Biomechanics and Physiology of Uphill and Downhill Running

Abstract

Most running studies have considered level running (LR), yet the regulation of locomotor behaviour during uphill (UR) and downhill (DR) running is fundamental to increase our understanding of human locomotion. The purpose of this article was to review the existing literature regarding biomechanical, neuromuscular and physiological adaptations during graded running. Relative to LR, UR is characterized by a higher step frequency, increased internal mechanical work, shorter swing/aerial phase duration, and greater duty factor, while DR is characterized by increased aerial time, reduced step frequency and decreased duty factor. Grade also modifies foot strike patterns, with a progressive adoption of a mid- to fore-foot strike pattern during UR, and rear-foot strike patterns during DR. In UR, lower limb muscles perform a higher net mechanical work compared to LR and DR to increase the body’s potential energy. In DR, energy dissipation is generally prevalent compared to energy generation. The increased demands for work as running incline increases are met by an increase in power output at all joints, particularly the hip. This implies that UR requires greater muscular activity compared to LR and DR. Energy cost of running (C
r) linearly increases with positive slope but C
r of DR decreases until a minimum slope is reached at −20 %, after which C
r increases again. The effects of slope on biomechanics, muscle contraction patterns and physiological responses have important implications for injury prevention and success of athletes engaged in graded running competitions.

Full text

REVIEW ARTICLE
Biomechanics and Physiology of Uphill and Downhill Running
Gianluca Vernillo
1,2,3
•Marle
`ne Giandolini
4,5
•W. Brent Edwards
1
•
Jean-Benoı
ˆt Morin
6
•Pierre Samozino
5
•Nicolas Horvais
4,5
•Guillaume Y. Millet
1
ÓSpringer International Publishing Switzerland 2016
Abstract Most running studies have considered level
running (LR), yet the regulation of locomotor behaviour
during uphill (UR) and downhill (DR) running is funda-
mental to increase our understanding of human locomotion.
The purpose of this article was to review the existing lit-
erature regarding biomechanical, neuromuscular and
physiological adaptations during graded running. Relative
to LR, UR is characterized by a higher step frequency,
increased internal mechanical work, shorter swing/aerial
phase duration, and greater duty factor, while DR is char-
acterized by increased aerial time, reduced step frequency
and decreased duty factor. Grade also modifies foot strike
patterns, with a progressive adoption of a mid- to fore-foot
strike pattern during UR, and rear-foot strike patterns
during DR. In UR, lower limb muscles perform a higher
net mechanical work compared to LR and DR to increase
the body’s potential energy. In DR, energy dissipation is
generally prevalent compared to energy generation. The
increased demands for work as running incline increases
are met by an increase in power output at all joints, par-
ticularly the hip. This implies that UR requires greater
muscular activity compared to LR and DR. Energy cost of
running (C
r
) linearly increases with positive slope but C
r
of
DR decreases until a minimum slope is reached at -20 %,
after which C
r
increases again. The effects of slope on
biomechanics, muscle contraction patterns and physiolog-
ical responses have important implications for injury pre-
vention and success of athletes engaged in graded running
competitions.
Key Points
Grade-specific biomechanical adaptations occur in
uphill and downhill running. These include changes
in foot strike pattern and ground reaction forces,
joint kinematics and kinetics, and impact shock.
The observed adaptations directly impact
neuromuscular activation, as demonstrated by
changes in lower limb electromyographic activity
with grade, these changes being specific to the
considered muscles.
Energy cost of running is also affected by slope,
which linearly increases as slope increases and
linearly decreases as slope decreases until a
minimum value is observed at -20 % grade.
&Guillaume Y. Millet
gmillet@ucalgary.ca
1
Human Performance Laboratory, Faculty of Kinesiology,
University of Calgary, 2500 University Dr NW, Calgary,
AB T2N 1N4, Canada
2
Department of Biomedical Sciences for Health, Universita
`
degli Studi di Milano, Milan, Italy
3
CeRiSM, Research Center for Sport, Mountain and Health,
University of Verona, Rovereto, TN, Italy
4
Salomon SAS, Innovation and Sport Science Lab,
74996 Annecy, France
5
Laboratory of Exercise Physiology, University Savoie Mont
Blanc, 73376 Le Bourget-du-Lac, France
6
Universite
´Co
ˆte d’Azur, LAMHESS, Nice, France
123
Sports Med
DOI 10.1007/s40279-016-0605-y

