Abbiss and Laursen, 2005Abbiss CR, Laursen PB. Models to explain fatigue during prolonged endurance cycling. Sports Med. 2005;35(10):865-98. http://dx.doi.org/10.2165/00007256-200535100-00004. PMid:16180946.
http://dx.doi.org/10.2165/00007256-20053...
). PO is directly related to two factors: the speed of contraction and the maximum generated force. Therefore, muscle fatigue determines a reduction in force when large, fast-twitch and rapidly fatigable motor units can no longer be recruited (reducing the maximum capacity to generate force quickly), while the units still activated have a slowness in their contractility (reducing the maximum speed of muscle shortening and joint movement), as described in Abbiss and Laursen (2005)Abbiss CR, Laursen PB. Models to explain fatigue during prolonged endurance cycling. Sports Med. 2005;35(10):865-98. http://dx.doi.org/10.2165/00007256-200535100-00004. PMid:16180946.
http://dx.doi.org/10.2165/00007256-20053...
.

Currently, three aerobic models are frequently used to investigate the mechanisms of muscle fatigue installation in cycling: (A) incremental test (IT), which consists of gradually increasing the workload until the cyclist becomes exhausted (Bini et al., 2012Bini RR, Senger D, Lanferdini F, Lopes AL. Joint kinematics assessment during cycling incremental test to exhaustion. Iso Exerc Sci. 2012;20(2):99-105. http://dx.doi.org/10.3233/IES-2012-0447.
http://dx.doi.org/10.3233/IES-2012-0447...
; Black et al., 1994Black AH, Sanderson DJ, Hennig EM. Kinematic and kinetic changes during an incremental exercise test on a bicycle ergometer. J Biomech. 1994;27(6):956. http://dx.doi.org/10.1016/0021-9290(94)90947-4.
http://dx.doi.org/10.1016/0021-9290(94)9...
); (B) constant test (CT) and sustained until exhaustion test (Diefenthaeler et al., 2012bDiefenthaeler F, Coyle EF, Bini RR, Carpes FP, Vaz MA. Muscle activity and pedal force profile of triathletes during cycling to exhaustion. Sports Biomech. 2012b;11(1):10-9. http://dx.doi.org/10.1080/14763141.2011.637125. PMid:22518941.
http://dx.doi.org/10.1080/14763141.2011....
); (C) time-trial (TT), which aims to assess the implications of muscle fatigue when the cyclist has the freedom to determine the workload in order to cover a pre-determined distance in the shortest possible time (Albertus et al., 2005 Albertus Y, Tucker R, Gibson ASC, Lambert E, Hampson DB, Noakes TD. Effect of distance feedback on pacing strategy and perceived exertion during cycling. Med Sci Sports Exerc. 2005;37(3):461-8. http://dx.doi.org/10.1249/01.MSS.0000155700.72702.76. PMid:15741846.
http://dx.doi.org/10.1249/01.MSS.0000155...
). These protocols (IT and CT) have a voluntary exhaustion criteria (Abbiss and Laursen, 2005Abbiss CR, Laursen PB. Models to explain fatigue during prolonged endurance cycling. Sports Med. 2005;35(10):865-98. http://dx.doi.org/10.2165/00007256-200535100-00004. PMid:16180946.
http://dx.doi.org/10.2165/00007256-20053...
). However, TT despite generating muscle fatigue, does not necessarily generate exhaustion, as it depends on the athlete's own perception of effort during its performance. Regardless of the experimental model of workload choice, an increase in different physiological variables related to performance (oxygen consumption, heart rate, and subjective perceived exertion) were observed after a prolonged period of cycling (Carpes et al., 2005Carpes FP, Bini RR, Nabinger E, Diefenthaeler F, Mota CB, Guimarães ACS. Aplicação de força no pedal em prova de ciclismo 40 km contra-relógio simulada: estudo preliminar. Rev Bras Educ Fís Esporte. 2005;19(2):105-13. http://dx.doi.org/10.1590/S1807-55092005000200002.
http://dx.doi.org/10.1590/S1807-55092005...
; Liedl et al., 1999Liedl MA, Swain DP, Branch JD. Physiological effects of constant versus variable power during endurance cycling. Med Sci Sports Exerc. 1999;31(10):1472-7. http://dx.doi.org/10.1097/00005768-199910000-00018. PMid:10527322.
http://dx.doi.org/10.1097/00005768-19991...
). During the TT model, it is possible to observe a voluntary PO increase at end of the test (Albertus et al., 2005 Albertus Y, Tucker R, Gibson ASC, Lambert E, Hampson DB, Noakes TD. Effect of distance feedback on pacing strategy and perceived exertion during cycling. Med Sci Sports Exerc. 2005;37(3):461-8. http://dx.doi.org/10.1249/01.MSS.0000155700.72702.76. PMid:15741846.
http://dx.doi.org/10.1249/01.MSS.0000155...
; Bini et al., 2008Bini RR, Carpes FP, Diefenthaeler F, Mota CB, Guimaraes AC. Physiological and electromyographic responses during 40-km cycling TT: relationship to muscle coordination and performance. J Sci Med Sport. 2008;11(4):363-70. http://dx.doi.org/10.1016/j.jsams.2007.03.006. PMid:17703997.
http://dx.doi.org/10.1016/j.jsams.2007.0...
; Carpes et al., 2007Carpes FP, Rossato M, Faria IE, Bolli Mota C. Bilateral pedaling asymmetry during a simulated 40-km cycling time-trial. J Sports Med Phys Fitness. 2007;47(1):51. http://dx.doi.org/10.1249/00005768-200605001-02540. PMid:17369798.
http://dx.doi.org/10.1249/00005768-20060...
). The comparison of physiological responses between different cycling protocols (e.g., IT versus TT) for the generation of muscle fatigue is difficult, because the fatigue installation process is related to the exercise type performed, increased workload, or a combination of these factors.

However, the evaluation of pedaling kinetic and kinematic parameters still needs further clarification, especially in relation to the effects of muscle fatigue on changes in pedal forces, forces acting on joints, and changes in lower limb kinematics. Nevertheless, to date, no studies have been found in the literature that reviewed the implications arising from muscle fatigue processes in the behavior of kinetic and kinematic variables during different cycling tests. Therefore, the aim of this study was to review the literature on the effects of muscle fatigue generated by different cycling protocols (IT; CT; and TT), on the kinetics (forces) and kinematics (articular angles) of crank cycling.

