Skip to main content

Downhill Running: What Are The Effects and How Can We Adapt? A Narrative Review

Abstract

Downhill running (DR) is a whole-body exercise model that is used to investigate the physiological consequences of eccentric muscle actions and/or exercise-induced muscle damage (EIMD). In a sporting context, DR sections can be part of running disciplines (off-road and road running) and can accentuate EIMD, leading to a reduction in performance. The purpose of this narrative review is to: (1) better inform on the acute and delayed physiological effects of DR; (2) identify and discuss, using a comprehensive approach, the DR characteristics that affect the physiological responses to DR and their potential interactions; (3) provide the current state of evidence on preventive and in-situ strategies to better adapt to DR. Key findings of this review show that DR may have an impact on exercise performance by altering muscle structure and function due to EIMD. In the majority of studies, EIMD are assessed through isometric maximal voluntary contraction, blood creatine kinase and delayed onset muscle soreness, with DR characteristics (slope, exercise duration, and running speed) acting as the main influencing factors. In previous studies, the median (25th percentile, Q1; 75th percentile, Q3) slope, exercise duration, and running speed were − 12% (− 15%; − 10%), 40 min (30 min; 45 min) and 11.3 km h−1 (9.8 km h−1; 12.9 km h−1), respectively. Regardless of DR characteristics, people the least accustomed to DR generally experienced the most EIMD. There is growing evidence to suggest that preventive strategies that consist of prior exposure to DR are the most effective to better tolerate DR. The effectiveness of in-situ strategies such as lower limb compression garments and specific footwear remains to be confirmed. Our review finally highlights important discrepancies between studies in the assessment of EIMD, DR protocols and populations, which prevent drawing firm conclusions on factors that most influence the response to DR, and adaptive strategies to DR.

FormalPara Key Points
Due to its eccentric nature, downhill running (DR) induces lower limb muscle damage, manifested by alterations in muscle structure, muscle function, and ensuing running performance for up to several days after exercise.
Manipulating DR characteristics (slope, running speed, and duration), independently or not, can influence the extent of exercise-induced muscle damage (EIMD). Although trained and/or accustomed people generally experience less muscle damage following DR, it is still unknown if sex and/or age may influence the adaptation to DR.
Scientific evidence suggests preventive strategies that consist of prior exposure to DR to limit the extent of muscle damage induced by DR.
Evidence is lacking to support the use of in-situ strategies such as compression garments, specific footwear, or modification in running stride to limit muscle damage induced by DR, which highlights the need for further high-quality research.

Introduction

Eccentric muscle contractions occur when the magnitude of the force applied to the muscle exceeds the strength produced by the muscle itself (i.e. negative work), resulting in a lengthening action of the musculotendinous system. Eccentric muscle contractions are known to induce high mechanical strain on the musculotendinous system, leading to moderate to severe exercise-induced muscle damage (EIMD) [1].

In laboratory settings, local (i.e. single muscle group tested with an isokinetic dynamometer) and whole-body eccentric-based models such as eccentric cycling and downhill running (DR) have been used to examine the physiological consequences of eccentric muscle actions and/or EIMD [2]. For example, intense and/or prolonged DR is well-known to induce muscle functional alterations [3]. More precisely, DR generally leads to substantial neuromuscular fatigue which can originate from both peripheral and central mechanisms. The peripheral component of neuromuscular fatigue may be attributed to longer muscle length (i.e. overstretched sarcomeres) during eccentric muscle actions over braking phases, leading to myofibrillar damage such as disrupted weaker sarcomeres and/or excitation–contraction coupling failure [1, 4]. The central component of neuromuscular fatigue may be attributed to spinal and/or supraspinal factors [5, 6]. Thus, the DR modality has often been used for different purposes including: (1) studying the recovery kinetics of physical performance following muscle damage (e.g. [7,8,9]); (2) testing the reliability and validity of varied techniques to assess EIMD (e.g. [6, 10]); (3) studying the effects of strenuous exercise on physiological adaptations and/or alterations (e.g. [11,12,13]); (4) testing different strategies to attenuate EIMD and/or improve subsequent recovery (e.g. [14,15,16]).

In a sporting context, DR sections can be part of off-road running races mostly taking place in natural environment and unsealed roads (e.g. trail running, mountain running, fell running and cross-country running, orienteering, obstacle course racing or ultramarathon running, [17]) or road running races including downhill sections (e.g. the St. George marathon, St George, USA; the Holualoa Tuscon marathon, Tuscon, USA; the Big Sur International marathon, Big Sur, USA) [18, 19]. Due to its eccentric-based muscle action modality, DR may play a major role in the occurrence of neuromuscular fatigue (especially due to peripheral factors) and muscle damage, and thus represents a main challenge for runners. For example, the maximal strength production capacity of lower-limb muscles (i.e. knee extensors, KE, and plantar flexors, PF), often assessed through isometric maximal voluntary contraction (MVC) is generally dramatically reduced (− 15 to − 40%) following trail running races (i.e. the most popular off-road running races, taking place in natural environment over a variety of terrains with minimal paved or asphalt roads; for review, [17]) (e.g. [19,20,21,22]). Although DR characteristics (running speed and/or intensity, running duration and slope) vary among running disciplines, they do not predispose to the extent of an alteration in strength production capacity [3, 23]. For example, comparable force/torque losses and peripheral alterations were reported following a 6.5 km DR at maximal speed (altitude drop: 1264 m; average slope: − 16.8%) and in ultra-marathons (i.e. > 42.195 km) in experienced trail runners (for review, [3]). In line with these observations, it has been suggested that performance in trail running is largely influenced by the demanding nature of graded sections (especially DR sections where eccentric muscle actions are predominant), leading to EIMD including neuromuscular fatigue [3]. The same hypothesis may be applied to other running disciplines that include notable DR sections.

On the other hand, DR could be used during specific training periods to improve running performance via neural and musculotendinous adaptations. Some narrative reviews have focused on the physiological and/or biomechanical adaptations to trail running and/or prolonged graded running [18, 23]. However, a comprehensive analysis of the effects of DR on both in-situ physiological responses and recovery kinetics (i.e. acute and delayed physiological responses and EIMD markers) according to training level is lacking. In parallel, anecdotal data from field observations and a growing number of research studies show an interest in strategies to facilitate the adaptation to DR, namely reduce EIMD. These strategies include for example, DR training, wearing compression garments and using specific footwear, though it is difficult to draw conclusions due to the variety of results.

Within this framework, the purpose of this narrative review is threefold: (1) to further our understanding of the physiological responses to DR; (2) to identify and discuss, using a comprehensive approach, the DR characteristics that affect the physiological responses to DR and their potential interactions; (3) to provide a synthesis of evidence on strategies to better tolerate DR by limiting EIMD. Manuscripts were acquired by searching the electronic databases of the US National Library of Medicine (PubMed), ScienceDirect and SPORTDiscus using the following keywords: “running” AND “downhill” OR “decline” OR “grade” OR “gradient” OR “slope” OR “muscle damage” OR “muscle fatigue” OR “biomechanics” OR “strategy” OR “compression garment” OR “running garment” OR “preconditioning” OR “training” OR “repeated bout effect” OR “footwear”. Electronic database searching was supplemented by examining reference sections of relevant articles (i.e. hand search). The literature search was conducted up to March 2020. In the entire manuscript, we limited our analysis to studies including DR only as a modality of whole-body eccentric-biased exercise, with human participants only. We did not consider studies using other means (e.g. steps, one-legged DR, sprint-assisted DR, eccentric cycling or eccentric muscle actions on isokinetic dynamometer) of generating muscle damage or eccentric muscle actions. In studies including DR exercises that also tested a nutritional strategy or a strategy to limit EIMD, only the placebo groups (with no strategy) were included in the analyses performed in the second part of the manuscript to identify and discuss DR factors responsible for EIMD and their interaction. No limit to the search domain was applied regarding population characteristics, training level, and DR characteristics (i.e. running speed and/or intensity, exercise duration, and slope). In the present review, the generic term ‘EIMD” refers to direct markers of muscle damage including ultrastructural alterations (e.g. myofibrillar disruption) as well as indirect markers such as physiological (e.g. systemic efflux of myocellular enzymes and proteins), perceptual (e.g. delayed onset muscle soreness) and functional alterations (e.g. loss in MVC force/torque) following DR [24]. Functional alterations refer to the concept of “neuromuscular fatigue” defined as any exercise-induced reduction in voluntary maximal force or power [25].

Muscular Alterations Following Downhill Running

Grade-specific biomechanical and neuromuscular alterations occur in running (for review, [18]). When compared to level running, DR is characterized by repeated and prolonged eccentric muscle actions of lower-limb muscles [14, 24], lowered capacity of the stretch–shortening cycle [26, 27], alterations in foot strike pattern (usually rear-foot strike pattern, i.e. heel contacts first) [27,28,29], changes in ground reaction forces (larger normal impact force and greater parallel braking force compared to level running, whatever the slope studied) [27, 30], specific mechanical energy fluctuations of the centre of mass during each stride (e.g. greater negative external work and lower positive external work, i.e. the work done to decelerate and accelerate the body’s centre of mass with respect to the environment, respectively) [26, 29, 31,32,33,34], and alterations in impact shock attenuation (e.g. greater tibial acceleration) [27, 33, 35,36,37]. Those grade-specific alterations originate from the greater mechanical strain applied to the lower-limb musculoskeletal system during the foot–ground contact time in DR, which may lead to accentuated acute and delayed EIMD (e.g. structural muscle alterations, leakage of specific-muscle proteins into the bloodstream, reduction in MVC force/torque) [3, 38], and consequently alteration in running economy (RE) and performance [3, 18]. As such, a better understanding of these alterations following DR is the first stage in our aim to investigate the DR characteristics responsible for such alterations, and adaptative strategies.

Structural Muscular Alterations Following Downhill Running

The presence of EIMD following strenuous exercise can be assessed through histological analysis of biopsy samples and magnetic resonance imaging (MRI) of muscle groups (KE and PF are the muscle groups the most investigated) involved in DR. Myofibrillar disruptions and necrosis in lower-limb (e.g. vastus lateralis) muscles are generally reported after eccentric exercise [39]. Following 30-min treadmill DR (slope: − 12%; intensity: 80% of maximal aerobic velocity recorded on level grade), Féasson et al. [40] reported important ultrastructural muscular alterations in the vastus lateralis of healthy males. These alterations included streaming, disruption and dissolution of Z-disk structures associated with A-band disruption and misalignment of myofibrils, and disturbances of the cross-striated band pattern along the longitudinal sections. Increases in skeletal muscle mRNA expression of several inflammation-related genes, increases in pro-inflammatory cytokine concentration, and satellite cells proliferation in KE muscles were also reported after DR [41, 42]. Using MRI, Maéo et al. [43] also reported structural muscular alterations (i.e. local inflammatory oedema estimated via transverse relaxation time, T2) in both KE and PF muscle groups following 45-min treadmill DR (slope: − 15%; average speed: 10.0 km h−1) in healthy young adults.

The important leakage of muscle-specific proteins (creatine kinase, CK; myoglobin, Mb; and lactate dehydrogenase, LDH) into the blood, accompanied by increases in muscle Ca2+ and K+ content following strenuous exercise, are also considered common indirect markers of EIMD [44,45,46,47]. Two main mechanisms could explain this efflux of muscle-specific proteins into the blood stream. Firstly, muscle fibres may exhibit an increased membrane permeability following an increase in cytoplasmatic Ca2+ through an inhibition of the Ca2+ pump that actively transports Ca2+ out of the cell, thus promoting the activation of the K+ channel and leading to membrane damage [48]. In addition, this could be explained by local tissue damage induced by the eccentric muscle actions which may cause a degeneration of the muscle structure [49]. Peake et al. [50] reported a large increase (+ 1800%) in plasma Mb concentration 1-h post-DR (45 min at 60% \(\dot{V}{\text{O}}_{{{\text{2max}}}}\), − 10% slope; with \(\dot{V}{\text{O}}_{{{\text{2max}}}}\) corresponding to the maximal aerobic capacity) followed by a large increase (+ 420%) in plasma CK concentration 24-h post-DR in well-trained runners. This efflux of muscle-specific proteins into the blood stream may persist for several days following DR. For example, Malm et al. [38] reported a significant efflux of serum CK (+ 150%) up to 7 days following DR.

These structural muscular alterations occurring during DR may be accompanied by MVC force/torque decrements [51, 52] and thus, reflect the level of neuromuscular fatigue [25]. Since the manifestation of MVC force/torque loss and structural muscular alteration are concomitant [53, 54], it appears important to discuss their relationship.

Functional Muscular Alterations Following Downhill Running

Loss of MVC force/torque is commonly used to assess the global state of neuromuscular fatigue that may originate from both peripheral and central levels [25]. Because the extent of force/torque loss is also influenced by the number of muscle fibres suffering from myofibrillar disruption and/or excitation–contraction failure [49, 53, 55,56,57], it may provide information on the extent of EIMD [54]. The reduction in MVC force/torque may depend on the exercise modality (i.e. grade), exercise characteristics (duration, running speed and/or intensity) and population characteristics (age, sex, training level). For example, Garnier et al. [58] reported greater decrements in isokinetic (concentric and eccentric) MVC torque of KE, accompanied by a greater occurrence of the peripheral component of neuromuscular fatigue, in-situ perceived exertion (in gluteus muscles) and delayed muscle pain (in KE, PF and gluteus) following a 45-min DR bout, compared to uphill and level running bouts performed at the same relative intensity (same reserve heart rate, HR).

Immediately after DR, large reductions in isometric MVC force/torque of KE and PF muscles are generally reported, and may vary from − 14 to − 55% for KE [5, 9, 10, 15, 38, 43, 58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87] and from − 15 to − 25% for PF [9, 15, 43]. Similarly, a decline in muscle performance (expressed as MVC force/torque loss or endurance capacity) was reported during isokinetic muscle actions (tested from 0.52 to 5.2 rad s−1 and from 0.52 to 2.6 rad s−1 for concentric and eccentric modalities, respectively) [58, 88, 89], dynamic strength measurement such as counter movement jump [15, 90] and muscle endurance test [91]. Decrements in MVC force/torque generally last up to 4–5 days before complete recovery [38, 70, 73, 92].