1 Introduction
Running performance derives from a combination of
anatomical, physiological and behavioural characteristics
that are uniquely evolved in humans [1,2]. Accordingly,
the study of human running has always been of great
interest for exercise physiologists and biomechanists in
order to increase our understanding of the physiological
and biomechanical bases of running capabilities in humans.
However, the vast majority of studies have considered only
level running (LR). This is not surprising because until
recently, the major running events have been road races
such as 10 km, half-marathon and marathon, which are
usually run on flat courses [3]. This, however, is not always
the case. South Africa, for instance, has held the world’s
most famous ultra-marathon race since 1921 [3], the
Comrades Marathon, which consists of a *90-km long
course that varies each year between the ‘up’ run [87 km,
1167 m of positive elevation change (D?)] starting from
Durban, and the ‘down’ run [89 km, 1810 m of negative
elevation change (D-)] starting from Pietermaritzburg.
More importantly, ultra-trail running has become increas-
ingly popular [4]. Indeed, in the last 40 years, there has
been an exponential growth of participation in ultra-trail
races (Fig. 1), likely due to greater appeal of these com-
petitions compared to road and track events [4]. There are
countless races worldwide over a broad range of distances
and variations in slope. In Europe, Ultra-Trail du Mont
Blanc
Ò
(UTMB) and Tor des Geants
Ò
(TdG) are famous
mountain ultra-marathon races, characterized not only by
an extreme distance/duration (166 and 330 km, respec-
tively) but also a high elevation (±9500 and ±24000 m,
respectively) [5–8]. The total number of participants is now
close to 10000 over five different distances for the UTMB
and 800 for the TdG, with 6500 and 5000 runners refused
in the 2015 edition, respectively. In North America, the
161 km Western States Endurance Run
Ò
(with 5500 m of
D?and 7000 m of D-) has increased exponentially in the
number of finishers from 1977 to 2008 [4].
Ultra-trail and shorter trail running races typically
involve running over (extremely) long distances on rough
terrain with large positive/negative elevation changes
throughout [5–8]. Thus, the study of the physiological and
biomechanical changes associated with graded running is
important because the ability to appropriately regulate
locomotor behaviour in response to changes in grade is
fundamental to increase our understanding of the control of
human locomotion [9–15]. Running speed was reported to
decrease by 0.1 to 0.3 kmh
-1
for every 1 % change in
gradient [16,17], leading to important biomechanical,
neuromuscular and physiological adaptations. Events such
as ultra-trail running are likely to be at the extremes of
human tolerance [18], and understanding these adaptations
is of paramount importance for health, training and com-
petition reasons.
The purpose of this review is to provide a comprehen-
sive overview of the literature related to the biomechanical,
neuromuscular and physiological responses to graded
running. In this review, manuscripts were acquired by
searching the electronic databases of MEDLINE, PubMed,
ScienceDirect, SPORTDiscus and Web of Science using
the following keywords in various combinations: ‘level’,
‘uphill’, ‘downhill’, ‘incline’, ‘decline’, ‘grade’, ‘gradient’,
‘slope’, ‘hilly’, ‘running’, ‘physiology’, ‘biomechanics’.
Due to the narrow focus on graded running, a relatively
limited number of articles were retrieved, and conse-
quently, no limit to the search period was applied. Elec-
tronic database searching was supplemented by examining
the bibliographies of relevant articles. In the literature, the
terms ‘slope’ and ‘gradient’ are interchangeably used, and
are employed in this paper to indicate running with varia-
tions in slope unless specified otherwise. The important
effects of graded running on fatigue and tissue damage
warrant their own critical evaluation, and are therefore not
considered in the current review.
2 Biomechanical Adaptations
2.1 Spatiotemporal Parameters and Centre of Mass
Kinematics
Several studies have systematically examined the influence
of uphill running (UR) on kinematic variables
[10,12,14,19–23] (Fig. 2) and observed differences when
compared to level running (LR). In UR, higher gradients
have been reported to be associated with a higher step
frequency [10,12,19,24] and consequently increased
internal mechanical work [12]. On the other hand,
Fig. 1 Number of 161-km ultra-trail races in North America from
1977 through 2008 (dashed line) and number of [100-km ultra-trail
races in France (solid line). Based on data from Hoffman et al. [4] and
from personal data
G. Vernillo et al.
123