METHODS

Eligibility criteria

The present study is characterized by a literature scoping review (Munn et al., 2018Munn Z, Peters MDJ, Stern C, Tufanaru C, McArthur A, Aromataris E. Systematic review or scoping review? Guidance for authors when choosing between a systematic or scoping review approach. BMC Med Res Methodol. 2018;18(1):143. http://dx.doi.org/10.1186/s12874-018-0611-x. PMid:30453902.
http://dx.doi.org/10.1186/s12874-018-061...
), developed based on the quantitative and qualitative analysis of published cross-sectional experimental design articles (IT, CT and TT). Studies evaluating cyclists and triathletes, competitive or recreational, aged between 18 and 45 years, were included in this review (Ansley and Cangley, 2009Ansley L, Cangley P. Determinants of “optimal” cadence during cycling. Eur J Sport Sci. 2009;9(2):61-85. http://dx.doi.org/10.1080/17461390802684325.
http://dx.doi.org/10.1080/17461390802684...
).

Search strategy

The search for scientific articles was carried out in the PubMed, Scopus, and Google Scholar databases between 1970 and 2021. The following keywords were used to search for articles: Fatigue; Cycling; Kinematics; Kinetics; Forces; and their respective terms in Portuguese: Fadiga; Ciclismo, Cinemática, Cinética, Forças. The combination of three keywords was performed in all searches (e.g., Cycling and Fatigue and Kinematics; Cycling and Fatigue and Kinetics; Cycling and Fatigue and Forces).

Selection of studies and data extraction

Initially, the titles of the articles found with the reviewer search strategy were read. From the first selection, after reading the titles, the abstracts were read in order to obtain information about the relationship or not of the article with the topic of interest. Original articles related to the kinematics and/or kinetics (forces) of cycling during IT, CT, or TT, written in English and/or Portuguese, were included in the study, and review articles were excluded. After analyzing the abstracts and excluding those that did not fit the inclusion criteria, the other articles were fully read to be included in the present work, which should be in accordance with the pre-established eligibility criteria. Using a standardized form, information was extracted from the included studies: (1) Author and year of study; (2) Study design; (3) Participants; (4) Joanna Briggs Institute (JBI); (5) Proposed methodology; (6) Main results.

Data analysis

The studies were qualitatively analyzed, described, and tabulated according to pre-established criteria. In addition, the methodological quality classification was determined through the JBI Critical Appraisal Checklist for Analytical Cross-Sectional Studies instruments (Aromataris and Munn, 2020Aromataris E, Munn Z, editors. JBI manual for evidence synthesis. 2020. https://doi.org/10.46658/JBIMES-20-01.
https://doi.org/10.46658/JBIMES-20-01...
).

RESULTS

A total of 1019 studies were identified in the databases. After applying the exclusion criteria and eliminating duplicated studies, twenty-two studies were included in this scoping review (see the literature flow diagram on Figure 2). The studies included in this analysis are shown in Tables 1, 2, and 3, which summarize the main findings of these studies. Supplementary material (Tables 1S, 2S and 3S) demonstrated that the studies’ methodological quality was low. The main weaknesses were related to the inclusion criteria, identification and strategies to deal with confounding factors and valid and reliable outcomes measured.

Figure 2
Flow diagram of study selection.
Table 1
Summary of sample, training experience, characteristics and results from studies investigating the effects of muscle fatigue on the maximal incremental cycling test.
Table 2
Summary of sample, training experience, characteristics and results from studies investigating the effects of muscle fatigue on the constant test.
Table 3
Summary of sample, training experience, characteristics and results from studies investigating the effects of muscle fatigue on the variable workload test.

The thorough analysis of the included studies revealed that seven of these studies assessed pedaling kinetics and/or kinematics during IT (Table 1). Eight studies (Table 2) evaluated kinetic and/or kinematic parameters in cycling exhaustion tests with CT. Another experimental model commonly used for evaluating mechanical aspects of cycling fatigue is the races’ simulation in the laboratory with TT, and its results are shown in Table 3.

DISCUSSION

The present review analysis of the studies showed that muscle fatigue reduces the PO capacity and the lower limbs’ torque output during cycling. Furthermore, outcomes of this review demonstrated changes in hip, knee, and ankle joints’ excursion (such as increased range of motion and reduced ankle contribution to the joint total torque), associated with changes in the direction of the forces applied to the pedal (improved pedaling technique).

During IT, Black et al. (1994) observed an increase in the effective force (EF) applied to the pedal, with a concomitant increase in the resultant force (RF) due to the workload increase during IT. An increase in the ankle dorsiflexion angle indicated a kinematics change due to increased workload and the occurrence of fatigue (Black et al., 1994Black AH, Sanderson DJ, Hennig EM. Kinematic and kinetic changes during an incremental exercise test on a bicycle ergometer. J Biomech. 1994;27(6):956. http://dx.doi.org/10.1016/0021-9290(94)90947-4.
http://dx.doi.org/10.1016/0021-9290(94)9...
). Corroborating previous studies, Bini and Diefenthaeler (2010)Bini RR, Diefenthaeler F. Kinetics and kinematics analysis of incremental cycling to exhaustion. Sports Biomech. 2010;9(4):223-35. http://dx.doi.org/10.1080/14763141.2010.540672. PMid:21309297.
http://dx.doi.org/10.1080/14763141.2010....
found a torque increase at the plantar flexors, knee flexors, and hip flexors, without changes on the dorsiflexors and knee extensors torque during IT. In addition, the authors also found a range of motion increase at the ankle and hip joints, without changes at the knee joint with increased workload. Moreover, they evaluated the lower limb resultant joints’ torques with the aim of understanding the coordination pattern with the progressive workload increase (Black et al., 1994Black AH, Sanderson DJ, Hennig EM. Kinematic and kinetic changes during an incremental exercise test on a bicycle ergometer. J Biomech. 1994;27(6):956. http://dx.doi.org/10.1016/0021-9290(94)90947-4.
http://dx.doi.org/10.1016/0021-9290(94)9...
). Kautz et al. (1991)Kautz SA, Feltner ME, Coyle EF, Baylor AM. The pedalling technique of elite endurance cyclists: changes with increased workload at constant cadence. J Appl Biomech. 1991;7(1):29-53. http://dx.doi.org/10.1123/ijsb.7.1.29.
http://dx.doi.org/10.1123/ijsb.7.1.29...
described a sensitivity joint kinematics with the increased cycling workload (e.g., during IT). Moreover, kinematic changes were linked to the exigence of force application used by cyclists to maintain the given performance standard (Sanderson and Black, 2003Sanderson DJ, Black A. The effect of prolonged cycling on pedal forces. J Sports Sci. 2003;21(3):191-9. http://dx.doi.org/10.1080/0264041031000071010. PMid:12703848.
http://dx.doi.org/10.1080/02640410310000...
).