DR is well-known to alter muscle structure and to induce neuromuscular fatigue. More specifically, the acute reduction in MVC force/torque following DR is typically associated with a reduction in maximal central drive (i.e. a mechanism associated with a central component of neuromuscular fatigue, assessed via maximal voluntary activation, VA; from − 2.5 to − 8% in KE and PF; [9, 10, 15]) and the so-called “low-frequency fatigue”. The latter (usually investigated via muscle or nerve electrical stimulation) manifests through a decrease of the low (10–20 Hz)-to-high (50–100 Hz) frequency doublet ratio [93], reflecting a reduction in Ca2+ release from the sarcoplasmic reticulum [93]. It is thus likely that the failure in excitation–contraction coupling is mostly responsible for the occurrence of the peripheral component of neuromuscular fatigue following DR. In addition, the acute reduction in maximal central drive immediately after DR may contribute to the acute reduction in MVC force/torque. Such reduction in VA may originate from the spinal and/or supraspinal level, with for instance a role of reflexes mediated by muscle III-IV afferents that may reduce the recruitment and/or firing rates of motoneurons [25]. In previous studies, the reduction in maximal central drive was usually observed through peripheral nerve stimulation (PNS). However, PNS does not allow quantification of the source of drive to the motoneurons making unclear the relative contribution of spinal and supraspinal components in the reduction of MVC force/torque. Bulbulian and Bowles [7] investigated the spinal component using the Hoffman reflex (H-reflex) expressed as a ratio of the maximal electrically stimulated muscle action potential (Hmax/Mmax ratio). The authors reported a reduction in Hmax/Mmax ratio following a 20-min DR (slope: − 10%; intensity: 50% \(\dot{V}{\text{O}}_{{{\text{2max}}}}\)) reflecting a reduction in motoneuron pool excitability, in higher proportion compared to a level bout (e.g. − 24.6% versus − 9.3%, respectively) performed at a comparable metabolic cost (expressed as %\(\dot{V}{\text{O}}_{{{\text{2max}}}}\)). It is possible that repeated and/or prolonged eccentric muscle actions could potentially damage muscle spindles [94, 95], which may impair motoneuron excitability by reducing Ia afferents input to the motoneuron pool. However, the H-reflex does not allow inferences on the potential role of supraspinal mechanisms implicated in the reduction of MVC force/torque post DR. A recent study reported an increased corticospinal excitability (assessed through motor-evoked potentials elicited by transcranial magnetic stimulation and recorded from the abductor pollicis brevis) 30-min post DR (duration: 30 min; slope: − 10%; intensity: 75% HRreserve). However, the absence of cortical VA measurements in this study makes unclear the potential role of changes in corticospinal excitability/inhibition in the occurrence of supraspinal fatigue post DR. Future studies should combine measures of corticospinal excitability and inhibition (e.g. using paired-pulse transcranial magnetic stimulation) with measures of cortical VA, obtained from muscles directly mobilised during DR (e.g. KE and/or PF). Furthermore, although no comparison analysis of VA was conducted between laboratory and ecological settings, the DR surface could influence the magnitude of acute and delayed central fatigue. A greater reduction in VA could be expected upon completion of an ecological DR session, due to the higher cognitive demands of running on technical single tracks, compared to laboratory conditions. For instance, DR in an ecological setting, compared to a laboratory, may further tax cognitive processes such as working memory and spatial navigation planning and thus exacerbate the activation of cortical areas such as the prefrontal cortex (PFC) [96]. A greater mobilization of brain resources may be expected during DR in an ecological setting, with the necessity to accomplish the motor task while dealing with the additional cognitive demand (i.e. dual task). For example, a greater and earlier depletion of brain resources in cortical structures such as the PFC may negatively impact the activity of interrelated motor areas such as the motor cortex, and lead to a greater reduction of VA. In line with this assumption, Mehta and Parasuraman [97] reported a decrease in PFC oxygenation at exhaustion following a fatiguing cognitive-motor dual task (i.e. submaximal handgrip and concomitant mental-math task) compared to the motor task performed alone. Moreover, Chatain et al. [98] found a greater decrease in VA during a fatiguing cognitive-motor dual task (i.e. intermittent isometric quadriceps contractions with concomitant n-back task) compared to the motor task alone. Because replicating the physiological and cognitive demands of ecological DR in a laboratory setting is challenging, this paradigm may be tested during treadmill DR by adding a concomitant cognitive task that may replicate the demanding real-life environment characterizing off-road running (e.g. using virtual reality technology).

It is well-reported that MVC force/torque is impaired for several days following DR (up to 4–5 days for a complete recovery; see Fig. 1). However, a better understanding of the mechanisms responsible for delayed MVC force/torque loss is warranted. Firstly, it is likely that several mechanisms related to EIMD could play a major role in delayed MVC force/torque loss [99, 100], including structural muscular alterations (e.g. sarcomeres ‘popping’-disruption, streaming, disruption, and dissolution of Z-disk structures) and impairments in the excitation–contraction coupling (e.g. damaged T-tubules, sarcoplasmic reticulum and sarcolemma, impaired Ca2+ release by the sarcoplasmic reticulum and impaired myofibrillar sensibility to Ca2+). To date, only a few studies have investigated recovery (expressed as MVC torque and coupled with peripheral and central assessments of neuromuscular fatigue) up to 48-h post DR [9, 15]. Although Ehrström et al. [15] reported a low-frequency force depression 24-h post DR (duration: 40 min; slope: − 15%; intensity: 55% \(\dot{V}{\text{O}}_{{{\text{2max}}}}\)), such alterations were not recorded 48-h after a 6.5-km ecological DR [9] where isometric MVC torque was still reduced. It is possible that the prolonged low-frequency force depression may be underestimated within days following DR, as it has been observed after an isokinetic eccentric exercise (200 eccentric MVCs of dorsiflexor muscles) [101]. The decrement in low-frequency force could be higher and/or longer than the aforementioned results and thus may partly explain the prolonged MVC force/torque loss. Moreover, a modification in the muscle length-tension relationship up to 48-h post could partly explain the MVC force/torque decrement following DR, as observed following eccentric-biased exercises [102, 103]. Finally, the important leakage of CK, Mb and LDH into the bloodstream, often associated with the appearance of delayed onset muscle soreness (DOMS) [53] and the inflammatory response, may contribute to delayed MVC force/torque loss [104]. Although the relationship between the inflammatory response, DOMS and MVC torque is not clear [105], all these alterations tend to disappear within 4–10 days post DR [71, 73]. It is noteworthy that few studies have compared the extent of neuromuscular fatigue between KE and PF following DR, with contrasting results [9, 15, 43]. Regarding isometric MVC torque, some studies showed greater decrements in KE than in PF [15, 43] whereas Giandolini et al. [9] reported the contrary. The latter results appear difficult to interpret, since higher peripheral alterations (e.g. amplitude torque reduction to evoked twitch torque, M-wave and 10 Hz-to-100 Hz ratio) were reported in KE despite lower isometric MVC torque loss after DR. These conflicting results warrant the need for additional studies investigating possible muscle-specific adaptations to DR.

Fig. 1
figure1

a Decrease (% from baseline) in isometric maximal voluntary contraction (MVC) torque of knee extensors after downhill running (DR); b increase (% from baseline) in blood (plasma and serum) creatine kinase (CK) concentration after DR; c delayed onset muscle soreness (DOMS) response (0–100 mm evaluated on visual analogue scale) for knee extensors after DR. Based on data from original research articles reporting isometric MVC force/torque decrements (n = 37; [5, 9, 10, 15, 38, 43, 58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87]), blood CK elevation (n = 83; [14, 16, 38, 40,41,42, 44, 46, 50, 59,60,61,62, 65,66,67, 70, 72,73,74,75, 77, 80, 81, 84, 85, 87,88,89,90, 92, 121, 134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183]) and DOMS (n = 23; [8, 15, 38, 58, 60, 66, 71, 75, 84, 89, 135, 151, 156, 159, 171, 178, 179, 182, 184,185,186,187,188]) responses immediately post-, 24 h post-, 48 h post-, 72 h post- and 96 h post-DR. In all panels, circles and bars refer to individual and mean data, respectively, in white and black for untrained (i.e. healthy and/or recreationally active) and trained populations (i.e. \(\dot{V}{\text{O}}_{{{\text{2max}}}}\) > 54–60 ml min kg−1 and were involved in endurance-based activities at least 3 times/week), respectively. In the cases where data were not fully presented in the manuscript, data were extracted from original figures using ImageJ software (ImageJ V.1.45 s, National Institute of Health, MD, USA)

While DR studies have mostly investigated the alteration of muscle function using isometric testing, this may not represent the most relevant testing modality. Indeed, single-joint sustained maximal contractions do not represent the real demand of most activities [106]. Future studies should combine various approaches including assessment of isometric and eccentric (recommended from 0.52 to 2.1 rad s−1) MVC force/torque, and whole-body (e.g. counter movement jump or squat jump) or isolated power/maximal velocity tests to better characterize EIMD.

Running Economy Alterations Following Downhill Running

In contrast with the aforementioned EIMD and muscle fatigue variables, RE may be measured during exercise and not only in a “pre-post” experimental design. RE is considered a major determinant of running performance [107, 108] and success in competitive distance running [109, 110]. It is typically measured to evaluate any form of intervention on global metabolic efficiency (e.g. [73, 92, 111]). In DR studies, RE is traditionally defined as the submaximal and steady-state oxygen uptake (\(\dot{V}{\text{O}}_{{2}}\), mlO2 min−1 kg−1 with rate of exchange ratio, RER < 1) for a given running speed and is generally assessed on level grade (e.g. [73, 92, 112]). However, RE is often used synonymously with other indicators of metabolic efficiency. In such cases, RE may be expressed as oxygen cost (mlO2 kg−1 km−1) from the body mass-specific \(\dot{V}{\text{O}}_{{2}}\). Given that substrate used to cover energy expenditure may vary according to exercise intensity and duration (for review, [113]), interpretations resulting only from the use of milliliters of oxygen (including oxygen cost) must be made with caution. For these reasons, expressing RE as gross energy cost (in J kg−1 m−1 or kcal kg−1 km−1), where each \(\dot{V}{\text{O}}_{{2}}\) valued is converted to its metabolic energy equivalent (which depends on the RER) would be more appropriate [114]. In the literature, an enhanced RE is associated with a lower oxygen demand, energy cost or oxygen cost for a given running speed.

The negative slope of the terrain could also influence RE due to the higher proportion of eccentric muscle actions compared to flat running. Although the recruitment order of motor units has been recently reported to be similar during submaximal shortening and lengthening contractions, the discharge rate is systematically lower during lengthening actions (for review, [115]) and thus, might lower the metabolic demand [116]. DR would be metabolically less demanding than level running and uphill running for a similar running speed and/or relative intensity (e.g. mechanical power, HR and \(\dot{V}{\text{O}}_{{2}}\)) [28, 31, 117,118,119,120]. For instance, at 75% HRreserve, Garnier et al. [117] linked the lower alteration in RE (expressed as \(\dot{V}{\text{O}}_{{2}}\)) during DR to a greater involvement of passive elastic structures in strength production compared to level and uphill treadmill exercise. The optimum slope (for which the metabolic demand is the lowest) is still a matter of debate due to the variety in DR protocols used and training levels of study participants.

Cardiorespiratory changes (e.g. increase in HR, \(\dot{V}{\text{O}}_{{2}}\), and minute ventilation) for a set speed [117, 121, 122], accompanied by an increase in core body temperature [121], generally occur during intense and/or prolonged DR sessions, and may be dependent on the slope that is used [123]. For example, a ~ 10% increase in \(\dot{V}{\text{O}}_{{2}}\) was measured immediately after a prolonged DR (30–40 min) in recreational runners [121, 122] whereas the increase was lower (+ 6.8%) in well-trained runners [15]. A reduced amplitude of the \(\dot{V}{\text{O}}_{{2}}\) slow component was also observed during a 15-min DR bout (slope: − 15%; average speed: 8.5 km h−1) in well-trained runners following the completion of a 15-min uphill bout (at the same running speed, with 10-min recovery between bouts [124]).

Alterations in RE were reported in various prolonged DR protocols and within several hours to days following DR [71, 73, 84, 112, 121, 122]. A 3–18% decrease in RE (expressed as \(\dot{V}{\text{O}}_{{2}}\) or energy cost) was reported during flat treadmill running sessions performed immediately after DR [71, 73, 84, 112] and may be associated with an increase in stride frequency and/or reduction in the range of motion of lower-limb joints [64, 71, 73, 84, 92, 112]. Chen et al. [71] reported a 4–7% increase in \(\dot{V}{\text{O}}_{{2}}\) up to 3 days after a 30-min DR (slope: − 15%; intensity: 70% \(\dot{V}{\text{O}}_{{{\text{2max}}}}\)), regardless of running speed [73]. While the time-course of RE alterations seems similar between studies, it was suggested that participants unaccustomed to running and/or untrained in running could experience greater alterations in RE during, immediately after and within days following DR [84].

The change in discharge rate of motor units over time [115], the preponderant type II muscle fiber recruitment [1, 122], and substantial normal impact force and parallel braking force [27] could account for the increased metabolic demand at the end of prolonged DR. This is aligned with the fact that type II fibres, which are energetically less efficient than type I fibres [125], may be further recruited following DR to maintain force production [126], whereas type I fibres could preferentially be recruited during DR [122]. RE alteration after DR may depend on the extent of EIMD, since a greater neural input to the muscle is required to offset the lack of efficiency of damaged fibres [122, 127], and to maintain the force production capacity (particularly necessary during the push-off phase of the running cycle) [128]. In contrast, Lima et al. [84] have recently demonstrated that alterations of RE (expressed as \(\dot{V}{\text{O}}_{{2}}\)) following DR (up to 3 days after one 30-min DR bout; slope: − 15%; average speed: 9.9 km h−1) were not explained by changes in markers of EIMD (serum CK elevation, DOMS, changes in muscle function) or alterations in running mechanics. The authors speculated that other parameters might alter RE following DR, including haemodynamic alterations (such as damaged capillaries [129], compromised flow-mediated vasodilation [130] and oxygen delivery [131] to the damaged sites) and the increase in resting energy expenditure [132].

Taken together, these data provide evidence that prolonged DR can lead to substantial physiological and biomechanical alterations, altering RE and subsequent running performance. While EIMD is well-known to be the main disruptor of running performance and subsequent recovery, underlying mechanisms which could influence the magnitude of muscle damage following DR must be clarified.

Factors Influencing The Magnitude of Muscle Damage Following Downhill Running

Although the physiological responses to DR have been extensively investigated, the influence of DR characteristics (i.e. slope, running speed and/or intensity, and exercise duration) on the magnitude of EIMD is still unclear. The variety in population characteristics (i.e. training status, sex, age) among studies also adds complexity to our understanding. As discussed in the previous section, muscle damage following DR is classically monitored within the first 24-h to 96-h following exercise via indirect markers of muscle structure, muscle function and perceptions of muscle soreness. As such, we analysed the time-course of changes in isometric MVC force/torque (for KE only), DOMS (for KE only using a 0-100 mm visual analogue scale) and blood CK, the most reported markers in the literature, within this time window. The purpose of this comprehensive analysis is to present the current state of knowledge on how DR characteristics influence muscle damage post DR while highlighting the lack of data in certain areas. The main factors included in the analysis were the training level (trained vs untrained in running) and DR characteristics (exercise duration, running speed and slope), while additional factors (age, sex) were also discussed.

Influence of Training Level and Downhill Running Characteristics

To investigate the effect of training level on indirect markers of EIMD, data extracted from original articles were separated into two different groups: untrained and trained populations. Untrained populations are described as healthy and/or recreationally active. In contrast, trained populations generally present a \(\dot{V}{\text{O}}_{{{\text{2max}}}}\) > 54–60 ml min kg−1 and are involved in endurance-based activities (i.e. long-distance running, triathlon, trail running) at least 3 times/week [133].

The literature describes acute and delayed changes in indirect markers of muscle damage after DR (Fig. 1). The reduction in isometric MVC force/torque generally peaks immediately post-DR [5, 9, 10, 15, 38, 43, 58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87], whereas increases in blood CK [14, 16, 38, 40,41,42, 44, 46, 50, 59,60,61,62, 65,66,67, 70, 72,73,74,75, 77, 80, 81, 84, 85, 87,88,89,90, 92, 121, 134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183] and DOMS [8, 15, 38, 58, 60, 66, 71, 75, 84, 89, 135, 151, 156, 159, 171, 178, 179, 182, 184,185,186,187,188] peak from 24 to 48 h post-DR. Immediately post DR, a greater reduction in isometric MVC force/torque is observed in untrained (mean: − 23.5%; 95% CI: [− 26.9% to − 17.2%] compared to trained populations (− 16.4%; 95% CI: [ − 19.5% to – 12.3%]). In addition, the recovery of isometric MVC force/torque seems to be faster in trained compared to untrained populations (return to baseline 72 h post vs. no full recovery 96 h post, respectively). The peak of DOMS is identified 48 h after DR and seems to be of similar magnitude between populations (49.0 mm; 95% CI: [42.0–58.0 mm] and 53.7 mm; 95% CI: [45.3–67.50 mm] in untrained and trained participants, respectively). Finally, the peak increase in blood CK is identified 24 h post DR in similar proportion between populations (+ 346.5%; 95% CI: [+ 164.7% to + 495.5%] and + 370.7%; 95% CI: [+ 173.6% to + 559.1%] in untrained and trained participants, respectively). However, it is possible that the leakage into the bloodstream is less pronounced 72 h and 96 h post DR in trained compared with untrained populations.