Gottschall and Kram [10] did not observe any variation in
contact and aerial times at a given running speed
(10.8 kmh
-1
) between LR, UR and downhill running (DR)
(±5.2, 10.5 and 15.8 %). Thus, no changes in duty factor,
step frequency, and stride length were observed. Similarly,
Telhan et al. [24] reported no changes in step frequency or
length when comparing –7 % DR, LR, and 7 % UR at
11 kmh
-1
. UR is characterized by a shorter swing/aerial
phase duration and a greater proportion of the stride cycle
spent in stance, i.e. duty factor (e.g. *33 vs. *29 % for
UR and LR, respectively) [23].
Contact time was found to be constant in DR at
10 kmh
-1
, while aerial time increased at –8 and –5 %
grade compared to LR and UR (2, 5 and 8 %) at the same
speed, resulting in a lower step frequency in DR [19,25].
Similarly, a greater stride length was reported during DR at
12 kmh
-1
and –17.4 % compared to 17.4 % UR at a
similar running speed [26].
Changes in external mechanical energy both during UR
and DR are concomitant with changes in running kine-
matics (Fig. 2; Table 1). Lower vertical displacement of
the centre of mass (CoM) during the stance phase and
greater vertical displacement during the aerial phase were
illustrated in DR compared to UR (e.g. *–20 and ?44 %
at 12 kmh
-1
and ±17.4 % grade, respectively) [26]. In
this study [26], the vertical displacement during the braking
(downward displacement) and propulsive (upward dis-
placement) phases was not separated. Lussiana et al. [25]
specified that running at 10 kmh
-1
and –8 and –5 %
grades induced greater downward displacement of the CoM
during the stance phase compared to running at shallow or
positive grades.
The use of laboratory settings to simulate UR and DR
implies significant technical challenges, limiting the sub-
ject’s ability to regulate running speed [17]. Accordingly,
Townshed et al. [17] investigated speed regulation and
kinematics parameters during a 9525-m overground UR
and DR. They illustrated that, when compared with LR,
stride length was 20.5 % shorter and 16.2 % longer during
UR and DR, respectively, suggesting that running speed
during overground graded running is predominantly regu-
lated by stride length.
2.2 Foot strike and Ground Reaction Forces
Grade has been shown to modify foot strike pattern during
running. Gottschall and Kram [10] and Lussiana et al. [19]
reported that runners progressively adopted a mid-foot or
forefoot strike pattern as slope changed from LR to UR.
Lussiana et al. [19] also reported a less pronounced heel
strike angle during running on inclined versus declined
gradients for a constant running speed. During downhill
trail running conditions, it was observed that high-level
trail runners (based on their skill in DR) adopted a midfoot
strike pattern, whereas medium-level trail runners adopted
a rearfoot strike pattern, irrespective of the technical profile
Fig. 2 Changes in contact time (CT) and step frequency (SF) as a function of speed and grade. Circles denote SF and CT when minimalistic
shoes were wore by the subjects
Biomechanics and Physiology of Graded Running
123

of the run (e.g. steep or shallow slope, with or without
rocks) [27]. In real trail running, however, runners may not
adopt a single foot strike pattern because of the need to
adapt to uneven surfaces, as was observed in a high-level
trail runner [28]. It has been recently observed that the foot
strike pattern adopted during a 6.5-km downhill trail run
(with 1264-m of negative elevation change and run as fast
as possible) differently influences the components of tibial
shock [29]. Although a forefoot strike reduces impact
severity and impact frequency content along the tibial
transverse axis, a rearfoot strike decreases them in the tibial
axial direction.
Gottschall and Kram [10] investigated the ground
reaction forces in running at 10.8 kmh
-1
at grades from
–15.8 to ?15.8 %. Normal (i.e. perpendicular to running
surface) impact force peaks decreased with slope, but
normal active force peaks remained the same. On the
contrary, the parallel propulsive force peaks and impulses
increased with grade [10]. That is, the parallel propulsive
impulse was 57 % lower in DR and 68 % higher in UR at
–15.8 and ?15.8 % slope, respectively, when compared to
LR. These changes likely reflect the need for developing
greater propulsive forces to generate the required upward
acceleration imposed by grade [22]. Recently, Padulo et al.
Table 1 Summary of studies investigating the effect of uphill and downhill running on spatio-temporal variables
Study N Running speed
(km·h-1)a
Slope
(%) CT AT DF SF SL
DeVita et al. [26] 13 12.1 +17.4 - - - -
12.1 -17.4 - - - -
Gottschall and Kram [10] 10 10.8 +15.8
10.8 +10.5
10.8 +5.2
10.8 -5.2
10.8 -10.5
10.8 -15.8
Lussiana et al. [19] 14 10.0 +8.0 -8/5 - -
10.0 +5.0 -8/5 - -
10.0 +2.0 -8/5 --8/5 -
10.0 -2.0 --8/5 -
10.0 -5.0 - -
10.0 -8.0 - -
Padulo et al. [20] 16 14.0 +2.0 -
15.0 +2.0 -
16.0 +2.0 -
17.0 +2.0 -
18.0 +2.0 -
14.0 +7.0 -
15.0 +7.0 -
16.0 +7.0 -
17.0 +7.0 -
18.0 +7.0 -
Padulo et al. [22] 18 15.0 +2.0 -
15.0 +7.0 -
Padulo et al. [21] 65 70% VO2max +2.0
+7.0
Snyder and Farley [14] 9 10.1 +5.2 - - - -
10.1 -5.2 - - - -
Swanson and Caldwell [23] 12 16.2 +30.0 - - -
Telhan et al. [24] 19 11.0 +7.0 - - -
11.0 -7.0 - - -
Nindicates the number of subjects
Changes from level and/or uphill (downhill) running are indicated by black and/or grey arrows, respectively. Ascendant or descendant arrows
indicate significant increases or decreases, respectively, compared to level running and/or uphill running. Horizontal arrows indicate no change
CT contact time, AT aerial time, DF duty factor, SF step frequency, SL step length
a
Except Padulo et al. [21] where the running speed is expressed in percentage of velocity associated with maximum oxygen uptake (vVO
2
max)
G. Vernillo et al.
123