However, Zameziati et al. (2006)Zameziati K, Mornieux G, Rouffet D, Belli A. Relationship between the increase of effectiveness indexes and the increase of muscular efficiency with cycling power. Eur J Appl Physiol. 2006;96(3):274-81. http://dx.doi.org/10.1007/s00421-005-0077-5. PMid:16283368.
http://dx.doi.org/10.1007/s00421-005-007...
observed an increased index of effectiveness (IE) with the workload increase until voluntary exhaustion (end of test), which is explained by an improvement in the pedaling technique during the recovery phase (180-360º) of the crank cycle. These findings are explained by the better use of the muscle forces produced and the consequent improvement in the pedaling technique with the increased workload during IT. Bini and Hume (2013)Bini RR, Hume PA. Between-day reliability of pedal forces for cyclists during an incremental cycling test to exhaustion. Iso Exerc Sci. 2013;21(3):203-9. http://dx.doi.org/10.3233/IES-130510.
http://dx.doi.org/10.3233/IES-130510...
complement that the progressive workload increase results in the increase of normal and anteroposterior forces applied on the pedals. Therefore, improvement in pedaling technique may be associated with an increase in the strength demand during IT (Bini and Diefenthaeler, 2010Bini RR, Diefenthaeler F. Kinetics and kinematics analysis of incremental cycling to exhaustion. Sports Biomech. 2010;9(4):223-35. http://dx.doi.org/10.1080/14763141.2010.540672. PMid:21309297.
http://dx.doi.org/10.1080/14763141.2010....
). In addition, increased ankle joint range motion with the workload increase in both groups (cyclists and non-athletes) is due to the attempt to support the mechanical work with the increase in workload during IT (Figure 3). This increased ankle joint range motion, in turn, is necessary to increase the plantar flexor muscles’ workload and shortening speed, which are related to the muscle power increase needed (Bini et al., 2012Bini RR, Senger D, Lanferdini F, Lopes AL. Joint kinematics assessment during cycling incremental test to exhaustion. Iso Exerc Sci. 2012;20(2):99-105. http://dx.doi.org/10.3233/IES-2012-0447.
http://dx.doi.org/10.3233/IES-2012-0447...
).

Figure 3
(A) Illustration of a cyclist on the bicycle; (B) Illustration of real force vectors and magnitudes (red arrows), where it can be observed that a large part of the propulsive forces and/or output power is generated at the middle propulsion-phase (30-150°) of the crank cycle (Turpin and Watier, 2020Turpin NA, Watier B. Cycling biomechanics and its relationship to performance. Appl Sci. 2020;10(12):4112. http://dx.doi.org/10.3390/app10124112.
http://dx.doi.org/10.3390/app10124112...
); (C) Effective force (EF) during 360° of crank cycle at the start (grey) and end (black), with a decline in negative EF at the recovery-phase of the crank cycle at the end of the time-to-exhaustion or time-trial tests (Sanderson and Black, 2003Sanderson DJ, Black A. The effect of prolonged cycling on pedal forces. J Sports Sci. 2003;21(3):191-9. http://dx.doi.org/10.1080/0264041031000071010. PMid:12703848.
http://dx.doi.org/10.1080/02640410310000...
; Carpes et al., 2005Carpes FP, Bini RR, Nabinger E, Diefenthaeler F, Mota CB, Guimarães ACS. Aplicação de força no pedal em prova de ciclismo 40 km contra-relógio simulada: estudo preliminar. Rev Bras Educ Fís Esporte. 2005;19(2):105-13. http://dx.doi.org/10.1590/S1807-55092005000200002.
http://dx.doi.org/10.1590/S1807-55092005...
); (D) Schematic of lower limb kinematic and muscle activation in the middle propulsion-phase of a 90° crank cycle (Turpin and Watier, 2020Turpin NA, Watier B. Cycling biomechanics and its relationship to performance. Appl Sci. 2020;10(12):4112. http://dx.doi.org/10.3390/app10124112.
http://dx.doi.org/10.3390/app10124112...
); (E) Schematic of lower limb kinematic and muscle activation in the middle recovery-phase of 270º crank cycle (Turpin and Watier, 2020Turpin NA, Watier B. Cycling biomechanics and its relationship to performance. Appl Sci. 2020;10(12):4112. http://dx.doi.org/10.3390/app10124112.
http://dx.doi.org/10.3390/app10124112...
), showing changes in lower limb kinematics {especially increased ankle plantarflexion and/or range of motion [illustrated by the change from the original foot position (dashed red line) to the solid black line (representing increased plantar flexion of the ankle)]} at the end of incremental (Bini and Diefenthaeler, 2010Bini RR, Diefenthaeler F. Kinetics and kinematics analysis of incremental cycling to exhaustion. Sports Biomech. 2010;9(4):223-35. http://dx.doi.org/10.1080/14763141.2010.540672. PMid:21309297.
http://dx.doi.org/10.1080/14763141.2010....
) and constant workload tests (Dingwell et al., 2008Dingwell JB, Joubert JE, Diefenthaeler F, Trinity JD. Changes in muscle activity and kinematics of highly trained cyclists during fatigue. IEEE Trans Biomed Eng. 2008;55(11):2666-74. http://dx.doi.org/10.1109/TBME.2008.2001130. PMid:18990638.
http://dx.doi.org/10.1109/TBME.2008.2001...
).