Endurance training seems to limit the occurrence of muscle damage following DR [3, 15]. Physical training has been shown to promote higher physiological muscle resistance to exercise due to a combination of neural (motor unit recruitment), morphological (muscle–tendon unit stiffness) and structural adaptations (muscle fascicle pennation angle, and fascicle length) [189, 190]. These data support the importance of training status and training modality to reduce the occurrence of EIMD. It is important to note that, in most research studies, endurance trained populations were not familiarised with DR and/or eccentric-based exercises. A greater training effect can be expected in participants familiarised with DR. They could benefit the most from specific training adaptations due to the important eccentric component of DR and, thus, limit the magnitude of muscle damage following DR.

When analyzing EIMD markers (Fig. 2), it is also important to consider the methodological differences between DR protocols. Slope, duration, running speed as well as the experimental design (i.e. continuous DR vs intermittent DR) may influence the magnitude of EIMD. Overall, in previous studies, for trained and untrained populations, the median (Q1; Q3) slope, exercise duration, and running speed were − 12.0% (− 15.0%; − 10.0%), 40 min (30 min; 45 min) and 11.3 km h−1 (9.8 km h−1; 12.9 km h−1), respectively. More specifically, in studies assessing isometric MVC in response to DR, the median (Q1; Q3) slope was − 14.95% (− 15.0%; − 12.0%, Fig. 2a). In studies assessing CK, and DOMS following DR, the median (Q1; Q3) slope was − 10% (− 15.0%; − 10.0%) and − 12.8% (− 15.8%; − 10.0%), respectively (Fig. 2b, c). The median (Q1; Q3) running speed was 11.5 km h−1 (10.1 km h−1; 12.9 km h−1), 11.3 km h−1 (9.7 km h−1; 12.5 km.h−1), 12.3 km.h−1 (9.7 km.h−1; 14.6 km.h−1) in studies analysing isometric MVC, CK and DOMS, respectively (Fig. 2d–f). Finally, the median (Q1; Q3) exercise duration in DR protocols was 40 min (30 min; 40 min), 30 min (30 min; 45 min), 40 min (30 min; 46.25 min), in studies analysing isometric MVC, CK and DOMS, respectively (Fig. 2g–i). Moreover, there was an important proportion of intermittent protocols in untrained compared to trained populations (48.0% vs. 21.1% on average, respectively), likely to facilitate the completion of DR exercises in people not accustomed to eccentric muscle actions. The results also highlight important discrepancies between studies in the assessment of DOMS (i.e. methods of evaluation, muscles and/or muscle groups investigated, type of scale used) limiting the amount of data presented in Figs. 1c and 2c, f, i. We can also notice a large variability in blood CK elevation in response to DR among studies in untrained and trained populations. Sex, age, genotype, menstrual cycle, familiarisation with DR and DR characteristics could explain this variability in blood CK response among studies. While blood CK elevation is considered a reliable and indirect marker of EIMD, comparing the extent of EIMD between studies using this marker seems impossible due its variable nature between conditions and individuals.

Fig. 2
figure2

Relationships between peak changes in indirect markers of exercise-induced muscle damage (i.e. isometric maximal voluntary contraction, MVC; blood (plasma and serum) creatine kinase, CK; and delayed onset muscle soreness, DOMS) and downhill running (DR) characteristics (i.e. slope (ac), running speed (df) and exercise duration (gi)]. All data presented and DR characteristics were extracted from original articles. Peak MVC force/torque decrement was reported immediately post-DR. Peak changes in blood CK and DOMS were reported between 24-h post and 48-h post DR. White and black circles refer to original data from untrained (i.e. healthy and/or recreationally active) and trained populations (i.e. \(\dot{V}{\text{O}}_{{{\text{2max}}}}\) > 54−60 ml min kg−1 and were involved in endurance-based activities at least 3 times/week), respectively. In each panel, the grey shape highlights the slope, running speed or exercise duration used in the majority of studies (ranging between the 25th and 75th percentile). In the cases where data were not fully presented in the manuscript, data were extracted from original figures using ImageJ software (ImageJ V.1.45 s, National Institute of Health, MD, USA)

Fig. 3
figure3

a Schematic representation of the time course of alterations following downhill running (DR) and b current scientific evidence on the benefits of different adaptation strategies to DR (i.e. prior exposure to DR [46, 63, 67, 68, 85, 92, 121, 141, 143, 165, 181, 184, 185, 192, 193, 196, 197], preconditioning strategies [16, 81], DR training [14, 209, 210, 254], changes in stride pattern [3267, 68, 218, 219, 221, 220228, 255], the use of lower limb compression garments [15, 236, 237], and the use of specific footwear [28149, 253, 256]. In a and b, orange, blue, red, purple, and green spheres correspond to isometric MVC force/torque loss, changes in running economy and mechanics, ultrastructural alterations, inflammation and oedema, and muscle soreness, respectively. In b, full sphere, indicates a high tendency for a beneficial effect; half full sphere, indicates a lack of tendency for a beneficial effect and/or lack of studies for this parameter; empty sphere, indicates no data for this parameter. In b for each strategy, the strength of scientific evidence is represented with stars on a 1–3 scale where 1 meaning little evidence and 3 meaning high evidence. The level of evidence was determined according to the abundance of data available and the number of studies reporting the same outcome. The illustration of the running man is adapted from ©maximmmmum/Adobe Stock

Manipulating DR characteristics, independently or not, may lead to varied extents of EIMD. For example, increasing the slope by 7.0% in combination with a higher speed (+ 4.5 km h−1) induced a greater reduction in MVC torque and blood CK elevation following a 45 min DR [38]. Nevertheless, knowing the DR characteristics that have been used the most in scientific studies so far may help orientate future protocols using DR models. Specifically, from the analysis presented in Fig. 2, where isometric MVC, blood CK and DOMS were investigated in response to DR, it becomes clear that high running speeds (> 15 km h−1), steeper slopes (> 15%) and longer exercise durations (> 60 min) remain to be investigated. Future studies should also aim to isolate the different characteristics of DR to understand whether one or a combination of them might induce more EIMD than others.

Other Factors Potentially Influencing Muscle Damage Following Downhill Running

Few studies have investigated the influence of sex on indirect markers of muscle damage following DR [10, 67, 147, 168, 191]. Following a 30 min DR (slope: − 20%; speed: 10.0 km h−1), no differences were observed in MVC torque loss and no alterations in the central component of neuromuscular fatigue were observed between females and males [10]. Although the magnitude of absolute (compared to baseline value) blood CK elevation is generally similar between males and females following DR [147, 168], Oosthuyse et al. [168] reported a faster return to baseline in females compared to males. It was suggested that an elevated oestrogen level could confer a protective effect against EIMD [148] and/or may reduce the secondary phase of EIMD caused by local inflammation [161]. Carter et al. [141] also reported lower plasma CK elevation in link with higher oestrogen contents after 30-min DR (slope: − 10%; intensity: 60% \(\dot{V}{\text{O}}_{{{\text{2max}}}}\)). In contrast, although blood CK and DOMS elevations generally occur concomitantly in males, this does not seem to be the case in females. The DOMS response following DR was delayed in females and may be influenced by the menstrual phase (with a greater recovery rate during the mid-luteal phase) [168], though this remains to be confirmed with additional studies.

Many studies have investigated adaptations to DR in adult populations, but only a limited number have included adolescents, pre-pubescent children and older populations. Some studies did not report differences in indirect markers of muscle damage between pre-pubescent children and adults [191], or between young and older trained triathletes [180] after DR. Other studies reported trends towards higher levels of indirect markers of muscle damage (neutrophil counts, plasma CK and DOMS) in young men compared to older men after DR [8, 142] but with comparable recovery kinetics [8]. Additional studies are required to better understand the effect of maturation and/or age on the physiological responses to DR.

Adaptation Strategies to Downhill Running

As discussed in Sects. 2 and 3 of this review, the occurrence of EIMD following DR may be deleterious to running performance and subsequent recovery. The search for adaptation strategies to DR, i.e. strategies to better tolerate repeated eccentric muscle actions, is, therefore, warranted. Applications extend from recreational to competitive sport involving DR, such as trail and road running. To date, the focus has been on either pre-exercise strategies designed to accustom the athlete to the demanding nature of DR, or in-situ strategies to reduce the occurrence of EIMD (Table 1 and Fig. 3). Pre-exercise strategies (i.e. preconditioning, DR training) involve a first exposure to eccentric muscle actions prior to DR. In-situ strategies mainly consist in wearing innovative running apparels (i.e. compression garments, specific footwear) or voluntarily changing one’s running pattern during DR.

Table 1 Summary of studies examining adaptation strategies to downhill running (DR), i.e. prior exposure to DR, preconditioning strategies, DR training, changes in stride pattern, the use of lower-limb compression garments and the use of specific footwear

Pre-exercise Adaptation Strategies

Prior Exposure to Downhill Running

Performing two bouts of DR separated by several days or weeks is well-known to reduce or attenuate markers of muscle damage after the second bout [192, 193]. This protective mechanism is termed as ‘repeated bout effect’ (RBE) [57, 194, 195]. Several mechanisms were identified to be likely involved in the RBE, including neural adaptations (e.g. ɑ-motoneuron excitability, shift in motor unit recruitment), adaptations of the muscle–tendon complex (e.g. reduced fascicle elongation, increased tendon compliance), increased sensitivity to inflammation and improved muscle extracellular matrix remodelling [190]. Byrnes et al. [193] reported smaller increases in plasma CK, plasma myoglobin and DOMS up to 48 h after a second DR bout when two 30 min bouts (slope: − 10%; intensity: 170 beats min−1 of heart rate recorded on level grade) were separated by 3-, 6- and 9-weeks. Further studies corroborated these results by reporting a lower leakage and/or a faster clearance of intracellular muscle proteins in the blood [46, 63, 67, 85, 92, 121, 141, 143, 165, 181, 185], lower DOMS [63, 68, 85, 92, 121, 141, 143, 185, 192, 196, 197] and enhanced recovery of MVC force/torque [63] after a second DR bout (Table 1 and Fig. 3b). The RBE is generally reported in greater proportion through blood CK elevation than DOMS and post-exercise MVC force/torque decrement [190]. Chen et al. [92] also suggested a beneficial effect of a first DR bout on RE (expressed as \(\dot{V}{\text{O}}_{{2}}\); preserved up to 72 h post exercise) and stride parameters (preserved stride length and frequency) recorded after the second bout, likely explained by less muscle damage after the second bout. It can be hypothesized that a lower magnitude of EIMD following a second bout of DR may limit the increase in neural input to the muscle (especially during the push-off phase of the running cycle) resulting in a lower increase in \(\dot{V}{\text{O}}_{{2}}\), and consequently lower alterations in RE. It would be interesting to analyse simultaneously the electromyographic activity of KE and PF and RE during the completion of two bouts of DR separated by several days or weeks.

Prior exposure to DR confers protective effects against EIMD that are limited in time. Byrnes et al. [193] showed that the RBE procured by a prior 30 min DR disappeared after 9 weeks with no eccentric muscle actions between the first and second bout. The magnitude of the RBE would mainly depend on the level of exposition to EIMD, with the most EIMD leading to the highest RBE [190, 198]. Within this context, implementing specific DR sessions in the training program of runners could be recommended to benefit from the protective effects of the RBE and adapt well to the next DR session or to better tolerate DR sections in off-road or road races.

Preconditioning Strategies

Performing an isolated strenuous exercise within days prior to a DR session, termed as ‘preconditioning exercise’ may also confer a form of RBE [16, 81]. Eston et al. [16] investigated the effects of repeated isolated KE eccentric muscle actions (100 continuous voluntary eccentric muscle actions at low speed: 0.58 rad s−1) performed 14 days prior to a 40 min DR bout (5 × 8 min interspersed with 2-min rest; slope: − 10%;intensity: 80% maximal heart rate). Compared to the control group, the reduction in maximal isokinetic peak torque (concentric and eccentric at 2.82 rad s−1 and 0.58 rad s−1) was less pronounced at lower eccentric and concentric muscle action speeds (− 22 and − 19% immediately post-DR, respectively), accompanied by a lower elevation in plasma CK (− 79% 48-h post-DR) and an increase in muscle tenderness (− 52% 48 h post-DR) up to 7 days post-DR.

A short isometric preconditioning exercise (10 MVCs at long muscle-length performed 2 days prior DR) could also confer RBE [81]. The authors reported beneficial effects of isometric preconditioning on MVC torque recovery (return to baseline 72-h post in the preconditioning group vs no full recovery 96-h post in the control group) and DOMS (− 25% 48-h post in the preconditioning group vs control group). However, no beneficial effects of isometric preconditioning were observed on RE (expressed as \(\dot{V}{\text{O}}_{{2}}\)), counter movement jump height and plasma CK [81]. Isometric preconditioning exercise at long muscle length could confer RBE, but in lower proportion compared to eccentric preconditioning, although these data are based on studies investigating adaptations of upper-limb muscles [199, 200]. Implementing isometric instead of eccentric-based exercises in training programmes could be an interesting strategy for runners aiming to benefit from the RBE but with no prior muscle damage, especially in the lead up to competitions.

Downhill Running Training

Eccentric-biased exercise training is well known to enhance maximal strength production [201, 202]. In endurance runners, resistance training has been proposed as a strategy to improve running economy [203, 204]. Concurrent plyometric and endurance training for several weeks (8–12 weeks) improved RE (expressed as \(\dot{V}{\text{O}}_{{2}}\); + 4 to + 8% recorded on level grade) [205,206,207,208]. Thus, due to their eccentric-biased muscle action modality, repeated DR sessions may also stimulate muscle growth factors, promote adaptations to the neural system, muscle–tendon complex and running biomechanics, and could lead to improvements in RE. Toyomura et al. [209] argued in favour of DR training to improve running performance on level grade. The authors suggested that DR training could improve the effectiveness of the stretch–shortening cycle (paramount for level running performance; [128]) by accentuating the eccentric work (impact and stance phase) involved, which may consequently enhance RE on flat sections. Further studies are required to verify if DR training may lead to a better RE on negative slopes.

In addition, DOMS recorded after a 45-min DR bout was lower following a short DR training (five training sessions in 1 week; duration: 5–15 min; slope: − 10%; intensity: 80% of running speed associated with \(\dot{V}{\text{O}}_{{{\text{2max}}}}\) recorded on level grade, s\(\dot{V}{\text{O}}_{{{\text{2max}}}}\), with % s\(\dot{V}{\text{O}}_{{{\text{2max}}}}\) corresponding to running speed associated to a percentage of \(\dot{V}{\text{O}}_{{{\text{2max}}}}\)) compared to a non-trained control group [14]. In the same study, a longer training period (ten training sessions in 2 weeks vs. five training sessions in 1 week) conferred a greater beneficial effect on DOMS after a 45-min DR compared to the control group. An improvement in maximal isometric and isokinetic (concentric and eccentric) torque (+ 9 to + 24%) was also recorded after a 5-week DR training in physically active young males (three sessions per week; duration: 5–20 min; slope: − 10%) [209]. In contrast, the same authors did not report any effect of DR training on \(\dot{V}{\text{O}}_{{{\text{2max}}}}\), running speed at \(\dot{V}{\text{O}}_{{{\text{2max}}}}\) and RE (expressed as energy cost) in physically young men. This result was supported by Shaw et al. [210], who reported no change in RE (expressed as energy cost) and stride parameters in already well-trained runners taking part in an 8-week DR training program (with two DR sessions per week added to their habitual training; duration: 15–45 min; slope: − 5%; speed: from 90 to 110% speed at lactate threshold). It can be hypothesized that the initial training level may lower the effectiveness of DR training on RE responses during level running and/or DR. In this regard, Breiner et al. [211] showed that the most economical runners in level running were also the most economical in uphill and downhill slopes, reinforcing the importance of running experience in the RE responses to DR training. It is well-established that at least a single bout of DR can confer a protective mechanism against EIMD. Although the literature is scarce on the load-response to DR training, it seems that a greater training volume could confer a greater protective effect against EIMD [14]. Accordingly, DR training could be incorporated in the training regime of off-road and road runners, in an attempt to improve tolerance to DR, and possibly enhance running performance in races. Recent data tend to support these recommendations showing that maximal strength and lower-limb musculotendinous stiffness as well s\(\dot{V}{\text{O}}_{{{\text{2max}}}}\) are strong predictors of DR performance in trail runners used to DR [212]. These results strengthen the rationale for including specific DR sessions in the athlete’s training regime. In addition, DR training may improve the effectiveness of the stretch–shortening cycle on level grade [128]. On another hand, caution must be taken, and a principle of progressivity must be applied when implementing DR sessions into a runner’s training program to avoid maladaptation and injuries. The greater negative net joint work accompanied by larger extension moments and negative joint power [34] reported in DR might require longer recovery times post training sessions, especially at the beginning of the implementation. Further studies should aim to investigate the load-response to DR training to provide practical guidance for runners. From a scientific standpoint, training data suggest that implementing more than one familiarisation session to DR is crucial in experimental cross-over studies (e.g. [15, 213]) using the DR model to investigate in-situ and recovery strategies, so that the RBE can be offset.