[22] investigated ground reaction forces during running at
15 kmh
-1
on a 50-m asphalt road with different grades.
These authors observed increases in forces and impulses of
12 and 14.7 %, respectively, as the slope increased from 0
to 7 %.
The impact force at foot contact is determined by the
effective lower extremity mass, landing velocity and pas-
sive shoe stiffness [30,31]. Effective mass changes as a
function of joint angle, therefore if kinematics do not
drastically change across gradients, for a given shoe, only
the speed at which the foot strikes the ground would
influence the impact force. As such, one would expect
higher impact forces in DR than in LR or UR. Indeed, a
greater impact peak force was observed during –7 % DR
compared to LR or 7 % UR at 11 kmh
-1
[24]. Similarly,
Gottschall and Kram [10] reported greater normal impact
forces at –15.8, –10.5 and –5.2 % DR than in LR for a
similar running speed (Fig. 3a, b), as well as higher loading
rates at the –15.8 and –10.5 % gradients compared to LR.
Regarding the antero-posterior component of force, greater
braking peak and impulse were observed by Gottschall and
Kram [10] in the three tested DR conditions compared to
LR. For instance, during –15.8 % DR, the braking impulse
increased by 108 % compared to LR [10].
2.3 Mechanics and Joint Kinetics
Knowledge of the changes in joint mechanics and kinetics
during UR and DR running may be important to understand
the adaptive mechanisms induced by sloped running, and
can provide additional information on the risk factors for
lower limb injuries. In the following sections, we discuss
how graded running may impact joint mechanics and
kinetics. A summary of the studies investigating the effect
of UR and DR on the main kinematics and kinetics
parameters at ankle, knee and hip joints is presented in
Table 2.
2.3.1 Mechanical Energy Fluctuations of the CoM
During LR, runners’ CoM behaviour oscillates cyclically
during each stride [32], and both the potential and kinetic
energy fluctuations are in-phase [15,33]. External work,
defined as the sum of potential, and horizontal and vertical
kinetic work associated with the displacement of the CoM,
was measured at different grades (-15 to 15 %) and speeds
(7.9 to 11.8 kmh
-1
)[12]. It was found that negative
external work (i.e. the work done to decelerate the body’s
CoM with respect to the environment [9]) linearly
increased as the slope decreased [12]. For instance, nega-
tive external work was *25 % of the total external work
during UR at 15 % grade, but was *75 % during DR at
–15 % grade. Therefore, more net mechanical energy
generation is required in UR, i.e. energy generation is
greater than absorption. Minetti et al. [12] measured
internal and external mechanical work during UR at dif-
ferent speeds. They reported that both positive external
mechanical work (i.e. the work done to move the body’s
CoM with respect to the environment [9]) and internal
mechanical work (i.e. the work done to move the lower
limbs with respect to the CoM [9]) per unit of distance
travelled increase linearly with slope. Thus, UR requires a
greater net mechanical work with each step to increase the
body’s potential energy [13], and the muscles must perform
greater net positive work both to raise the body’s CoM to
its height at toe-off and to give it sufficient kinetic energy
to reach its highest point during the aerial phase [14].
In DR, albeit positive external work is necessary at
shallow slopes (-5 %), energy dissipation, rather than
energy generation, is generally observed [14,15]. Snyder
et al. [15] measured the mechanical energy fluctuations of
the CoM during LR, UR and DR at 10.8 kmh
-1
. They
observed that some positive mechanical energy is still
required at shallow grades (-5.6 and –10.5 %), but almost
all mechanical energy is negative at –15.6 % grade.
Accordingly, at 12 kmh
-1
, both the total negative and
positive work of the joints were 38 % greater and 265 %
lower in DR (-17.4 %) than in UR (?17.4 %), respec-
tively [26].
2.3.2 Ankle Joint Kinematics and Kinetics
Combined with video analysis, ground reaction forces can
provide useful information about the joint torques of the
support leg during running. Data on the effects of grade
on ankle kinematics are rather heterogeneous, but there is
basically no major or consistent change between LR, UR,
and DR both in terms of ankle kinematics and negative
work. Ankle positive work does not change at shallow
slopes but increases in UR at steep slopes compared to
DR.
Over 30 min of DR (-7 %) and LR (5 % faster than the
individual anaerobic threshold: 12.7 ±0.7 kmh
-1
), ankle
range of motion during the braking phase (dorsiflexion)
only increased after 15 min of DR [34]. Comparing UR
(30 % grade) and LR at 16.0 kmh
-1
, Swanson and Cald-
well [23] observed that the ankle was more dorsiflexed at
foot strike and exhibited a lower dorsiflexion range of
motion in UR. However, the plantar flexion range of
motion was greater during the propulsive phase in UR.
Ankle angular velocity was also considerably lower during
the stance phase in UR than in LR. During the swing phase,
ankle range of motion was greater in UR than in LR, with
angular velocity being similar between the two conditions.
Although Telhan et al. [24] observed no changes in ankle
kinematics between LR, UR and DR (±7%)at11kmh
-1
,
Biomechanics and Physiology of Graded Running
123