In order to better understand the effects of fatigue on the muscles that act on the different joints of the lower limb during crank cycle in this model, it is important to evaluate the contribution of each joint to the absolute sum of joint moments. Mornieux et al. (2007)Mornieux G, Guenette JA, Sheel AW, Sanderson DJ. Influence of cadence, power output and hypoxia on the joint moment distribution during cycling. Eur J Appl Physiol. 2007;102(1):11-8. http://dx.doi.org/10.1007/s00421-007-0555-z. PMid:17846783.
http://dx.doi.org/10.1007/s00421-007-055...
suggest that there seems to be no change in the contribution of each joint to the absolute sum of joint moments as an effect of the fatigue installation process in TTE. The behavior of the resulting joint torques during TTE was investigated by Sanderson and Black (2003)Sanderson DJ, Black A. The effect of prolonged cycling on pedal forces. J Sports Sci. 2003;21(3):191-9. http://dx.doi.org/10.1080/0264041031000071010. PMid:12703848.
http://dx.doi.org/10.1080/02640410310000...
, who found changes in the ankle (greater plantar flexor torque), knee (greater flexor torque), and hip (greater extensor torque) joints peak torques. The only assessment made so far of the coordination pattern during cycling, through the analysis of joint torques, was described by Mornieux et al. (2007),Mornieux G, Guenette JA, Sheel AW, Sanderson DJ. Influence of cadence, power output and hypoxia on the joint moment distribution during cycling. Eur J Appl Physiol. 2007;102(1):11-8. http://dx.doi.org/10.1007/s00421-007-0555-z. PMid:17846783.
http://dx.doi.org/10.1007/s00421-007-055...
who, when re-analyzing the results of Sanderson and Black (2003)Sanderson DJ, Black A. The effect of prolonged cycling on pedal forces. J Sports Sci. 2003;21(3):191-9. http://dx.doi.org/10.1080/0264041031000071010. PMid:12703848.
http://dx.doi.org/10.1080/02640410310000...
, observed maintenance of the coordination pattern (torques contribution of each joint for the total lower limb torque) during the fatigue protocol. Similarly, only one analysis was made in relation to the behavior of joint forces, with the aim of understanding how these are influenced by the fatigue installation process. Bini et al. (2010)Bini RR, Diefenthaeler F, Mota CB. Fatigue effects on the coordinative pattern during cycling: kinetics and kinematics evaluation. J Electromyogr Kinesiol. 2010;20(1):102-7. http://dx.doi.org/10.1016/j.jelekin.2008.10.003. PMid:19028111.
http://dx.doi.org/10.1016/j.jelekin.2008...
found a decline of the ankle joint contribution on CT end, which may be related to the joint muscles’ difficulty (e.g., triceps surae) in transferring force to the pedal with fatigue. There was also an increase in torque resulting from the hip and knee joints at the end of the test, as a cyclists' strategy to maintain performance. Furthermore, Diefenthaeler et al. (2012a)Diefenthaeler F, Bini RR, Vaz MA. Análise da técnica de pedalada durante o ciclismo até a exaustão. Motriz. 2012a;18(3):476-86. http://dx.doi.org/10.1590/S1980-65742012000300008.
http://dx.doi.org/10.1590/S1980-65742012...
observed that IE did not show significant pedal force changes, indicating a pedaling technical maintenance of the applied pedal force, possibly as a strategy to maintain the workload during high intensity cycling. Changes in muscle recruitment caused by the onset of fatigue processes may generate changes in the capacity to produce force during crank cycle, possibly explaining these results (Dorel et al., 2009Dorel S, Drouet JM, Couturier A, Champoux Y, Hug F. Changes of pedaling technique and muscle coordination during an exhaustive exercise. Med Sci Sports Exerc. 2009;41(6):1277-86. http://dx.doi.org/10.1249/MSS.0b013e31819825f8. PMid:19461537.
http://dx.doi.org/10.1249/MSS.0b013e3181...
).

However, Sanderson and Black (2003)Sanderson DJ, Black A. The effect of prolonged cycling on pedal forces. J Sports Sci. 2003;21(3):191-9. http://dx.doi.org/10.1080/0264041031000071010. PMid:12703848.
http://dx.doi.org/10.1080/02640410310000...
observed an increased EF after CT until exhaustion (80% of maximal oxygen uptake), as well as a reduction in the negative EF during the recovery phase of crank cycle (Figure 3), in addition to increased hip and knee joints’ extension angles. These changes may be the result of intrinsic muscle strategies for exercise maintenance (Sanderson and Black, 2003Sanderson DJ, Black A. The effect of prolonged cycling on pedal forces. J Sports Sci. 2003;21(3):191-9. http://dx.doi.org/10.1080/0264041031000071010. PMid:12703848.
http://dx.doi.org/10.1080/02640410310000...
). Dingwell et al. (2008)Dingwell JB, Joubert JE, Diefenthaeler F, Trinity JD. Changes in muscle activity and kinematics of highly trained cyclists during fatigue. IEEE Trans Biomed Eng. 2008;55(11):2666-74. http://dx.doi.org/10.1109/TBME.2008.2001130. PMid:18990638.
http://dx.doi.org/10.1109/TBME.2008.2001...
found an association between joint range changes with muscle recruitment (assessed by means of median frequency analysis of the electromyographic signals) with the fatigue processes’ onset on lower limb muscles. Dingwell et al. (2008)Dingwell JB, Joubert JE, Diefenthaeler F, Trinity JD. Changes in muscle activity and kinematics of highly trained cyclists during fatigue. IEEE Trans Biomed Eng. 2008;55(11):2666-74. http://dx.doi.org/10.1109/TBME.2008.2001130. PMid:18990638.
http://dx.doi.org/10.1109/TBME.2008.2001...
found an increase on the ankle plantarflexion angles, without changes at knee and hip joint angles, with a median frequency reduction on the medial gastrocnemius activation (Figure 3), which is indicative of muscle fatigue (probably related to a reduction in the motor units’ action potential conduction velocity).

Therefore, fatigue mechanisms may be associated with these changes: (1) increase in the workload during IT; or (2) arrival at the end of the TTE (CT). In both tests, gastrocnemius, vasti and/or hamstrings muscles were sensitive to workload (Silva et al., 2016Silva JCL, Tarassova O, Ekblom MM, Anderson E, Rönquist G, Arndt A. Quadriceps and hamstring muscle activity during cycling as measured with intramuscular electromyography. Eur J Appl Physiol. 2016;116(9):1807-17. http://dx.doi.org/10.1007/s00421-016-3428-5. PMid:27448605.
http://dx.doi.org/10.1007/s00421-016-342...
; Pouliquen et al., 2021Pouliquen C, Nicolas G, Bideau B, Bideau N. Impact of power output on muscle activation and 3D kinematics during an incremental test to exhaustion in professional cyclists. Front Sports Act Living. 2021;10(2):e516911. http://dx.doi.org/10.3389/fspor.2020.516911. PMid:33778484.
http://dx.doi.org/10.3389/fspor.2020.516...
) or exhaustion (Dingwell et al., 2008Dingwell JB, Joubert JE, Diefenthaeler F, Trinity JD. Changes in muscle activity and kinematics of highly trained cyclists during fatigue. IEEE Trans Biomed Eng. 2008;55(11):2666-74. http://dx.doi.org/10.1109/TBME.2008.2001130. PMid:18990638.
http://dx.doi.org/10.1109/TBME.2008.2001...
; Dorel et al., 2009Dorel S, Drouet JM, Couturier A, Champoux Y, Hug F. Changes of pedaling technique and muscle coordination during an exhaustive exercise. Med Sci Sports Exerc. 2009;41(6):1277-86. http://dx.doi.org/10.1249/MSS.0b013e31819825f8. PMid:19461537.
http://dx.doi.org/10.1249/MSS.0b013e3181...
; von Tscharner, 2009von Tscharner V. Spherical classification of wavelet transformed EMG intensity patterns. J Electromyogr Kinesiol. 2009;19(5):e334-44. http://dx.doi.org/10.1016/j.jelekin.2008.07.001. PMid:18710816.
http://dx.doi.org/10.1016/j.jelekin.2008...
), especially causing an increase of the ankle joint plantarflexion range of motion (Dingwell et al., 2008Dingwell JB, Joubert JE, Diefenthaeler F, Trinity JD. Changes in muscle activity and kinematics of highly trained cyclists during fatigue. IEEE Trans Biomed Eng. 2008;55(11):2666-74. http://dx.doi.org/10.1109/TBME.2008.2001130. PMid:18990638.
http://dx.doi.org/10.1109/TBME.2008.2001...
; Bini and Diefenthaeler, 2010Bini RR, Diefenthaeler F. Kinetics and kinematics analysis of incremental cycling to exhaustion. Sports Biomech. 2010;9(4):223-35. http://dx.doi.org/10.1080/14763141.2010.540672. PMid:21309297.
http://dx.doi.org/10.1080/14763141.2010....
; Bini et al., 2012Bini RR, Senger D, Lanferdini F, Lopes AL. Joint kinematics assessment during cycling incremental test to exhaustion. Iso Exerc Sci. 2012;20(2):99-105. http://dx.doi.org/10.3233/IES-2012-0447.
http://dx.doi.org/10.3233/IES-2012-0447...
) and pedaling forces efficiency (Zameziati et al., 2006Zameziati K, Mornieux G, Rouffet D, Belli A. Relationship between the increase of effectiveness indexes and the increase of muscular efficiency with cycling power. Eur J Appl Physiol. 2006;96(3):274-81. http://dx.doi.org/10.1007/s00421-005-0077-5. PMid:16283368.
http://dx.doi.org/10.1007/s00421-005-007...
), probably postponing exhaustion in both tests (Figure 3).