In-situ Adaptation Strategies

Optimisation of Stride and Foot Strike Pattern

The manipulation of foot stride (i.e. length and frequency) and foot strike pattern (i.e. rear-, mid- and fore-foot) can influence the mechanical strain applied to lower limb muscles during running [214,215,216,217]. Accordingly, manipulating foot stride frequency [218] and foot strike pattern [219] during DR could reduce EIMD including neuromuscular fatigue. Following an intermittent 45-min treadmill DR (9 × 5-min; slope: − 15%; speed: 10.5 km h−1), Rowlands et al. [68] reported lower MVC torque decrements post-DR using an understride strategy (− 8.8% MVC torque; 92% preferred stride length) compared with an overstride (− 14.7% MVC torque; 108% preferred stride length) or preferred stride strategy (− 15.5% MVC torque). This was associated with a faster recovery of muscle function within days following exercise. Interestingly, the authors also reported a greater RBE conferred by a first bout of DR with the overstride strategy, likely caused by more EIMD (+ 20 to + 40 mm for DOMS measured on a visual analogue scale immediately post- and 24-h post exercise, respectively) compared to understride and preferred stride strategies. In contrast, Eston et al. [67] observed no difference in plasma CK, MVC force and muscle tenderness after a 40-min intermittent DR (5 × 8-min; slope: − 12%; speed: 11.3 km h−1) in untrained participants, regardless of the foot stride manipulation tested. Regarding the impact of foot stride manipulation on running performance, Sheehan et al. [220] reported that foot stride manipulation can affect RE (expressed as energy cost) during DR (slope: − 10.5%; speed: 10.8 km h−1) with a lower energy cost reported with a preferred stride frequency (PSF) compared to understride (− 12% for 85% PSF) and overstride (− 6% for 115% PSF). Similar results, albeit not significant, were reported by Snyder and Farley [32] when PSF was compared to understride (− 17.4% vs. 85% PSF) and overstride (− 16.2% vs. 115% PSF) during DR at shallow negative slope and low running speed (− 5.2%; speed: 7.2 km h−1). Recently, Vincent et al. [221] corroborated previous results by showing that slight changes in PSF (± 5%) during DR had no detrimental effect on the energy cost of running. In addition, the choice of stride length affects the energy absorption and impact attenuation characteristics of lower extremity joints during DR [218]. More precisely, the authors reported that shortening step length by 10% (i.e. using an overstride strategy) reduced knee joint (at a slope corresponding to − 8.8% and − 17.6%) and hip energy absorption (at a slope corresponding to − 8.8%) and enhanced impact attenuation. Such a strategy may be applied to reduce EIMD and maintain running performance [218]. It is worth mentioning that, on level grade, novice runners ran with a PSF that was about 8% lower than their optimal stride frequency (established from polynomial equations with stride frequency, \(\dot{V}{\text{O}}_{{2}}\) and HR) whereas the PSF of experienced and trained runners was significantly closer to their optimal one (~ − 3%) [222]. Taken together, these data suggest that during DR: (1) metabolic cost, energy absorption and impact attenuation depend on the stride pattern; (2) adopting a stride pattern close to PSF may be an effective strategy to optimize RE. On another hand, the benefits of increasing stride frequency on energy absorption and impact attenuation may occur at the expense of RE. Additional studies are necessary to clarify the effects of stride manipulations on RE and subsequent EIMD during DR, while also taking into account different training levels.

By influencing muscle-length and muscle activity during the ground-contact phase, foot strike pattern could also influence the occurrence of EIMD. Depending on the portion of the foot that initially hits the ground [223], three main foot strike patterns employed by runners have been identified: rearfoot (heel contacts first), midfoot (metatarsal heads contact first accompanied by heel contact) and forefoot (metatarsal heads contact first without heel contact). The forefoot pattern is characterized by greater plantar and knee flexion at initial contact [224,225,226]. The negative work (i.e. the work done to decelerate the body’s centre of mass with respect to the environment) has been shown to be lower at the knee and greater at the ankle in forefoot compared to rearfoot strike [227]. In line with these observations, Giandolini et al. [219] investigated the effects of foot strike pattern on muscle activity and muscle fatigue following a 6.5 km off-road DR (average slope: − 16.8%) in well-trained trail runners. In this study, forefoot strike was associated with higher activity of the gastrocnemius lateralis and lower activity of the vastus lateralis and tibialis anterior during DR. It was also positively correlated with higher decrements in the peripheral fatigue components (i.e. twitch and 10 to 100 Hz ratio decrements) compared to rearfoot strike [219], which may potentially accentuate damage in PF muscles. Interestingly, runners exhibiting various foot strike patterns (alternation between forefoot, midfoot and rearfoot) during DR presented lesser peripheral alterations underlying neuromuscular fatigue following the run. Although no ideal foot strike pattern seems to exist, Giandolini et al. [219] suggested that a high variability in foot strike pattern (based on regression analysis) may limit neuromuscular fatigue during DR. However, when this strategy (i.e. voluntarily alternating foot strike patterns every 30 s) was applied in DR sections over a 2.5-h graded treadmill run, no benefit was reported in terms of neuromuscular alterations compared to the control group (i.e. no switch pattern over DR sections), though no marker of EIMD was recorded in this study [228]. It is possible that (1) the beneficial effect of the variability in foot strike pattern during DR sections was offset by the extent of neuromuscular fatigue during the uphill and level sections (both performed with natural foot strike for 60 min and 20 min in total, respectively), (2) a longer training/familiarisation period is required to benefit the most from this strategy. In the field, we can assume that the best runners spontaneously adapt their running pattern, technique and propulsive function to the varied characteristics of the terrain, which would influence the neuromuscular, energetic and biomechanical demands, thus limiting direct comparisons with laboratory studies.

The Use of Lower Limb Compression Garments

Although wearing lower limb compression garments (CGs) after exercise has been shown to facilitate the recovery process [229,230,231], there is currently no consensus regarding their use during exercise [15, 232,233,234,235]. To date, only a few studies have investigated the impact of wearing CGs during DR [15, 236, 237]. Ehrström et al. [15] showed that wearing high-pressure compression garments (15–20 mmHg) during 40-min treadmill DR (slope: − 15%; intensity: 55% \(\dot{V}{\text{O}}_{{{\text{2max}}}}\)) likely presented benefits for reducing alterations in the peripheral and central components of neuromuscular fatigue (for KE muscles) immediately after DR, in well-trained trail runners. The beneficial effects of CGs may be explained by an attenuation of soft-tissue vibrations which might improve muscle function [238], accompanied by lower muscle activity during exercise [15, 239]. Ehrström et al. [15] suggested that wearing CGs may exert ‘dynamic immobilization’, reducing soft-tissue oscillation and improving joint stability, and in turn, enhancing neural input [240, 241]. Through a histological and immunohistochemical analysis of muscle biopsy samples of KE muscles, Valle et al. [237] reported less muscle fibre injuries (− 26.7% on average) after 40-min DR (slope: − 10%) for the compressed leg compared to the control leg in amateur soccer players. However, since soccer players were not accustomed to DR, this raises the question of the extent of the protective effect conferred by CGs in trained athletes used to running on DR sections. In addition, CGs might contribute to enhanced post-exercise muscle recovery [15, 239]. A greater mechanical protective effect was also observed during the recovery period in KE compared to PF muscles only when athletes wore CGs during DR. This suggests a beneficial mechanical support particularly for the largest muscles recruited in DR [15]. In summary, these few data suggest that wearing CGs could be a relevant strategy to limit EIMD during specific off-road and/or road races involving notable DR sections. Recreational runners and masters athletes (> 40 years) more prone to EIMD may also benefit the most from CGs to help them to stabilise their muscle mass during DR. Wearing CGs could also facilitate adherence to training by limiting the risk of muscle–tendon unit injuries thanks to a reduction in impact shock accelerations during long duration running sessions [15, 242].

The Use of Specific Running Footwear

The selection of appropriate running footwear has become an essential requirement for distance running [243]. Recent meta-analyses and systematic reviews showed that footwear characteristics (i.e. shoe mass, cushioning, motion control, midsole viscoelasticity, comfort, longitudinal bending stiffness, drop height) may reduce the risk of injury [244,245,246] and improve RE [247, 248] on level grade. Minimalist shoes (i.e. lighter mass, greater sole flexibility, lower drop height, smaller heel elevation) have been shown to induce beneficial biomechanical adjustments (e.g. accentuated mid-forefoot stride pattern, knee and ankle range of motion changes) during level running compared to traditional shoes [246, 249]. A lower \(\dot{V}{\text{O}}_{{2}}\) (− 1 to − 4.5%) was reported during level running at a set running speed with minimalist shoes compared to traditional shoes [111, 250,251,252]. Similar RE (measured as cost of running) improvements with minimalist shoes were reported during treadmill graded running (slope: + 8% to − 8%; speed: 10 km h−1) [28], and from a specific RE (measured as cost of running) protocol (flat and uphill treadmill evaluations) completed before a short trail running session (18.4 km with an alternation of uphill and downhill sections) [111]. Although the metabolic benefit of wearing minimalist shoes is evident in the non-fatigued condition, additional investigations are needed to verify whether these benefits can be preserved with fatigue in trained and experienced minimalist runners.

Hardin and Hamill [149] investigated the effects of specific footwear features (soft-, mid-, and hard-midsole) during DR. Following a 30-min treadmill DR session (slope: − 12%; speed: 12.2 km h−1), no difference was reported between midsole conditions on leg shock and EIMD.

In parallel, additional cushioning provided by maximalist shoes has been claimed by manufacturers to provide shock absorption during running, potentially reducing the impact loading and the risk of injury. However, wearing maximalist shoes might not be capable of reducing the impact loading on a level surface and might even increase the external impact loading during short DR treadmill sessions [253].

In summary, current scientific evidence suggests that running footwear is the least effective in-situ strategy to limit the physiological alterations induced by DR. So far, the “metabolic saving” conferred by minimalist shoes has only been recorded in flat running and on non-fatigued muscles.

Conclusion

Downhill running (DR) is a whole-body exercise characterised by a high proportion of eccentric-biased muscle actions well known to induce muscle damage (EIMD) including neuromuscular fatigue, and ensuing alterations in exercise performance. These physiological alterations generally persist for several days after exercise with a peak recorded between immediately post and 96-h post exercise, depending on the variable that is monitored. Our review shows that in the majority of studies conducted so far, EIMD was assessed through isometric maximal voluntary contraction, blood CK and DOMS, with DR characteristics (slope, exercise duration, and running speed) acting as the main influencing factors. In previous studies, the median (Q1; Q3) slope, exercise duration, and running speed were − 12% (− 15%; − 10%), 40 min (30 min; 45 min) and 11.3 km h−1 (9.8 km h−1; 12.9 km h−1), respectively. The training level, and specifically that being used to train on DR sections, can also greatly influence the magnitude of EIMD and must be considered in future studies. Other factors including age and sex might influence the response to DR, though evidence is lacking. Moreover, our analysis highlights the large variety of protocols using the DR model, which prohibits firm conclusions about the factors most responsible for muscle damage and fatigue in DR. In this regard, there is a need for further high-quality research using a consistent approach in the assessment of muscle damage.

The final aim of this review was to gather scientific evidence on strategies implemented in the field to limit EIMD and thus better adapt to DR. We identified two types of strategies; (1) pre-exercise strategies that mainly consist of prior exposure to DR; (2) in-situ strategies that involve the use of specific sportswear (lower limb compression garments and running shoes), and/or voluntary modifications in stride and foot strike patterns. Current scientific evidence shows that prior exposure to DR is the most effective strategy to limit the magnitude of EIMD as a result of the so called “repeated bout effect”. Amongst in-situ strategies, CGs present the most potential but additional studies are required to confirm these findings and understand the underlying mechanisms. Finally, despite a growing interest in the development of innovative running shoes, current data, albeit limited, do not show any influence on the adaptation to DR.

References

  1. 1.

    Douglas J, Pearson S, Ross A, McGuigan M. Eccentric exercise: physiological characteristics and acute responses. Sports Med. 2017;47(4):663–75.

    PubMed  Google Scholar 

  2. 2.

    Coratella G, Longo S, Cè E, Esposito F, de Campos YAC, Pereira-Guimarães M, et al. Commentaries on Viewpoint: distinct modalities of eccentric exercise: different recipes, not the same dish. J Appl Physiol (1985). 2019;127(3):884–91.

    Google Scholar 

  3. 3.

    Giandolini M, Vernillo G, Samozino P, Horvais N, Edwards WB, Morin JB, et al. Fatigue associated with prolonged graded running. Eur J Appl Physiol. 2016;116(10):1859–73.

    PubMed  Google Scholar 

  4. 4.

    Proske U, Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol. 2001;537(Pt 2):333–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Garnier YM, Lepers R, Stapley PJ, Papaxanthis C, Paizis C. Changes in cortico-spinal excitability following uphill versus downhill treadmill exercise. Behav Brain Res. 2017;15(317):242–50.

    Google Scholar 

  6. 6.

    Verges S, Maffiuletti NA, Kerherve H, Decorte N, Wuyam B, Millet GY. Comparison of electrical and magnetic stimulations to assess quadriceps muscle function. J Appl Physiol (1985). 2009;106(2):701–10.

    Google Scholar 

  7. 7.

    Bulbulian R, Bowles DK. Effect of downhill running on motoneuron pool excitability. J Appl Physiol (1985). 1992;73(3):968–73.

    CAS  Google Scholar 

  8. 8.

    Hayashi K, Leary ME, Roy SJ, Laosiripisan J, Pasha EP, Tanaka H. Recovery from strenuous downhill running in young and older physically active adults. Int J Sports Med. 2019;40(11):696–703.

    CAS  PubMed  Google Scholar 

  9. 9.

    Giandolini M, Horvais N, Rossi J, Millet GY, Morin JB, Samozino P. Acute and delayed peripheral and central neuromuscular alterations induced by a short and intense downhill trail run. Scand J Med Sci Sports. 2016;26(11):1321–33.

    CAS  PubMed  Google Scholar 

  10. 10.

    Martin V, Millet GY, Martin A, Deley G, Lattier G. Assessment of low-frequency fatigue with two methods of electrical stimulation. J Appl Physiol (1985). 2004;97(5):1923–9.

    CAS  Google Scholar 

  11. 11.

    Kang YS, Kim CH, Kim JS. The effects of downhill and uphill exercise training on osteogenesis-related factors in ovariectomy-induced bone loss. J Exerc Nutrition Biochem. 2017;21(3):1–10.

    PubMed  PubMed Central  Google Scholar 

  12. 12.