Another experimental model commonly used to assess neurophysiological aspects of cycling fatigue is the simulation of tests in the laboratory, or TT (Albertus et al., 2005 Albertus Y, Tucker R, Gibson ASC, Lambert E, Hampson DB, Noakes TD. Effect of distance feedback on pacing strategy and perceived exertion during cycling. Med Sci Sports Exerc. 2005;37(3):461-8. http://dx.doi.org/10.1249/01.MSS.0000155700.72702.76. PMid:15741846.
http://dx.doi.org/10.1249/01.MSS.0000155...
; Bini and Hume, 2015Bini RR, Hume PA. Relationship between pedal force asymmetry and performance in cycling time trial. J Sports Med Phys Fitness. 2015;55(9):892-8. PMid:26470634.). This model has as an advantage in relation to the IT and CT, related to the fact that the cyclist chooses the effort intensity, enabling the investigation of the factors that determine the race pace choice (Liedl et al., 1999Liedl MA, Swain DP, Branch JD. Physiological effects of constant versus variable power during endurance cycling. Med Sci Sports Exerc. 1999;31(10):1472-7. http://dx.doi.org/10.1097/00005768-199910000-00018. PMid:10527322.
http://dx.doi.org/10.1097/00005768-19991...
). Duc et al. (2005)Duc S, Betik AC, Grappe F. EMG activity does not change during a TT in competitive cyclists. Int J Sports Med. 2005;26(2):145-50. http://dx.doi.org/10.1055/s-2004-817922. PMid:15726491.
http://dx.doi.org/10.1055/s-2004-817922...
did not find changes in lower limb muscle activation and torque during TT, suggesting that there was no central and/or peripheral fatigue in the participants evaluated. In addition, Bini et al. (2008)Bini RR, Carpes FP, Diefenthaeler F, Mota CB, Guimaraes AC. Physiological and electromyographic responses during 40-km cycling TT: relationship to muscle coordination and performance. J Sci Med Sport. 2008;11(4):363-70. http://dx.doi.org/10.1016/j.jsams.2007.03.006. PMid:17703997.
http://dx.doi.org/10.1016/j.jsams.2007.0...
observed that triathletes increased the PO and oxygen uptake at the end of TT. In addition, an increase in the vastus lateralis activation was observed throughout the test, without change of the other lower limbs muscles’ activation, indicating a type of selective activation aimed at improving performance and minimizing muscle fatigue (Bini et al., 2008Bini RR, Carpes FP, Diefenthaeler F, Mota CB, Guimaraes AC. Physiological and electromyographic responses during 40-km cycling TT: relationship to muscle coordination and performance. J Sci Med Sport. 2008;11(4):363-70. http://dx.doi.org/10.1016/j.jsams.2007.03.006. PMid:17703997.
http://dx.doi.org/10.1016/j.jsams.2007.0...
).

However, five studies found an increase in PO, RF, EF, IE, and torque at the end of the TT (Albertus et al., 2005 Albertus Y, Tucker R, Gibson ASC, Lambert E, Hampson DB, Noakes TD. Effect of distance feedback on pacing strategy and perceived exertion during cycling. Med Sci Sports Exerc. 2005;37(3):461-8. http://dx.doi.org/10.1249/01.MSS.0000155700.72702.76. PMid:15741846.
http://dx.doi.org/10.1249/01.MSS.0000155...
; Bini and Hume, 2015Bini RR, Hume PA. Relationship between pedal force asymmetry and performance in cycling time trial. J Sports Med Phys Fitness. 2015;55(9):892-8. PMid:26470634.; Bini et al., 2008Bini RR, Carpes FP, Diefenthaeler F, Mota CB, Guimaraes AC. Physiological and electromyographic responses during 40-km cycling TT: relationship to muscle coordination and performance. J Sci Med Sport. 2008;11(4):363-70. http://dx.doi.org/10.1016/j.jsams.2007.03.006. PMid:17703997.
http://dx.doi.org/10.1016/j.jsams.2007.0...
; Carpes et al., 2007Carpes FP, Rossato M, Faria IE, Bolli Mota C. Bilateral pedaling asymmetry during a simulated 40-km cycling time-trial. J Sports Med Phys Fitness. 2007;47(1):51. http://dx.doi.org/10.1249/00005768-200605001-02540. PMid:17369798.
http://dx.doi.org/10.1249/00005768-20060...
; Carpes et al., 2005Carpes FP, Bini RR, Nabinger E, Diefenthaeler F, Mota CB, Guimarães ACS. Aplicação de força no pedal em prova de ciclismo 40 km contra-relógio simulada: estudo preliminar. Rev Bras Educ Fís Esporte. 2005;19(2):105-13. http://dx.doi.org/10.1590/S1807-55092005000200002.
http://dx.doi.org/10.1590/S1807-55092005...
). These studies suggest that there are improvements in pedaling technique, and that this may be associated with better use of the generated force (e.g., RF) to generate the bicycle's propulsion. The improvement in the pedaling technique can be associated with the control of effort intensity during the test, which is increased towards the end of the test, and may be associated with greater neuromuscular efficiency (Bini et al., 2008Bini RR, Carpes FP, Diefenthaeler F, Mota CB, Guimaraes AC. Physiological and electromyographic responses during 40-km cycling TT: relationship to muscle coordination and performance. J Sci Med Sport. 2008;11(4):363-70. http://dx.doi.org/10.1016/j.jsams.2007.03.006. PMid:17703997.
http://dx.doi.org/10.1016/j.jsams.2007.0...
).

Nevertheless, Sayers et al. (2012)Sayers MG, Tweddle AL, Every J, Wiegand A. Changes in drive phase lower limb kinematics during a 60 min cycling TT. J Sci Med Sport. 2012;15(2):169-74. http://dx.doi.org/10.1016/j.jsams.2011.09.002. PMid:22018522.
http://dx.doi.org/10.1016/j.jsams.2011.0...
found an increase in hip joint extension and ankle joint dorsiflexion at the start compared to the end of the TT. Changes in the hip joint might be related to rotational changes of the pelvis. However, the authors comment that, when compared to TTE tests’ studies, there is approximately a 10º variation with a reduction in the ankle range of motion for the TT. These changes that occurred at the ankle joint appear to be related to the increased use of the stretching-shortening cycle. This mechanism may be related to the increase in the muscle shortening velocity, or even to the increased storage of elastic energy absorbed by the ankle muscles during the eccentric-phase of the crank cycle (Bini and Diefenthaeler, 2010Bini RR, Diefenthaeler F. Kinetics and kinematics analysis of incremental cycling to exhaustion. Sports Biomech. 2010;9(4):223-35. http://dx.doi.org/10.1080/14763141.2010.540672. PMid:21309297.
http://dx.doi.org/10.1080/14763141.2010....
), providing an increase in PO by the plantar flexors’ stretching-shortening cycle (Connick and Li, 2013Connick MJ, Li FX. The impact of altered task mechanics on timing and duration of eccentric bi-articular muscle contractions during cycling. J Electromyogr Kinesiol. 2013;23(1):223-9. http://dx.doi.org/10.1016/j.jelekin.2012.08.012. PMid:23010605.
http://dx.doi.org/10.1016/j.jelekin.2012...
).

CRITICAL LITERATURE ANALYSIS

The attempt to understand the fatigue installation process using the IT and CT seems to provide relevant information about the repercussions of fatigue on cycling kinetics and kinematics. However, there are few studies that sought to relate the implications of fatigue with coordination in cycling (Bini et al., 2008Bini RR, Carpes FP, Diefenthaeler F, Mota CB, Guimaraes AC. Physiological and electromyographic responses during 40-km cycling TT: relationship to muscle coordination and performance. J Sci Med Sport. 2008;11(4):363-70. http://dx.doi.org/10.1016/j.jsams.2007.03.006. PMid:17703997.
http://dx.doi.org/10.1016/j.jsams.2007.0...
; Mornieux et al., 2007Mornieux G, Guenette JA, Sheel AW, Sanderson DJ. Influence of cadence, power output and hypoxia on the joint moment distribution during cycling. Eur J Appl Physiol. 2007;102(1):11-8. http://dx.doi.org/10.1007/s00421-007-0555-z. PMid:17846783.
http://dx.doi.org/10.1007/s00421-007-055...
), which indicates a gap in the literature about the effects of fatigue on motor control during cycling. The advantage of IT and CT experimental models in relation to the TT model lies in the control of effort intensity and in the possibility of leading the evaluated cyclist, which often does not happen in the TT model (Bini et al., 2008Bini RR, Carpes FP, Diefenthaeler F, Mota CB, Guimaraes AC. Physiological and electromyographic responses during 40-km cycling TT: relationship to muscle coordination and performance. J Sci Med Sport. 2008;11(4):363-70. http://dx.doi.org/10.1016/j.jsams.2007.03.006. PMid:17703997.
http://dx.doi.org/10.1016/j.jsams.2007.0...
; Duc et al., 2005Duc S, Betik AC, Grappe F. EMG activity does not change during a TT in competitive cyclists. Int J Sports Med. 2005;26(2):145-50. http://dx.doi.org/10.1055/s-2004-817922. PMid:15726491.
http://dx.doi.org/10.1055/s-2004-817922...
). Nevertheless, the TT model makes it possible to evaluate cycling performance in ecological real situation (e.g., cycling race). Therefore, based on our review, the outcomes of muscle fatigue effects on kinematics and pedaling kinetics are still inconclusive, despite some consistent evidence discussed in this review. Therefore, we suggest that further studies should be carried out with the three different cycling tests (e.g., comparing the IT, CT and TT in the same sample), and with greater methodological rigor to strengthen the knowledge about the influence of muscle fatigue on the crank cycle’s kinetics and kinematics in cyclists.

Assessing cycling kinetics and kinematics is relatively straightforward in a laboratory set up. Miniaturization of electromyography sensors, force sensors embodied in the pedals, and increasingly accessible cameras or inertial sensors, allow researchers to provide information about the biomechanics of pedaling in real time. However, it must be emphasized that most kinetics and kinematics of cycling are difficult to interpret directly in terms of performance due to fatigue and several other conditions (e.g., muscle mechanics, discomfort, history of injuries, cyclist morphology) and nature of the effort, such as cycling race (Turpin and Watier, 2020Turpin NA, Watier B. Cycling biomechanics and its relationship to performance. Appl Sci. 2020;10(12):4112. http://dx.doi.org/10.3390/app10124112.
http://dx.doi.org/10.3390/app10124112...
).

CONCLUSION

Understanding the motor strategies adopted during the fatigue installation process in cycling involves understanding physiological, neural, and biomechanical aspects. In summary, knowing the kinetic and kinematic changes caused by fatigue processes during cycling, allows the development of strategies to optimize the transfer of mechanical energy from the segment to the crank and, therefore, delay the onset of muscle fatigue, postponing exhaustion and improving cycling performance. Outcomes of the reviewed studies demonstrated that instauration of fatigue process during cycling tests provoked increase of RF, EF and efficiency during end of tests, postponing exhaustion. Additionally, outcomes showed changes in hip, knee, and ankle joints (such as increased range of motion and reduced ankle contribution to the joint torque total) during aerobic cycling tests.

FUNDING

Supplementary Material

The Supplementary Material for this article can be found online at: 10.6084/m9.figshare.16888528

ACKNOWLEDGEMENTS

  • The present work did not have financial support of any kind for its realization.
  • The authors Fábio J. Lanferdini and Marco A. Vaz, acknowledge CAPES and CNPq for the research grants received, during the period of elaboration of the present work.