    Burr JF, Boulter M, Beck K. Arterial stiffness results from eccentrically biased downhill running exercise. J Sci Med Sport. 2015;18(2):230–5.

    CAS  PubMed  Google Scholar 

  13. 13.

    Alkahtani SA, Yakout SM, Reginster JY, Al-Daghri NM. Effect of acute downhill running on bone markers in responders and non-responders. Osteoporos Int. 2019;30(2):375–81.

    CAS  PubMed  Google Scholar 

  14. 14.

    Schwane JA, Williams JS, Sloan JH. Effects of training on delayed muscle soreness and serum creatine-kinase activity after running. Med Sci Sport Exerc. 1987;19(6):584–90.

    CAS  Google Scholar 

  15. 15.

    Ehrstrom S, Gruet M, Giandolini M, Chapuis S, Morin JB, Vercruyssen F. Acute and delayed neuromuscular alterations induced by downhill running in trained trail runners: beneficial effects of high-pressure compression garments. Front Physiol. 2018;9:1627.

    PubMed  PubMed Central  Google Scholar 

  16. 16.

    Eston RG, Finney S, Baker S, Baltzopoulos V. Muscle tenderness and peak torque changes after downhill running following a prior bout of isokinetic eccentric exercise. J Sports Sci. 1996;14(4):291–9.

    CAS  PubMed  Google Scholar 

  17. 17.

    Scheer V, Basset P, Giovanelli N, Vernillo G, Millet GPP, Costa RJS. Defining off-road running: a position statement from the ultra sports science foundation. Int J Sports Med. 2020;41(5):275–84.

    PubMed  Google Scholar 

  18. 18.

    Vernillo G, Giandolini M, Edwards WB, Morin JB, Samozino P, Horvais N, et al. Biomechanics and physiology of uphill and downhill running. Sports Med. 2017;47(4):615–29.

    PubMed  Google Scholar 

  19. 19.

    Millet GY, Tomazin K, Verges S, Vincent C, Bonnefoy R, Boisson RC, et al. Neuromuscular consequences of an extreme mountain ultra-marathon. PLoS ONE. 2011;6(2):e17059.

    CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Temesi J, Arnal PJ, Rupp T, Feasson L, Cartier R, Gergele L, et al. Are females more resistant to extreme neuromuscular fatigue? Med Sci Sports Exerc. 2015;47(7):1372–82.

    PubMed  Google Scholar 

  21. 21.

    Temesi J, Rupp T, Martin V, Arnal PJ, Feasson L, Verges S, et al. Central fatigue assessed by transcranial magnetic stimulation in ultratrail running. Med Sci Sports Exerc. 2014;46(6):1166–75.

    PubMed  Google Scholar 

  22. 22.

    Saugy J, Place N, Millet GY, Degache F, Schena F, Millet GP. Alterations of neuromuscular function after the world's most challenging mountain ultra-marathon. PLoS ONE. 2013;8(6):e65596.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Millet GY. Can neuromuscular fatigue explain running strategies and performance in ultra-marathons? The flush model Sports Med. 2011;41(6):489–506.

    PubMed  Google Scholar 

  24. 24.

    Hyldahl RD, Hubal MJ. Lengthening our perspective: morphological, cellular, and molecular responses to eccentric exercise. Muscle Nerve. 2014;49(2):155–70.

    PubMed  Google Scholar 

  25. 25.

    Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev. 2001;81(4):1725–89.

    CAS  PubMed  Google Scholar 

  26. 26.

    Snyder KL, Kram R, Gottschall JS. The role of elastic energy storage and recovery in downhill and uphill running. J Exp Biol. 2012;215(Pt 13):2283–7.

    PubMed  Google Scholar 

  27. 27.

    Gottschall JS, Kram R. Ground reaction forces during downhill and uphill running. J Biomech. 2005;38(3):445–52.

    PubMed  Google Scholar 

  28. 28.

    Lussiana T, Fabre N, Hebert-Losier K, Mourot L. Effect of slope and footwear on running economy and kinematics. Scand J Med Sci Sports. 2013;23(4):e246–e253253.

    CAS  PubMed  Google Scholar 

  29. 29.

    Dewolf AH, Penailillo LE, Willems PA. The rebound of the body during uphill and downhill running at different speeds. J Exp Biol. 2016;219(Pt 15):2276–88.

    CAS  PubMed  Google Scholar 

  30. 30.

    Telhan G, Franz JR, Dicharry J, Wilder RP, Riley PO, Kerrigan DC. Lower limb joint kinetics during moderately sloped running. J Athl Train. 2010;45(1):16–211.

    PubMed  PubMed Central  Google Scholar 

  31. 31.

    Minetti AE, Ardigo LP, Saibene F. Mechanical determinants of the minimum energy cost of gradient running in humans. J Exp Biol. 1994;195:211–25.

    CAS  PubMed  Google Scholar 

  32. 32.

    Snyder KL, Farley CT. Energetically optimal stride frequency in running: the effects of incline and decline. J Exp Biol. 2011;214(Pt 12):2089–95.

    PubMed  Google Scholar 

  33. 33.

    Devita P, Janshen L, Rider P, Solnik S, Hortobágyi T. Muscle work is biased toward energy generation over dissipation in non-level running. J Biomech. 2008;41(16):3354–9.

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Park SK, Jeon HM, Lam WK, Stefanyshyn D, Ryu J. The effects of downhill slope on kinematics and kinetics of the lower extremity joints during running. Gait Posture. 2019;68:181–6.

    PubMed  Google Scholar 

  35. 35.

    Wells MD, Dickin DC, Popp J, Wang H. Effect of downhill running grade on lower extremity loading in female distance runners. Sports Biomech. 2018;1:1–9.

    Google Scholar 

  36. 36.

    Chu JJ, Caldwell GE. Stiffness and damping response associated with shock attenuation in downhill running. J Appl Biomech. 2004;20(3):291.

    Google Scholar 

  37. 37.

    Hamill CL, Clarke IE, Frederick EG, Goodyear LJ, Howley ET. Effects of grade running on kinematics and impact force. Med Sci Sports Exerc. 1984;16:185–22.

    Google Scholar 

  38. 38.

    Malm C, Sjodin TL, Sjoberg B, Lenkei R, Renstrom P, Lundberg IE, et al. Leukocytes, cytokines, growth factors and hormones in human skeletal muscle and blood after uphill or downhill running. J Physiol. 2004;556(Pt 3):983–1000.

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Paulsen G, Mikkelsen UR, Raastad T, Peake JM. Leucocytes, cytokines and satellite cells: what role do they play in muscle damage and regeneration following eccentric exercise? Exerc Immunol Rev. 2012;18:42–97.

    PubMed  Google Scholar 

  40. 40.

    Feasson L, Stockholm D, Freyssenet D, Richard I, Duguez S, Beckmann JS, et al. Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol. 2002;543(Pt 1):297–306.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Buford TW, Cooke MB, Shelmadine BD, Hudson GM, Redd L, Willoughby DS. Effects of eccentric treadmill exercise on inflammatory gene expression in human skeletal muscle. Appl Physiol Nutr Metab. 2009;34(4):745–53.

    CAS  PubMed  Google Scholar 

  42. 42.

    van de Vyver M, Myburgh KH. Cytokine and satellite cell responses to muscle damage: interpretation and possible confounding factors in human studies. J Muscle Res Cell Motil. 2012;33(3–4):177–85.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Maeo S, Ando Y, Kanehisa H, Kawakami Y. Localization of damage in the human leg muscles induced by downhill running. Sci Rep. 2017;7(1):5769.

    PubMed  PubMed Central  Google Scholar 

  44. 44.

    Maughan RJ, Donnelly AE, Gleeson M, Whiting PH, Walker KA, Clough PJ. Delayed-onset muscle damage and lipid peroxidation in man after a downhill run. Muscle Nerve. 1989;12(4):332–6.

    CAS  PubMed  Google Scholar 

  45. 45.

    Byrne C, Twist C, Eston R. Neuromuscular function after exercise-induced muscle damage: theoretical and applied implications. Sports Med. 2004;34(1):49–69.

    PubMed  Google Scholar 

  46. 46.

    McKune AJ, Smith LL, Semple SJ, Mokethwa B, Wadee AA. Immunoglobulin responses to a repeated bout of downhill running. Br J Sports Med. 2006;40(10):844–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Overgaard K, Lindstrøm T, Ingemann-Hansen T, Clausen T. Membrane leakage and increased content of Na+ -K+ pumps and Ca2+ in human muscle after a 100-km run. J Appl Physiol (1985). 2002;92(5):1891–8.

    CAS  Google Scholar 

  48. 48.

    Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle-fiber injury. Sports Med. 1991;12(3):184–207.

    CAS  PubMed  Google Scholar 

  49. 49.

    Warren GL, Ingalls CP, Lowe DA, Armstrong RB. Excitation-contraction uncoupling: major role in contraction-induced muscle injury. Exerc Sport Sci Rev. 2001;29(2):82–7.

    CAS  PubMed  Google Scholar 

  50. 50.

    Peake JM, Suzuki K, Wilson G, Hordern M, Nosaka K, Mackinnon L, et al. Exercise-induced muscle damage, plasma cytokines, and markers of neutrophil activation. Med Sci Sports Exerc. 2005;37(5):737–45.

    CAS  PubMed  Google Scholar 

  51. 51.

    Gibala MJ, Macdougall JD, Tarnopolsky MA, Stauber WT, Elorriga A. Changes in human skeletal muscle ultrastructure and force production after acute resitance exercise. J Appl Physiol (1985). 1995;78:702–8.

    CAS  Google Scholar 

  52. 52.

    Lauritzen F, Paulsen G, Raastad T, Bergersen LH, Owe SG. Gross ultrastructural changes and necrotic fiber segments in elbow flexor muscles after maximal voluntary eccentric action in humans. J Appl Physiol (1985). 2009;107(6):1923–34.

    Google Scholar 

  53. 53.

    Peake JM, Neubauer O, Della-Gatta PA, Nosaka K. Muscle damage and inflammation during recovery from exercise. J Appl Physiol (1985). 2017;122(3):559–70.

    CAS  Google Scholar 

  54. 54.

    Damas F, Nosaka K, Libardi CA, Chen TC, Ugrinowitsch C. Susceptibility to exercise-induced muscle damage: a cluster analysis with a large sample. Int J Sports Med. 2016;37(8):633–40.

    CAS  PubMed  Google Scholar 

  55. 55.

    Raastad T, Owe SG, Paulsen G, Enns D, Overgaard K, Crameri R, et al. Changes in calpain activity, muscle structure, and function after eccentric exercise. Med Sci Sports Exerc. 2010;42(1):86–95.

    PubMed  Google Scholar 

  56. 56.

    McCully KK, Faulkner JA. Characteristics of lengthening contractions associated with injury to skeletal muscle fibers. J Appl Physiol (1985). 1986;61(1):293–9.

    CAS  Google Scholar 

  57. 57.

    McHugh MP. Recent advances in the understanding of the repeated bout effect: the protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports. 2003;13(2):88–97.

    PubMed  Google Scholar 

  58. 58.

    Garnier YM, Lepers R, Dubau Q, Pageaux B, Paizis C. Neuromuscular and perceptual responses to moderate-intensity incline, level and decline treadmill exercise. Eur J Appl Physiol. 2018;118(10):2039–53.

    PubMed  Google Scholar 

  59. 59.

    Donnelly AE, Maughan RJ, Whiting PH. Effects of ibuprofen on exercise-induced muscle soreness and indices of muscle damage. Br J Sports Med. 1990;24(3):191–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Dobridge JD, Hackney AC. The effects of estrogen on indices of skeletal muscle tissue damage after eccentric exercise in postmenopausal women. Fiziol Cheloveka. 2004;30(4):98–102.

    CAS  PubMed  Google Scholar 

  61. 61.

    Ormsbee MJ, Ward EG, Bach CW, Arciero PJ, McKune AJ, Panton LB. The impact of a pre-loaded multi-ingredient performance supplement on muscle soreness and performance following downhill running. J Int Soc Sports Nutr. 2015;12(1):2.

    PubMed  PubMed Central  Google Scholar 

  62. 62.

    Green MS, Corona BT, Doyle JA, Ingalls CP. Carbohydrate-protein drinks do not enhance recovery from exercise-induced muscle injury. Int J Sport Nutr Exerc Metab. 2008;18:1–18.

    CAS  PubMed  Google Scholar 

  63. 63.

    Green MS, Doyle JA, Ingalls CP, Benardot D, Rupp JC, Corona BT. Adaptation of insulin-resistance indicators to a repeated bout of eccentric exercise in human skeletal muscle. Int J Sport Nutr Exerc Metab. 2010;20(3):181–90.

    CAS  PubMed  Google Scholar 

  64. 64.

    Sharwood KA, Lambert MI, St Clair-Gibson A, Noakes TD. Changes in muscle power and neuromuscular efficiency after a 40-minute downhill run in veteran long distance runners. Clin J Sport Med. 2000;10(2):129–35.

    CAS  PubMed  Google Scholar 

  65. 65.

    Muller E, Proller P, Ferreira-Briza F, Aglas L, Stoggl T. Effectiveness of grounded sleeping on recovery after intensive eccentric muscle loading. Front Physiol. 2019;10:35.

    PubMed  PubMed Central  Google Scholar 

  66. 66.

    Lima LCR, Barreto RV, Bassan NM, Greco CC, Denadai BS. Consumption of an anthocyanin-rich antioxidant juice accelerates recovery of running economy and indirect markers of exercise-induced muscle damage following downhill running. Nutrients. 2019;11:10.

    Google Scholar 

  67. 67.

    Eston RG, Lemmey AB, McHugh P, Byrne C, Walsh SE. Effect of stride length on symptoms of exercise-induced muscle damage during a repeated bout of downhill running. Scand J Med Sci Sports. 2000;10(4):199–204.

    CAS  PubMed  Google Scholar 

  68. 68.

    Rowlands AV, Eston RG, Tilzey C. Effect of stride length manipulation on symptoms of exercise-induced muscle damage and the repeated bout effect. J Sports Sci. 2001;19(5):333–40.

    CAS  PubMed  Google Scholar 

  69. 69.

    Cleary MA, Sitler MR, Kendrick ZV. Dehydration and symptoms of delayed-onset muscle soreness in normothermic men. J Athl Train. 2006;41(1):36–45.

    PubMed  PubMed Central  Google Scholar 

  70. 70.

    Nottle C, Nosaka K. Changes in power assessed by the Wingate Anaerobic Test following downhill running. J Strength Cond Res. 2007;21(1):145–50.

    PubMed  Google Scholar 

  71. 71.

    Chen TC, Nosaka K, Tu JH. Changes in running economy following downhill running. J Sports Sci. 2007;25(1):55–63.

    PubMed  Google Scholar 

  72. 72.

    Etheridge T, Philp A, Watt PW. A single protein meal increases recovery of muscle function following an acute eccentric exercise bout. Appl Physiol Nutr Metab. 2008;33(3):483–8.

    CAS  PubMed  Google Scholar 

  73. 73.

    Chen TC, Nosaka K, Lin MJ, Chen HL, Wu CJ. Changes in running economy at different intensities following downhill running. J Sports Sci. 2009;27(11):1137–44.

    PubMed  Google Scholar 

  74. 74.

    Chen TC, Nosaka K, Wu CC. Effects of a 30-min running performed daily after downhill running on recovery of muscle function and running economy. J Sci Med Sport. 2008;11(3):271–9.

    PubMed  Google Scholar 

  75. 75.

    Baumann CW, Green MS, Doyle JA, Rupp JC, Ingalls CP, Corona BT. Muscle injury after low-intensity downhill running reduces running economy. J Strength Cond Res. 2014;28(5):1212–8.

    PubMed  Google Scholar 

  76. 76.

    Cook MD, Myers SD, Kelly JS, Willems ME. Acute postexercise effects of concentric and eccentric exercise on glucose tolerance. Int J Sport Nutr Exerc Metab. 2015;25(1):14–9.