REFERENCES

  • Abbiss CR, Laursen PB. Models to explain fatigue during prolonged endurance cycling. Sports Med. 2005;35(10):865-98. http://dx.doi.org/10.2165/00007256-200535100-00004 PMid:16180946.
    » http://dx.doi.org/10.2165/00007256-200535100-00004
  • Albertus Y, Tucker R, Gibson ASC, Lambert E, Hampson DB, Noakes TD. Effect of distance feedback on pacing strategy and perceived exertion during cycling. Med Sci Sports Exerc. 2005;37(3):461-8. http://dx.doi.org/10.1249/01.MSS.0000155700.72702.76 PMid:15741846.
    » http://dx.doi.org/10.1249/01.MSS.0000155700.72702.76
  • Amann M, Venturelli M, Ives SJ, McDaniel J, Layec G, Rossman MJ, et al. Peripheral fatigue limits endurance exercise via a sensory feedback-mediated reduction in spinal motoneuronal output. J Appl Physiol. 2013;115(3):355-64. http://dx.doi.org/10.1152/japplphysiol.00049.2013 PMid:23722705.
    » http://dx.doi.org/10.1152/japplphysiol.00049.2013
  • Amoroso A, Sanderson DJ, Hennig EM. Kinematic and kinetic changes in cycling resulting from fatigue. In: XIV International Congress of Biomechanics [Internet]; 1993; Paris, France. Proceedings. Paris: ISB; 1993 p. 94-95 [cited 2021 Aug 1]. Available from: https://www.researchgate.net/publication/230824855
    » https://www.researchgate.net/publication/230824855
  • Ansley L, Cangley P. Determinants of “optimal” cadence during cycling. Eur J Sport Sci. 2009;9(2):61-85. http://dx.doi.org/10.1080/17461390802684325
    » http://dx.doi.org/10.1080/17461390802684325
  • Aromataris E, Munn Z, editors. JBI manual for evidence synthesis. 2020. https://doi.org/10.46658/JBIMES-20-01
    » https://doi.org/10.46658/JBIMES-20-01
  • Bigland-Ritchie B, Woods JJ. Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve. 1984;7(9):691-9. http://dx.doi.org/10.1002/mus.880070902 PMid:6100456.
    » http://dx.doi.org/10.1002/mus.880070902
  • Bini RR, Carpes FP, Diefenthaeler F, Mota CB, Guimaraes AC. Physiological and electromyographic responses during 40-km cycling TT: relationship to muscle coordination and performance. J Sci Med Sport. 2008;11(4):363-70. http://dx.doi.org/10.1016/j.jsams.2007.03.006 PMid:17703997.
    » http://dx.doi.org/10.1016/j.jsams.2007.03.006
  • Bini RR, Diefenthaeler F, Carpes FP, Mota CB. External work bilateral symmetry during incremental cycling exercise. In: 25th International Symposium on Biomechanics in Sports [Internet]; 2007; Ouro Preto, Brazil. Proceedings. Konstanz: ISBS; 2007. https://doi.org/10.13140/RG.2.1.4938.5846
    » https://doi.org/10.13140/RG.2.1.4938.5846
  • Bini RR, Diefenthaeler F, Mota CB. Fatigue effects on the coordinative pattern during cycling: kinetics and kinematics evaluation. J Electromyogr Kinesiol. 2010;20(1):102-7. http://dx.doi.org/10.1016/j.jelekin.2008.10.003 PMid:19028111.
    » http://dx.doi.org/10.1016/j.jelekin.2008.10.003
  • Bini RR, Diefenthaeler F. Kinetics and kinematics analysis of incremental cycling to exhaustion. Sports Biomech. 2010;9(4):223-35. http://dx.doi.org/10.1080/14763141.2010.540672 PMid:21309297.
    » http://dx.doi.org/10.1080/14763141.2010.540672
  • Bini RR, Hume PA. Between-day reliability of pedal forces for cyclists during an incremental cycling test to exhaustion. Iso Exerc Sci. 2013;21(3):203-9. http://dx.doi.org/10.3233/IES-130510
    » http://dx.doi.org/10.3233/IES-130510
  • Bini RR, Hume PA. Relationship between pedal force asymmetry and performance in cycling time trial. J Sports Med Phys Fitness. 2015;55(9):892-8. PMid:26470634.
  • Bini RR, Senger D, Lanferdini F, Lopes AL. Joint kinematics assessment during cycling incremental test to exhaustion. Iso Exerc Sci. 2012;20(2):99-105. http://dx.doi.org/10.3233/IES-2012-0447
    » http://dx.doi.org/10.3233/IES-2012-0447
  • Black AH, Sanderson DJ, Hennig EM. Kinematic and kinetic changes during an incremental exercise test on a bicycle ergometer. J Biomech. 1994;27(6):956. http://dx.doi.org/10.1016/0021-9290(94)90947-4
    » http://dx.doi.org/10.1016/0021-9290(94)90947-4
  • Carpes FP, Bini RR, Nabinger E, Diefenthaeler F, Mota CB, Guimarães ACS. Aplicação de força no pedal em prova de ciclismo 40 km contra-relógio simulada: estudo preliminar. Rev Bras Educ Fís Esporte. 2005;19(2):105-13. http://dx.doi.org/10.1590/S1807-55092005000200002
    » http://dx.doi.org/10.1590/S1807-55092005000200002
  • Carpes FP, Dagnese F, Bini RR, Diefenthaeler F, Rossato M, Mota CB, et al. Características cinemáticas da pedalada em ciclistas competitivos de diferentes modalidades. Rev Port Cienc Desporto. 2006;2006(1):7-14. http://dx.doi.org/10.5628/rpcd.06.01.07
    » http://dx.doi.org/10.5628/rpcd.06.01.07
  • Carpes FP, Rossato M, Faria IE, Bolli Mota C. Bilateral pedaling asymmetry during a simulated 40-km cycling time-trial. J Sports Med Phys Fitness. 2007;47(1):51. http://dx.doi.org/10.1249/00005768-200605001-02540 PMid:17369798.
    » http://dx.doi.org/10.1249/00005768-200605001-02540
  • Connick MJ, Li FX. The impact of altered task mechanics on timing and duration of eccentric bi-articular muscle contractions during cycling. J Electromyogr Kinesiol. 2013;23(1):223-9. http://dx.doi.org/10.1016/j.jelekin.2012.08.012 PMid:23010605.
    » http://dx.doi.org/10.1016/j.jelekin.2012.08.012
  • Diefenthaeler F, Bini RR, Vaz MA. Análise da técnica de pedalada durante o ciclismo até a exaustão. Motriz. 2012a;18(3):476-86. http://dx.doi.org/10.1590/S1980-65742012000300008
    » http://dx.doi.org/10.1590/S1980-65742012000300008
  • Diefenthaeler F, Coyle EF, Bini RR, Carpes FP, Vaz MA. Muscle activity and pedal force profile of triathletes during cycling to exhaustion. Sports Biomech. 2012b;11(1):10-9. http://dx.doi.org/10.1080/14763141.2011.637125 PMid:22518941.
    » http://dx.doi.org/10.1080/14763141.2011.637125
  • Dingwell JB, Joubert JE, Diefenthaeler F, Trinity JD. Changes in muscle activity and kinematics of highly trained cyclists during fatigue. IEEE Trans Biomed Eng. 2008;55(11):2666-74. http://dx.doi.org/10.1109/TBME.2008.2001130 PMid:18990638.