    CAS  PubMed  Google Scholar 

  77. 77.

    Mickleborough TD, Sinex JA, Platt D, Chapman RF, Hirt M. The effects PCSO-524(R), a patented marine oil lipid and omega-3 PUFA blend derived from the New Zealand green lipped mussel (Perna canaliculus), on indirect markers of muscle damage and inflammation after muscle damaging exercise in untrained men: a randomized, placebo controlled trial. J Int Soc Sports Nutr. 2015;12:10.

    PubMed  PubMed Central  Google Scholar 

  78. 78.

    Gavin JP, Myers SD, Willems ME. The effect of glycogen reduction on cardiorespiratory and metabolic responses during downhill running. Eur J Appl Physiol. 2015;115(5):1125–33.

    CAS  PubMed  Google Scholar 

  79. 79.

    Gavin JP, Myers SD, Willems ME. Effect of eccentric exercise with reduced muscle glycogen on plasma interleukin-6 and neuromuscular responses of musculus quadriceps femoris. J Appl Physiol (1985). 2016;121(1):173–84.

    CAS  Google Scholar 

  80. 80.

    Ely MR, Romero SA, Sieck DC, Mangum JE, Luttrell MJ, Halliwill JR. A single dose of histamine-receptor antagonists before downhill running alters markers of muscle damage and delayed-onset muscle soreness. J Appl Physiol (1985). 2017;122(3):631–41.

    CAS  Google Scholar 

  81. 81.

    Lima LCR, Bassan NM, Cardozo AC, Goncalves M, Greco CC, Denadai BS. Isometric pre-conditioning blunts exercise-induced muscle damage but does not attenuate changes in running economy following downhill running. Hum Mov Sci. 2018;60:1–9.

    PubMed  Google Scholar 

  82. 82.

    Brandenberger KJ, Ingalls CP, Otis JS, Warren GL, Doyle JA. Downhill running impairs strength and activation of the elbow flexors. Med Sci Sport Exerc. 2018;50(5):558–9.

    Google Scholar 

  83. 83.

    Nelson MR, Conlee RK, Parcell AC. Inadequate carbohydrate intake following prolonged exercise does not increase muscle soreness after 15 minutes of downhill running. Int J Sport Nutr Exerc Metab. 2004;14:171–84.

    PubMed  Google Scholar 

  84. 84.

    Lima LCR, Nosaka K, Chen TC, Pinto RS, Greco CC, Denadai BS. Decreased running economy is not associated with decreased force production capacity following downhill running in untrained, young men. Eur J Sport Sci. 2020;23:1–9.

    Google Scholar 

  85. 85.

    He F, Hockemeyer JA, Sedlock D. Does combined antioxidant vitamin supplementation blunt repeated bout effect? Int J Sports Med. 2015;36(5):407–13.

    CAS  PubMed  Google Scholar 

  86. 86.

    Cook MD, Myers SD, Kelly JSM, Willems MET. Effect of level and downhill running on breathing efficiency. Sports. 2015;3(1):12–20.

    Google Scholar 

  87. 87.

    Chrismas BC, Taylor L, Siegler JC, Midgley AW. A reduction in maximal incremental exercise test duration 48 h post downhill run is associated with muscle damage derived exercise induced pain. Front Physiol. 2017;8:135.

    PubMed  PubMed Central  Google Scholar 

  88. 88.

    Close GL, Ashton T, Cable T, Doran D, MacLaren DP. Eccentric exercise, isokinetic muscle torque and delayed onset muscle soreness: the role of reactive oxygen species. Eur J Appl Physiol. 2004;91(5–6):615–21.

    CAS  PubMed  Google Scholar 

  89. 89.

    Hickner RC, Mehta PM, Dyck D, Devita P, Houmard JA, Koves T, et al. Relationship between fat-to-fat-free mass ratio and decrements in leg strength after downhill running. J Appl Physiol (1985). 2001;90(4):1334–41.

    CAS  Google Scholar 

  90. 90.

    Mizuno S, Morii I, Tsuchiya Y, Goto K. Wearing compression garment after endurance exercise promotes recovery of exercise performance. Int J Sports Med. 2016;37(11):870–7.

    CAS  PubMed  Google Scholar 

  91. 91.

    Carmichael MD, Davis JM, Murphy EA, Brown AS, Carson JA, Mayer E, et al. Recovery of running performance following muscle-damaging exercise: relationship to brain IL-1beta. Brain Behav Immun. 2005;19(5):445–52.

    CAS  PubMed  Google Scholar 

  92. 92.

    Chen T, Chen H, Wu C, Lin M, Chen C-H, Wang L-C, et al. Changes in running economy following a repeated bout of downhill running. J Exerc Sci Fit. 2007;5(2):109–17.

    Google Scholar 

  93. 93.

    Jones DA. High-and low-frequency fatigue revisited. Acta Physiol Scand. 1996;156(3):265–70.

    CAS  PubMed  Google Scholar 

  94. 94.

    Sonkodi B, Berkes I, Koltai E. Have we looked in the wrong direction for more than 100 years? Delayed onset muscle soreness is, in fact, neural microdamage rather than muscle damage. Antioxidants (Basel, Switzerl). 2020;9(3):212.

    CAS  Google Scholar 

  95. 95.

    Martin V, Millet G, Lattier G, Perrod L. Why does knee extensor muscles torque decrease after eccentric-type exercise? J Sports Med Phys Fitness. 2005;2005:45.

    Google Scholar 

  96. 96.

    Spiers HJ. Keeping the goal in mind: prefrontal contributions to spatial navigation. Neuropsychologia. 2008;46(7):2106–8.

    PubMed  PubMed Central  Google Scholar 

  97. 97.

    Mehta RK, Parasuraman R. Effects of mental fatigue on the development of physical fatigue: a neuroergonomic approach. Hum Factors. 2014;56(4):645–56.

    PubMed  Google Scholar 

  98. 98.

    Chatain C, Radel R, Vercruyssen F, Rabahi T, Vallier JM, Bernard T, et al. Influence of cognitive load on the dynamics of neurophysiological adjustments during fatiguing exercise. Psychophysiology. 2019;56(6):e13343.

    PubMed  Google Scholar 

  99. 99.

    Clarkson PM, Hubal MJ. Exercise-induced muscle damage in humans. Am J Phys Med Rehabil. 2002;81(11 Suppl):S52–69.

    PubMed  Google Scholar 

  100. 100.

    Peake JM, Suzuki K, Hordern M, Wilson G, Nosaka K, Coombes JS. Plasma cytokine changes in relation to exercise intensity and muscle damage. Eur J Appl Physiol. 2005;95(5–6):514–21.

    CAS  PubMed  Google Scholar 

  101. 101.

    Ruggiero L, Bruce CD, Cotton PD, Dix GU, McNeil CJ. Prolonged low-frequency force depression is underestimated when assessed with doublets compared with tetani in the dorsiflexors. J Appl Physiol (1985). 2019;126(5):1352–9.

    PubMed Central  Google Scholar 

  102. 102.

    Jones C, Allen T, Talbot J, Morgan DL, Proske U. Changes in the mechanical properties of human and amphibian muscle after eccentric exercise. Eur J Appl Physiol Occup Physiol. 1997;76(1):21–31.

    CAS  PubMed  Google Scholar 

  103. 103.

    Brockett CL, Morgan DL, Proske U. Human hamstring muscles adapt to eccentric exercise by changing optimum length. Med Sci Sports Exerc. 2001;33(5):783–90.

    CAS  PubMed  Google Scholar 

  104. 104.

    Peake J, Nosaka K, Suzuki K. Characterization of inflammatory responses to eccentric exercise in humans. Exerc Immunol Rev. 2005;11:64–85.

    PubMed  Google Scholar 

  105. 105.

    Nosaka K, Newton M. Concentric or eccentric training effect on eccentric exercise-induced muscle damage. Med Sci Sports Exerc. 2002;34(1):63–9.

    PubMed  Google Scholar 

  106. 106.

    Place N, Millet GY. Quantification of neuromuscular fatigue: what do we do wrong and why? Sports Med. 2020;50(3):439–47.

    PubMed  Google Scholar 

  107. 107.

    Morgan DW, Craib M. Physiological aspects of running economy. Med Sci Sports Exerc. 1992;24(4):456–61.

    CAS  PubMed  Google Scholar 

  108. 108.

    Conley DL, Krahenbuhl GS, Burkett LN. Training for aerobic capacity and running economy. Phys Sportsmed. 1981;9(4):107–46.

    CAS  PubMed  Google Scholar 

  109. 109.

    Lucia A, Esteve-Lanao J, Olivan J, Gomez-Gallego F, San Juan AF, Santiago C, et al. Physiological characteristics of the best Eritrean runners-exceptional running economy. Appl Physiol Nutr Metab. 2006;31(5):530–40.

    CAS  PubMed  Google Scholar 

  110. 110.

    Joyner MJ, Coyle EF. Endurance exercise performance: the physiology of champions. J Physiol. 2008;586(1):35–44.

    CAS  PubMed  Google Scholar 

  111. 111.

    Vercruyssen F, Tartaruga M, Horvais N, Brisswalter J. Effects of footwear and fatigue on running economy and biomechanics in trail runners. Med Sci Sports Exerc. 2016;48(10):1976–84.

    PubMed  Google Scholar 

  112. 112.

    Braun WA, Dutto DJ. The effects of a single bout of downhill running and ensuing delayed onset of muscle soreness on running economy performed 48 h later. Eur J Appl Physiol. 2003;90(1–2):29–34.

    PubMed  Google Scholar 

  113. 113.

    Vernillo G, Millet GP, Millet GY. Does the running economy really increase after ultra-marathons? Front Physiol. 2017;8:783.

    PubMed  PubMed Central  Google Scholar 

  114. 114.

    Fletcher JR, Esau SP, Macintosh BR. Economy of running: beyond the measurement of oxygen uptake. J Appl Physiol (1985). 2009;107(6):1918–22.

    Google Scholar 

  115. 115.

    Duchateau J, Enoka RM. Neural control of lengthening contractions. J Exp Biol. 2016;219(Pt 2):197–204.

    PubMed  Google Scholar 

  116. 116.

    Abbott BC, Bigland B, Ritchie JM. The physiological cost of negative work. J Physiol. 1952;117(3):380–90.

    CAS  PubMed  PubMed Central  Google Scholar 

  117. 117.

    Garnier Y, Lepers R, Assadi H, Paizis C. Cardiorespiratory changes during prolonged downhill versus uphill treadmill exercise. Int J Sports Med. 2020;41(2):69–74.

    CAS  PubMed  Google Scholar 

  118. 118.

    Minetti AE, Moia C, Roi GS, Susta D, Ferretti G. Energy cost of walking and running at extreme uphill and downhill slopes. J Appl Physiol (1985). 2002;93(3):1039–46.

    Google Scholar 

  119. 119.

    Abe D, Fukuoka Y, Muraki S, Yasukouchi A, Sakaguchi Y, Niihata S. Effects of load and gradient on energy cost of running. J Physiol Anthropol. 2011;30(4):153–60.

    PubMed  Google Scholar 

  120. 120.

    Robergs RA, Wagner DR, Skemp KM. Oxygen consumption and energy expenditure of level versus downhill running. J Sports Med Phys Fitness. 1997;37(3):168–74.

    CAS  PubMed  Google Scholar 

  121. 121.

    Westerlind KC, Byrnes WC, Mazzeo RS. A comparison of the oxygen drift in downhill vs level running. J Appl Physiol (1985). 1992;72(2):796–800.

    CAS  Google Scholar 

  122. 122.

    Dick RW, Cavanagh PR. An explanation of the upward drift in oxygen uptake during prolonged sub-maximal downhill running. Med Sci Sports Exerc. 1987;19(3):310–7.

    CAS  PubMed  Google Scholar 

  123. 123.

    Lin M-J, Chen TC, Chen H-L, Wu C-J, Tseng W-C. Effects of gradient variations on physiological responses to a 30-minute run. J Exerc Sci Fit. 2009;7(2):85–90.

    Google Scholar 

  124. 124.

    Lemire M, Lonsdorfer-Wolf E, Isner-Horobeti ME, Kouassi BYL, Geny B, Favret F, et al. Cardiorespiratory responses to downhill versus uphill running in endurance athletes. Res Q Exerc Sport. 2018;89(4):511–7.

    PubMed  Google Scholar 

  125. 125.

    Woledge RC. Possible effects of fatigue on muscle efficiency. Acta Physiol Scand. 1998;162(3):267–73.

    CAS  PubMed  Google Scholar 

  126. 126.

    Essén B. Glycogen depletion of different fibre types in human skeletal muscle during intermittent and continuous exercise. Acta Physiol Scand. 1978;103(4):446–55.

    PubMed  Google Scholar 

  127. 127.

    Bigland-Ritchie B, Woods JJ. Integrated EMG and oxygen uptake during dynamic contractions of human muscles. J Appl Physiol. 1974;36(4):475–9.

    CAS  PubMed  Google Scholar 

  128. 128.

    Nicol C, Avela J, Komi PV. The stretch-shortening cycle: a model to study naturally occurring neuromuscular fatigue. Sports Med. 2006;36(11):977–99.

    PubMed  Google Scholar 

  129. 129.

    Kano Y, Padilla DJ, Behnke BJ, Hageman KS, Musch TI, Poole DC. Effects of eccentric exercise on microcirculation and microvascular oxygen pressures in rat spinotrapezius muscle. J Appl Physiol (1985). 2005;99(4):1516–22.

    Google Scholar 

  130. 130.

    Caldwell JT, Wardlow GC, Branch PA, Ramos M, Black CD, Ade CJ. Effect of exercise-induced muscle damage on vascular function and skeletal muscle microvascular deoxygenation. Physiol Rep. 2016;4:22.

    Google Scholar 

  131. 131.

    Davies RC, Eston RG, Poole DC, Rowlands AV, DiMenna F, Wilkerson DP, et al. Effect of eccentric exercise-induced muscle damage on the dynamics of muscle oxygenation and pulmonary oxygen uptake. J Appl Physiol (1985). 2008;105(5):1413–21.

    CAS  Google Scholar 

  132. 132.

    Jamurtas AZ, Koutedakis Y, Paschalis V, Tofas T, Yfanti C, Tsiokanos A, et al. The effects of a single bout of exercise on resting energy expenditure and respiratory exchange ratio. Eur J Appl Physiol. 2004;92(4–5):393–8.

    CAS  PubMed  Google Scholar 

  133. 133.

    Whaley MH, Brubaker PH, Otto RM, Armstrong LE. ACSM's guidelines for exercise testing and prescription. Philadelphia: Lippincott Williams & Wilkins; 2006.

    Google Scholar 

  134. 134.

    Schwane JA, Watrous BG, Johnson SR, Armstrong RB. Is lactic acid related to delayed-onset muscle soreness? Phys Sportsmed. 1983;11(3):124–31.

    CAS  PubMed  Google Scholar 

  135. 135.

    Kong PW, Chua YH, Kawabata M, Burns SF, Cai C. Effect of post-exercise massage on passive muscle stiffness measured using myotonometry—a double-blind study. J Sports Sci Med. 2018;17(4):599–606.

    PubMed  PubMed Central  Google Scholar 

  136. 136.

    Sorichter S, Mair J, Arnold K, Gebert W, Rama D, Calzolari C, et al. Skeletal troponin I as a marker of exercise-induced muscle damage. J Appl Physiol. 1985;1997(83):1076–82.

    Google Scholar 

  137. 137.

    Wheat MR, McCoy SL, Barton ED, Starcher BM, Schwane JA. Hydroxylysine excretion does not indicate collagen damage with downhill running in young men. Int J Sport Med. 1989;10:155–60.

    CAS  Google Scholar 

  138. 138.

    Sherman WM, Lash JM, Simonsen JC, Bloomfield SA. Effects of downhill running on the responses to an oral glucose challenge. Int J Sport Nutr. 1992;2(3):251–9.

    CAS  PubMed  Google Scholar 

  139. 139.

    Kirwan JP, Hickner RC, Yarasheski KE, Kohrt WM, Wiethop BV, Holloszy JO. Eccentric exercise induces transient insulin resistance in healthy individuals. J Appl Physiol (1985). 1992;72(6):2197–202.

    CAS  Google Scholar 

  140. 140.

    Fielding RA, Manfredi TJ, Ding W, Fiatarone MA, Evans WJ, Cannon JG. Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol. 1993;265(1 Pt 2):R166–72.

    CAS  PubMed  Google Scholar 

  141. 141.

    Westerlind KC, Byrnes WC, Harris C, Wilcox AR. Alterations in oxygen-consumption during and between bouts of level and downhill running. Med Sci Sport Exerc. 1994;26(9):1144–52.

    CAS  Google Scholar 

  142. 142.

    Cannon JG, Fiatarone MA, Fielding RA, Evans WJ. Aging and stress-induced changes in complement activation and neutrophil mobilization. J Appl Physiol (1985). 1994;76(6):2616–20.

    CAS  Google Scholar 

  143. 143.

    Smith LL, Bond JA, Holbert D, Houmard JA, Israel RG, McCammon MR, et al. Differential white cell count after two bouts of downhill running. Int J Sports Med. 1998;19(6):432–7.

    CAS  PubMed  Google Scholar 

  144. 144.

    Sorichter S, Mair J, Koller A, Pelsers MMAL, Puschendorf B, Glatz JFC. Early assessment of exercise induced skeletal muscle injury using plasma fatty acid binding protein. Br J Sports Med. 1998;32:121–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  145. 145.

    Hubinger L, Mackinnon LT, Barber L, McCosker J, Howard A, Lepre F. Acute effects of treadmill running on lipoprotein(a) levels in males and females. Med Sci Sports Exerc. 1997;29(4):436–42.

    PubMed  Google Scholar 

  146. 146.

    Koskinen SOA, Höyhtyä M, Turpeenniemi-Hujanen T, Martikkala V, Mäkinen TT, Oksa J, et al. Serum concentrations of collagen degrading enzymes and their inhibitors after downhill running. Scand J Med Sci Sports. 2001;11:9–15.

    CAS  PubMed  Google Scholar 

  147. 147.

    Sorichter M, Koller C, Huonker P, et al. Release ofmuscle proteins after downhill running in male and female subjects. Scand J Med Sci Sports. 2001;11:28–322.

    CAS  PubMed  Google Scholar 

  148. 148.

    Carter A, Dobridge J, Hackney AC. Influence of estrogen on markers of muscle tissue damage following eccentric exercise. Fiziol Cheloveka. 2001;27(5):133–7.

    CAS  PubMed  Google Scholar 

  149. 149.

    Hardin EC, Hamill J. The influence of midsole cushioning on mechanical and hematological responses during a prolonged downhill run. Res Q Exerc Sport. 2002;73(2):125–33.

    CAS  PubMed  Google Scholar 

  150. 150.

    Akimoto T, Furudate M, Saitoh M, Sugiura K, Waku T, Akama T, et al. Increased plasma concentrations of intercellular adhesion molecule-1 after strenuous exercise associated with muscle damage. Eur J Appl Physiol. 2002;86(3):185–90.

    CAS  PubMed  Google Scholar 

  151. 151.

    Thompson D, Bailey DM, Hill J, Hurst T, Powell JR, Williams C. Prolonged vitamin C supplementation and recovery from eccentric exercise. Eur J Appl Physiol. 2004;92(1–2):133–8.

    CAS  PubMed  Google Scholar 

  152. 152.

    Close GL, Ashton T, Cable T, Doran D, Noyes C, McArdle F, et al. Effects of dietary carbohydrate on delayed onset muscle soreness and reactive oxygen species after contraction induced muscle damage. Br J Sports Med. 2005;39(12):948–53.

    CAS  PubMed  PubMed Central  Google Scholar 

  153. 153.

    Racette R, Peronnet F, Massicotte D, Lavoie C. Metabolic response to prolonged cycling with (13)C-glucose ingestion following downhill running. Eur J Appl Physiol. 2005;93(5–6):598–605.

    CAS  PubMed  Google Scholar 

  154. 154.

    Mooren FC, Lechtermann A, Fobker M, Brandt B, Sorg C, Volker K, et al. The response of the novel pro-inflammatory molecules S100A8/A9 to exercise. Int J Sports Med. 2006;27(9):751–8.

    CAS  PubMed  Google Scholar 

  155. 155.

    Kingsley MI, Kilduff LP, McEneny J, Dietzig RE, Benton D. Phosphatidylserine supplementation and recovery following downhill running. Med Sci Sports Exerc. 2006;38(9):1617–25.

    CAS  PubMed  Google Scholar 

  156. 156.

    Nunan D, Howatson G, van Someren KA. Exercise-induced muscle damage is not attenuated by beta-hydroxy-beta-methylbutyrate and alpha-ketoisocaproic acid supplementation. J Strength Cond Res. 2010;24(2):531–7.

    PubMed  Google Scholar 

  157. 157.

    Macaluso F, Brooks NE, Niesler CU, Myburgh KH. Satellite cell pool expansion is affected by skeletal muscle characteristics. Muscle Nerve. 2013;48(1):109–16.

    CAS  PubMed  Google Scholar 

  158. 158.

    Jamurtas AZ, Garyfallopoulou A, Theodorou AA, Zalavras A, Paschalis V, Deli CK, et al. A single bout of downhill running transiently increases HOMA-IR without altering adipokine response in healthy adult women. Eur J Appl Physiol. 2013;113(12):2925–32.

    CAS  PubMed  Google Scholar 

  159. 159.

    van de Vyver M, Myburgh KH. Variable inflammation and intramuscular STAT3 phosphorylation and myeloperoxidase levels after downhill running. Scand J Med Sci Sports. 2014;24(5):e360–e371371.

    PubMed  Google Scholar 

  160. 160.

    Pumpa KL, Fallon KE, Bensoussan A, Papalia S. The effects of Panax notoginseng on delayed onset muscle soreness and muscle damage in well-trained males: a double blind randomised controlled trial. Complement Ther Med. 2013;21(3):131–40.

    PubMed  Google Scholar 

  161. 161.

    Welsh MC, Allen DL, Byrnes WC. Plasma matrix metalloproteinase-9 response to downhill running in humans. Int J Sports Med. 2014;35(5):363–70.

    CAS  PubMed  Google Scholar 

  162. 162.

    Drobnic F, Riera J, Appendino G, Togni S, Franceschi F, Valle X, et al. Reduction of delayed onset muscle soreness by a novel curcumin delivery system (Meriva (R)): a randomised, placebo-controlled trial. J Int Soc Sport Nutr. 2014;18:11.

    Google Scholar 

  163. 163.

    Pokora I, Kempa K, Chrapusta SJ, Langfort J. Effects of downhill and uphill exercises of equivalent submaximal intensities on selected blood cytokine levels and blood creatine kinase activity. Biol Sport. 2014;31(3):173–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  164. 164.

    Gatterer H, Peters P, Philippe M, Burtscher M. The effect of pulsating electrostatic field application on the development of delayed onset of muscle soreness (DOMS) symptoms after eccentric exercise. J Phys Ther Sci. 2015;27(10):3105–7.

    PubMed  PubMed Central  Google Scholar 

  165. 165.

    Park KS, Lee MG. Effects of unaccustomed downhill running on muscle damage, oxidative stress, and leukocyte apoptosis. J Exerc Nutr Biochem. 2015;19(2):55–63.

    Google Scholar 

  166. 166.

    Muders K, Pilat C, Deuster V, Frech T, Kruger K, Pons-Kuhnemann J, et al. Effects of traumeel (Tr14) on exercise-induced muscle damage response in healthy subjects: a double-blind RCT. Mediators Inflamm. 2016;2016:1693918.

    PubMed  PubMed Central  Google Scholar 

  167. 167.

    Lin HF, Tung K, Chou CC, Lin CC, Lin JG, Tanaka H. Panax ginseng and salvia miltiorrhiza supplementation abolishes eccentric exercise-induced vascular stiffening: a double-blind randomized control trial. BMC Complement Altern Med. 2016;6(16):168.

    Google Scholar 

  168. 168.

    Oosthuyse T, Bosch AN. The effect of gender and menstrual phase on serum creatine kinase activity and muscle soreness following downhill running. Antioxidants (Basel). 2017;6:1.

    Google Scholar 

  169. 169.

    Tsuchiya Y, Mizuno S, Goto K. Irisin response to downhill running exercise in humans. J Exerc Nutr Biochem. 2018;22(2):12–7.

    Google Scholar 

  170. 170.

    Xia Z, Cholewa JM, Dardevet D, Huang T, Zhao Y, Shang H, et al. Effects of oat protein supplementation on skeletal muscle damage, inflammation and performance recovery following downhill running in untrained collegiate men. Food Funct. 2018;9(9):4720–9.

    CAS  PubMed  Google Scholar 

  171. 171.

    Jafariyan S, Monazzami A, Nikousefat Z, Nobahar M, Yari K. Inflammatory and immune responses to a 3-day period of downhill running in active females. Cell Mol Biol (Noisy-le-grand). 2017;63(7):76–83.

  172. 172.

    Pizza FX, Mitchell JB, Davis BH, Starling RD, Holtz RW, Bigelow N. Exercise-induced muscle damage: effect on circulating leukocyte and lymphocyte subsets. Med Sci Sports Exerc. 1995;27(3):363–70.

    CAS  PubMed  Google Scholar 

  173. 173.

    Shave R, Dawson E, Whyte G, George K, Ball D, Collinson P, et al. The cardiospecificity of the third-generation cTnT assay after exercise-induced muscle damage. Med Sci Sports Exerc. 2002;34(4):651–4.

    PubMed  Google Scholar 

  174. 174.

    Simpson RJ, Florida-James GD, Whyte GP, Guy K. The effects of intensive, moderate and downhill treadmill running on human blood lymphocytes expressing the adhesion/activation molecules CD54 (ICAM-1), CD18 (beta2 integrin) and CD53. Eur J Appl Physiol. 2006;97(1):109–21.

    CAS  PubMed  Google Scholar 

  175. 175.

    Takahashi J, Ishihara K, Aoki J. Effect of aqua exercise on recovery of lower limb muscles after downhill running. J Sports Sci. 2006;24(8):835–42.

    PubMed  Google Scholar 

  176. 176.

    Su QS, Tian Y, Zhang JG, Zhang H. Effects of allicin supplementation on plasma markers of exercise-induced muscle damage, IL-6 and antioxidant capacity. Eur J Appl Physiol. 2008;103(3):275–83.

    CAS  PubMed  Google Scholar 

  177. 177.

    Burnett D, Smith K, Smeltzer C, Young K, Burns S. Perceived muscle soreness in recreational female runners. Int J Exerc Sci. 2010;3(3):108–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  178. 178.

    Broadbent S, Rousseau JJ, Thorp RM, Choate SL, Jackson FS, Rowlands DS. Vibration therapy reduces plasma IL6 and muscle soreness after downhill running. Br J Sports Med. 2010;44(12):888–94.

    CAS  PubMed  Google Scholar 

  179. 179.

    Pumpa KL, Fallon KE, Bensoussan A, Papalia S. The effects of Lyprinol((R)) on delayed onset muscle soreness and muscle damage in well trained athletes: a double-blind randomised controlled trial. Complement Ther Med. 2011;19(6):311–8.

    PubMed  Google Scholar 

  180. 180.

    Doering TM, Jenkins DG, Reaburn PR, Borges NR, Hohmann E, Phillips SM. Lower integrated muscle protein synthesis in masters compared with younger athletes. Med Sci Sports Exerc. 2016;48(8):1613–8.

    CAS  PubMed  Google Scholar 

  181. 181.

    Park KS, Sedlock DA, Navalta JW, Lee MG, Kim SH. Leukocyte apoptosis and pro-/anti-apoptotic proteins following downhill running. Eur J Appl Physiol. 2011;111(9):2349–57.

    PubMed  Google Scholar 

  182. 182.

    Kohne JL, Ormsbee MJ, McKune AJ. The effects of a multi-ingredient supplement on markers of muscle damage and inflammation following downhill running in females. J Int Soc Sports Nutr. 2016;13:44.

    PubMed  PubMed Central  Google Scholar 

  183. 183.

    Nieman DC, Capps CL, Capps CR, Shue ZL, McBride JE. Effect of 4-Week ingestion of tomato-based carotenoids on exercise-induced inflammation, muscle damage, and oxidative stress in endurance runners. Int J Sport Nutr Exerc Metab. 2018;28(3):266–73.

    CAS  PubMed  Google Scholar 

  184. 184.

    Smith LL, Semple SJ, McKune AJ, Neveling N, Caldeira M, Swanepoel JM, et al. Changes in neutrophil count, creatine kinases and muscle soreness after repeated bouts of downhill running. S Afr J Sports Med. 2007;19(3):86–93.

    Google Scholar 

  185. 185.

    Smith LL, McKune AJ, Semple SJ, Sibanda E, Steel H, Anderson R. Changes in serum cytokines after repeated bouts of downhill running. Appl Physiol Nutr Metab. 2007;32(2):233–40.

    CAS  PubMed  Google Scholar 

  186. 186.

    van de Vyver M, Engelbrecht L, Smith C, Myburgh KH. Neutrophil and monocyte responses to downhill running: intracellular contents of MPO, IL-6, IL-10, pstat3, and SOCS3. Scand J Med Sci Sports. 2016;26(6):638–47.

    PubMed  Google Scholar 

  187. 187.

    Szymura J, Maciejczyk M, Wiecek M, Maciejczyk G, Wiecha S, Ochalek K, et al. Effects of kinesio taping on anaerobic power recovery after eccentric exercise. Res Sports Med. 2016;24(3):257–68.

  188. 188.

    Steward CJ, Zhou Y, Keane G, Cook MD, Liu Y, Cullen T. One week of magnesium supplementation lowers IL-6, muscle soreness and increases post-exercise blood glucose in response to downhill running. Eur J Appl Physiol. 2019;119(11–12):2617–27.

    CAS  PubMed  Google Scholar 

  189. 189.

    Burgess TL, Lambert MI. The effects of training, muscle damage and fatigue on running economy. Int Sportmed J. 2010;11(4):363–79.

    Google Scholar 

  190. 190.

    Hyldahl RD, Chen TC, Nosaka K. Mechanisms and mediators of the skeletal muscle repeated bout effect. Exerc Sport Sci Rev. 2017;45(1):24–33.

    PubMed  Google Scholar 

  191. 191.

    Webber LM, Byrnes WC, Rowlands TW, Foster VL. Serum creatine kinase activity and delayed onset muscle soreness in prepubescent children. Pediatr Exerc Sci. 1989;1:351–43535.

    Google Scholar 

  192. 192.

    Pierrynowski MR, Tudus PM, Plyley MJ. Effects of downhill or uphill training prior to a downhill run. Eur J Appl Physiol Occup Physiol. 1987;56(6):668–72.

    CAS  PubMed  Google Scholar 

  193. 193.

    Byrnes WC, Clarkson PM, White JS, Hsieh SS, Frykman PN, Maughan RJ. Delayed onset muscle soreness following repeated bouts of downhill running. J Appl Physiol (1985). 1985;59(3):710–5.

  194. 194.

    McHugh MP, Connolly DA, Eston RG, Gleim GW. Exercise-induced muscle damage and potential mechanisms for the repeated bout effect. Sports Med. 1999;27(3):157–70.

    CAS  PubMed  Google Scholar 

  195. 195.

    Clarkson PM, Nosaka K, Braun B. Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc. 1992;24(5):512–20.

    CAS  PubMed  Google Scholar 

  196. 196.