    » http://dx.doi.org/10.1109/TBME.2008.2001130
  • Dorel S, Drouet JM, Couturier A, Champoux Y, Hug F. Changes of pedaling technique and muscle coordination during an exhaustive exercise. Med Sci Sports Exerc. 2009;41(6):1277-86. http://dx.doi.org/10.1249/MSS.0b013e31819825f8 PMid:19461537.
    » http://dx.doi.org/10.1249/MSS.0b013e31819825f8
  • Duc S, Betik AC, Grappe F. EMG activity does not change during a TT in competitive cyclists. Int J Sports Med. 2005;26(2):145-50. http://dx.doi.org/10.1055/s-2004-817922 PMid:15726491.
    » http://dx.doi.org/10.1055/s-2004-817922
  • Kautz SA, Feltner ME, Coyle EF, Baylor AM. The pedalling technique of elite endurance cyclists: changes with increased workload at constant cadence. J Appl Biomech. 1991;7(1):29-53. http://dx.doi.org/10.1123/ijsb.7.1.29
    » http://dx.doi.org/10.1123/ijsb.7.1.29
  • Lambert EV, St Clair Gibson A, Noakes TD. Complex systems model of fatigue: integrative homoeostatic control of peripheral physiological systems during exercise in humans. Br J Sports Med. 2005;39(1):52-62. http://dx.doi.org/10.1136/bjsm.2003.011247 PMid:15618343.
    » http://dx.doi.org/10.1136/bjsm.2003.011247
  • Liedl MA, Swain DP, Branch JD. Physiological effects of constant versus variable power during endurance cycling. Med Sci Sports Exerc. 1999;31(10):1472-7. http://dx.doi.org/10.1097/00005768-199910000-00018 PMid:10527322.
    » http://dx.doi.org/10.1097/00005768-199910000-00018
  • Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med. 2004;34(2):105-16. http://dx.doi.org/10.2165/00007256-200434020-00004 PMid:14965189.
    » http://dx.doi.org/10.2165/00007256-200434020-00004
  • Mornieux G, Guenette JA, Sheel AW, Sanderson DJ. Influence of cadence, power output and hypoxia on the joint moment distribution during cycling. Eur J Appl Physiol. 2007;102(1):11-8. http://dx.doi.org/10.1007/s00421-007-0555-z PMid:17846783.
    » http://dx.doi.org/10.1007/s00421-007-0555-z
  • Munn Z, Peters MDJ, Stern C, Tufanaru C, McArthur A, Aromataris E. Systematic review or scoping review? Guidance for authors when choosing between a systematic or scoping review approach. BMC Med Res Methodol. 2018;18(1):143. http://dx.doi.org/10.1186/s12874-018-0611-x PMid:30453902.
    » http://dx.doi.org/10.1186/s12874-018-0611-x
  • Noakes TD. The central governor model of exercise regulation applied to the marathon. Sports Med. 2007;37(4-5):374-7. http://dx.doi.org/10.2165/00007256-200737040-00026 PMid:17465612.
    » http://dx.doi.org/10.2165/00007256-200737040-00026
  • Pouliquen C, Nicolas G, Bideau B, Bideau N. Impact of power output on muscle activation and 3D kinematics during an incremental test to exhaustion in professional cyclists. Front Sports Act Living. 2021;10(2):e516911. http://dx.doi.org/10.3389/fspor.2020.516911 PMid:33778484.
    » http://dx.doi.org/10.3389/fspor.2020.516911
  • Rattey J, Martin PG, Kay D, Cannon J, Marino FE. Contralateral muscle fatigue in human quadriceps muscle: evidence for a centrally mediated fatigue response and cross-over effect. Pflugers Arch. 2006;452(2):199-207. http://dx.doi.org/10.1007/s00424-005-0027-4 PMid:16365782.
    » http://dx.doi.org/10.1007/s00424-005-0027-4
  • Sanderson DJ, Black A. The effect of prolonged cycling on pedal forces. J Sports Sci. 2003;21(3):191-9. http://dx.doi.org/10.1080/0264041031000071010 PMid:12703848.
    » http://dx.doi.org/10.1080/0264041031000071010
  • Sayers MG, Tweddle AL, Every J, Wiegand A. Changes in drive phase lower limb kinematics during a 60 min cycling TT. J Sci Med Sport. 2012;15(2):169-74. http://dx.doi.org/10.1016/j.jsams.2011.09.002 PMid:22018522.
    » http://dx.doi.org/10.1016/j.jsams.2011.09.002
  • Silva JCL, Tarassova O, Ekblom MM, Anderson E, Rönquist G, Arndt A. Quadriceps and hamstring muscle activity during cycling as measured with intramuscular electromyography. Eur J Appl Physiol. 2016;116(9):1807-17. http://dx.doi.org/10.1007/s00421-016-3428-5 PMid:27448605.
    » http://dx.doi.org/10.1007/s00421-016-3428-5
  • Turpin NA, Watier B. Cycling biomechanics and its relationship to performance. Appl Sci. 2020;10(12):4112. http://dx.doi.org/10.3390/app10124112
    » http://dx.doi.org/10.3390/app10124112
  • Ulmer H-V. Concept of an extracellular regulation of muscular metabolic rate during heavy exercise in humans by psychophysiological feedback. Experientia. 1996;52(5):416-20. http://dx.doi.org/10.1007/BF01919309 PMid:8641377.
    » http://dx.doi.org/10.1007/BF01919309
  • von Tscharner V. Spherical classification of wavelet transformed EMG intensity patterns. J Electromyogr Kinesiol. 2009;19(5):e334-44. http://dx.doi.org/10.1016/j.jelekin.2008.07.001 PMid:18710816.
    » http://dx.doi.org/10.1016/j.jelekin.2008.07.001
  • Wiest MJ, Carpes FP, Rossato M, Mota CB. Efeito de um exercício extenuante sobre o padrão angular de pedalada: estudo preliminar. Rev Bras Cineantr Desemp Hum. 2009;11(4):386-91. http://dx.doi.org/10.1590/1980-0037.2009v11n4p386
    » http://dx.doi.org/10.1590/1980-0037.2009v11n4p386
  • Zameziati K, Mornieux G, Rouffet D, Belli A. Relationship between the increase of effectiveness indexes and the increase of muscular efficiency with cycling power. Eur J Appl Physiol. 2006;96(3):274-81. http://dx.doi.org/10.1007/s00421-005-0077-5 PMid:16283368.
    » http://dx.doi.org/10.1007/s00421-005-0077-5

Publication Dates

  • Publication in this collection
    03 Dec 2021
  • Date of issue
    2021

History

  • Received
    25 Aug 2021
  • Accepted
    29 Oct 2021
Colégio Brasileiro de Ciências do Esporte Universidade de Brasilia - Campus Universitário Darcy Ribeiro, Faculdade de Educação Física, Asa Norte - CEP 70910-970 - Brasilia, DF - Brasil, Telefone: +55 (61) 3107-2542 - Brasília - DF - Brazil
E-mail: rbceonline@gmail.com