    Tuttle JA, Chrismas BCR, Gibson OR, Barrington JH, Hughes DC, Castle PC, et al. The Hsp72 and Hsp90alpha mRNA responses to hot downhill running are reduced following a prior bout of hot downhill running, and occur concurrently within leukocytes and the vastus lateralis. Front Physiol. 2017;8:473.

    PubMed  PubMed Central  Google Scholar 

  197. 197.

    Dolci A, Fortes MB, Walker FS, Haq A, Riddle T, Walsh NP. Repeated muscle damage blunts the increase in heat strain during subsequent exercise heat stress. Eur J Appl Physiol. 2015;115(7):1577–88.

    CAS  PubMed  Google Scholar 

  198. 198.

    Nosaka K, Aoki MS. Repeated bout effect: research update and future perspective. Braz J Biomotricity. 2011;5:5–15.

    Google Scholar 

  199. 199.

    Chen TC, Chen HL, Lin MJ, Chen CH, Pearce AJ, Nosaka K. Effect of two maximal isometric contractions on eccentric exercise-induced muscle damage of the elbow flexors. Eur J Appl Physiol. 2013;113(6):1545–54.

    PubMed  Google Scholar 

  200. 200.

    Chen TC, Chen HL, Pearce AJ, Nosaka K. Attenuation of eccentric exercise-induced muscle damage by preconditioning exercises. Med Sci Sports Exerc. 2012;44(11):2090–8.

    PubMed  Google Scholar 

  201. 201.

    Vogt M, Hoppeler HH. Eccentric exercise: mechanisms and effects when used as training regime or training adjunct. J Appl Physiol (1985). 2014;116(11):1446–54.

  202. 202.

    Douglas J, Pearson S, Ross A, McGuigan M. Chronic adaptations to eccentric training: a systematic review. Sports Med. 2017;47(5):917–41.

    PubMed  Google Scholar 

  203. 203.

    Saunders PU, Pyne DB, Telford RD, Hawley JA. Factors affecting running economy in trained distance runners. Sports Med. 2004;34(7):465–85.

    PubMed  Google Scholar 

  204. 204.

    Barnes KR, Kilding AE. Strategies to improve running economy. Sports Med. 2015;45(1):37–56.

    PubMed  Google Scholar 

  205. 205.

    Johnson RE, Quinn TJ, Kertzer R, Vroman NB. Strength training in female distance runners. J Strength Cond Res. 1997;11(4):224–9.

    Google Scholar 

  206. 206.

    Paavolainen L, Hakkinen K, Hamalainen I, Nummela A, Rusko H. Explosive-strength training improves 5-km running time by improving running economy and muscle power. J Appl Physiol (1985). 1999;86(5):1527–33.

  207. 207.

    Saunders PU, Telford RD, Pyne DB, Peltola EM, Cunningham RB, Gore CJ, et al. Short-term plyometric training improves running economy in highly trained middle and long distance runners. J Strength Cond Res. 2006;20(4):947–54.

    PubMed  Google Scholar 

  208. 208.

    Sedano S, Marin PJ, Cuadrado G, Redondo JC. Concurrent training in elite male runners: the influence of strength versus muscular endurance training on performance outcomes. J Strength Cond Res. 2013;27(9):2433–43.

    PubMed  Google Scholar 

  209. 209.

    Toyomura J, Mori H, Tayashiki K, Yamamoto M, Kanehisa H, Maeo S. Efficacy of downhill running training for improving muscular and aerobic performances. Appl Physiol Nutr Metab. 2018;43(4):403–10.

    CAS  PubMed  Google Scholar 

  210. 210.

    Shaw AJ, Ingham SA, Folland JP. The efficacy of downhill running as a method to enhance running economy in trained distance runners. Eur J Sport Sci. 2018;18(5):630–8.

    PubMed  Google Scholar 

  211. 211.

    Breiner TJ, Ortiz ALR, Kram R. Level, uphill and downhill running economy values are strongly inter-correlated. Eur J Appl Physiol. 2019;119(1):257–64.

    PubMed  Google Scholar 

  212. 212.

    Lemire M, Hureau TJ, Favret F, Geny B, Kouassi BYL, Boukhari M, et al. Physiological factors determining downhill vs uphill running endurance performance. J Sci Med Sport. 2020. https://doi.org/10.1016/j.jsams.2020.06.004.

    Article  PubMed  Google Scholar 

  213. 213.

    Lemire M, Hureau TJ, Remetter R, Geny B, Kouassi BYL, Lonsdorfer E, et al. Trail runners cannot reach vo2max during a maximal incremental downhill test. Med Sci Sports Exerc. 2020;52(5):1135–43.

    PubMed  Google Scholar 

  214. 214.

    Giandolini M, Horvais N, Farges Y, Samozino P, Morin JB. Impact reduction through long-term intervention in recreational runners: midfoot strike pattern versus low-drop/low-heel height footwear. Eur J Appl Physiol. 2013;113(8):2077–90.

    PubMed  Google Scholar 

  215. 215.

    Lieberman DE, Venkadesan M, Werbel WA, Daoud AI, D'Andrea S, Davis IS, et al. Foot strike patterns and collision forces in habitually barefoot versus shod runners. Nature. 2010;463(7280):531–5.

    CAS  PubMed  Google Scholar 

  216. 216.

    Divert C, Mornieux G, Baur H, Mayer F, Belli A. Mechanical comparison of barefoot and shod running. Int J Sports Med. 2005;26(7):593–8.

    CAS  PubMed  Google Scholar 

  217. 217.

    Boyer ER, Derrick TR. Select injury-related variables are affected by stride length and foot strike style during running. Am J Sports Med. 2015;43(9):2310–7.

    Google Scholar 

  218. 218.

    Baggaley M, Vernillo G, Martinez A, Horvais N, Giandolini M, Millet GY, et al. Step length and grade effects on energy absorption and impact attenuation in running. Eur J Sport Sci. 2019;24:1–11.

    Google Scholar 

  219. 219.

    Giandolini M, Horvais N, Rossi J, Millet GY, Morin JB, Samozino P. Effects of the foot strike pattern on muscle activity and neuromuscular fatigue in downhill trail running. Scand J Med Sci Sports. 2017;27(8):809–19.

    CAS  PubMed  Google Scholar 

  220. 220.

    Sheehan RC, Gottschall JS. Preferred step frequency during downhill running may be determined by muscle activity. J Electromyogr Kinesiol. 2013;23(4):826–30.

    PubMed  Google Scholar 

  221. 221.

    Vincent HK, Massengill C, Harris A, Chen C, Wasser JG, Bruner M, et al. Cadence impact on cardiopulmonary, metabolic and biomechanical loading during downhill running. Gait Posture. 2019;71:186–91.

    PubMed  Google Scholar 

  222. 222.

    de Ruiter CJ, Verdijk PW, Werker W, Zuidema MJ, de Haan A. Stride frequency in relation to oxygen consumption in experienced and novice runners. Eur J Sport Sci. 2014;14(3):251–8.

    PubMed  Google Scholar 

  223. 223.

    Hamill J, Gruber AH. Is changing footstrike pattern beneficial to runners? J Sport Health Sci. 2017;6(2):146–53.

    PubMed  PubMed Central  Google Scholar 

  224. 224.

    Shih Y, Lin KL, Shiang TY. Is the foot striking pattern more important than barefoot or shod conditions in running? Gait Posture. 2013;38(3):490–4.

    PubMed  Google Scholar 

  225. 225.

    Ahn AN, Brayton C, Bhatia T, Martin P. Muscle activity and kinematics of forefoot and rearfoot strike runners. J Sport Health Sci. 2014;3(2):102–12.

  226. 226.

    Yong JR, Silder A, Delp SL. Differences in muscle activity between natural forefoot and rearfoot strikers during running. J Biomech. 2014;47(15):3593–7.

    PubMed  PubMed Central  Google Scholar 

  227. 227.

    Hamill J, Gruber AH, Derrick TR. Lower extremity joint stiffness characteristics during running with different footfall patterns. Eur J Sport Sci. 2014;14(2):130–6.

    PubMed  Google Scholar 

  228. 228.

    Vernillo G, Aguiar M, Savoldelli A, Martinez A, Giandolini M, Horvais N, et al. Regular changes in foot strike pattern during prolonged downhill running do not influence neuromuscular, energetics, or biomechanical parameters. Eur J Sport Sci. 2019;8:1–10.

    Google Scholar 

  229. 229.

    Beliard S, Chauveau M, Moscatiello T, Cros F, Ecarnot F, Becker F. Compression garments and exercise: no influence of pressure applied. J Sport Sci Med. 2015;14(1):75–83.

    Google Scholar 

  230. 230.

    Brown F, Gissane C, Howatson G, van Someren K, Pedlar C, Hill J. Compression garments and recovery from exercise: a meta-analysis. Sports Med. 2017;47(11):2245–67.

    PubMed  Google Scholar 

  231. 231.

    Hill J, Howatson G, van Someren K, Leeder J, Pedlar C. Compression garments and recovery from exercise-induced muscle damage: a meta-analysis. Br J Sports Med. 2014;48(18):1340–6.

    PubMed  Google Scholar 

  232. 232.

    Vercruyssen F, Easthope C, Bernard T, Hausswirth C, Bieuzen F, Gruet M, et al. The influence of wearing compression stockings on performance indicators and physiological responses following a prolonged trail running exercise. Eur J Sport Sci. 2014;14(2):144–50.

    PubMed  Google Scholar 

  233. 233.

    Ali A, Creasy RH, Edge JA. The effect of graduated compression stockings on running performance. J Strength Cond Res. 2011;25(5):1385–92.

    PubMed  Google Scholar 

  234. 234.

    Sperlich B, Haegele M, Achtzehn S, Linville J, Holmberg HC, Mester J. Different types of compression clothing do not increase sub-maximal and maximal endurance performance in well-trained athletes. J Sports Sci. 2010;28(6):609–14.

    PubMed  Google Scholar 

  235. 235.

    Varela-Sanz A, Espana J, Carr N, Boullosa DA, Esteve-Lanao J. Effects of gradual-elastic compression stockings on running economy, kinematics, and performance in runners. J Strength Cond Res. 2011;25(10):2902–10.

    PubMed  Google Scholar 

  236. 236.

    Willems MET, Webb EC. Effects of wearing graduated compression garment during eccentric exercise. Med Sport. 2010;14(4):193–8.

    Google Scholar 

  237. 237.

    Valle X, Til L, Drobnic F, Turmo A, Montoro JB, Valero O, et al. Compression garments to prevent delayed onset muscle soreness in soccer players. Muscles Ligaments Tendons J. 2013;3(4):295–302.

    PubMed  Google Scholar 

  238. 238.

    Hsu W-C, Tseng L-W, Chen F-C, Wang L-C, Yang W-W, Lin Y-J, et al. Effects of compression garments on surface EMG and physiological responses during and after distance running. J Sport Health Sci. 2017. https://doi.org/10.1016/j.jshs.2017.01.001.

    Article  Google Scholar 

  239. 239.

    Broatch JR, Brophy-Williams N, Phillips EJ, O’Bryan SJ, Halson SL, Barnes S, et al. Compression garments reduce muscle movement and activation during submaximal running. Med Sci Sports Exerc. 2020;52(3):685–95.

    PubMed  Google Scholar 

  240. 240.

    Doan BK, Kwon YH, Newton RU, Shim J, Popper EM, Rogers RA, et al. Evaluation of a lower-body compression garment. J Sports Sci. 2003;21(8):601–10.

    PubMed  Google Scholar 

  241. 241.

    Kraemer WJ, Bush JA, Wickham RB, Denegar CR, Gómez AL, Gotshalk LA, et al. Influence of compression therapy on symptoms following soft tissue injury from maximal eccentric exercise. J Orthop Sports Phys Ther. 2001;31(6):282–90.

    CAS  PubMed  Google Scholar 

  242. 242.

    Lucas-Cuevas AG, Priego-Quesada JI, Aparicio I, Gimenez JV, Llana-Belloch S, Perez-Soriano P. Effect of 3 weeks use of compression garments on stride and impact shock during a fatiguing run. Int J Sports Med. 2015;36(10):826–31.

    CAS  PubMed  Google Scholar 

  243. 243.

    Hennig EM. Eighteen years of running shoe testing in Germany—a series of biomechanical studies. Footwear Sci. 2011;3(2):71–81.

    Google Scholar 

  244. 244.

    Kaplan Y. Barefoot versus shoe running: from the past to the present. Phys Sportsmed. 2014;42(1):30–5.

    PubMed  Google Scholar 

  245. 245.

    Altman AR, Davis IS. Barefoot running: biomechanics and implications for running injuries. Curr Sports Med Rep. 2012;11(5):244–50.

  246. 246.

    Rixe JA, Gallo RA, Silvis ML. The barefoot debate: can minimalist shoes reduce running-related injuries? Curr Sports Med Rep. 2012;11(3):160–5.

  247. 247.

    Cheung RT, Ngai SP. Effects of footwear on running economy in distance runners: a meta-analytical review. J Sci Med Sport. 2016;19(3):260–6.

    CAS  PubMed  Google Scholar 

  248. 248.

    Fuller JT, Bellenger CR, Thewlis D, Tsiros MD, Buckley JD. The effect of footwear on running performance and running economy in distance runners. Sports Med. 2015;45(3):411–22.

    PubMed  Google Scholar 

  249. 249.

    Bonacci J, Saunders PU, Hicks A, Rantalainen T, Vicenzino BG, Spratford W. Running in a minimalist and lightweight shoe is not the same as running barefoot: a biomechanical study. Br J Sports Med. 2013;47(6):387–92.

    PubMed  Google Scholar 

  250. 250.

    Divert C, Mornieux G, Freychat P, Baly L, Mayer F, Belli A. Barefoot-shod running differences: shoe or mass effect? Int J Sports Med. 2008;29(6):512–8.

    CAS  PubMed  Google Scholar 

  251. 251.

    Perl DP, Daoud AI, Lieberman DE. Effects of footwear and strike type on running economy. Med Sci Sports Exerc. 2012;44(7):1335–433.

    PubMed  Google Scholar 

  252. 252.

    Franz JR, Wierzbinski CM, Kram R. Metabolic cost of running barefoot versus shod: is lighter better? Med Sci Sports Exerc. 2012;44(8):1519–25.

    CAS  PubMed  Google Scholar 

  253. 253.

    Chan ZYS, Au IPH, Lau FOY, Ching ECK, Zhang JH, Cheung RTH. Does maximalist footwear lower impact loading during level ground and downhill running? Eur J Sport Sci. 2018;18(8):1083–9.

    PubMed  Google Scholar 

  254. 254.

    Law PG, Goforth HW, Prusaczyk WK, Sopchick-Smith T, Vailas AC. Downhill running to enhance operational performance in mountain terrains. NHRC. 1995;1995:94–36.

  255. 255.

    Giandolini M, Horvais N, Rossi J, Millet GY, Samozino P, Morin JB. Foot strike pattern differently affects the axial and transverse components of shock acceleration and attenuation in downhill trail running. J Biomech. 2016;49(9):1765–71.

    PubMed  Google Scholar 

  256. 256.

    Lussiana T, Hébert-Losier K, Mourot L. Effect of minimal shoes and slope on vertical and leg stiffness during running. J Sport Health Sci. 2015;4(2):195–202.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Julien Louis.

Ethics declarations

Funding

This review was not supported by any research funding.

Conflicts of interest

Bastien Bontemps, Fabrice Vercruyssen, Mathieu Gruet and Julien Louis declare that they have no conflicts of interest relevant to the content of this review.

Availability of data and material

Not applicable to this manuscript.

Ethics approval

For this type of study, formal consent is not required.

Author contributions

All authors contributed equally to this article.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Bontemps, B., Vercruyssen, F., Gruet, M. et al. Downhill Running: What Are The Effects and How Can We Adapt? A Narrative Review. Sports Med 50, 2083–2110 (2020). https://doi.org/10.1007/s40279-020-01355-z

Download citation