Buczek and Cavanagh [35] showed that the instant of
maximum dorsiflexion, ankle peak power absorption, ankle
negative work and the relative duration of the ankle neg-
ative work period over the stance phase increased by 10,
36, 52 and 34 %, respectively, during –8.3 % DR com-
pared to LR at a given speed (15.9 kmh
-1
). Furthermore,
the power generation at the ankle joint was decreased by
49 % in DR (-17.4 % grade) compared to UR (?17.4 %)
at 12 kmh
-1
and no difference in ankle negative work was
observed between DR and UR [26]. Roberts and Belliveau
[13] observed no variation in the net work done at the ankle
joint in UR compared to LR at 10.8 to 12.6 kmh
-1
and 0,
10 and 21.2 % grades.
2.3.3 Knee Joint Kinematics and Kinetics
Knee flexion at contact increases in UR compared to LR
and DR [23,24]. During the braking phase, knee power
absorption increases in DR as a result of a greater knee
range of motion; while during the propulsion phase, knee
power generation increases at steep UR gradients but is
constant across grades at shallow slopes [26].
DR was associated with substantially more knee exten-
sion at initial contact than LR [34,35] and UR [19]ata
given speed [range: 10–16 kmh
-1
]. DR was also associ-
ated with greater knee range of motion in the sagittal plane
during the braking phase [34,35], as well as a delayed time
Fig. 3 Ground reaction forces
(GRFs) expressed as percentage
of body weight (BW) in
different gradient conditions
during treadmill running at
10.8 kmh
-1
:anormal;
bparallel. Adapted from
Gottschall and Kram [10], with
permission. cTypical signals of
tibial accelerations for the
vertical (solid line) and
transversal (dashed line)
components measured along the
tibial anteromedial aspect in
various conditions of slope
during a trail running race.
From authors’ personal data
G. Vernillo et al.
123

Table 2 Summary of studies investigating the effect of uphill and downhill running on the main kinematics and kinetics (angle of flexion at foot strike, sagittal range of motion, negative work
or power absorption and positive work or power generation) at ankle, knee and hip joints
Ankle kinematics and kinetics Knee kinematics and kinetics Hip kinematics and kinetics
Study n
Running
speed
(km·h-1)
Slope
(%)
Dorsiflexion
at FS
Sagittal
RoM
Negative
work/
power
absorption
Positive
work/
power
generation
Flexion
at FS
Sagittal
RoM
Negative
work/
power
absorption
Positive
work/
power
generation
Flexion
at FS
Sagittal
RoM
Negative
work/
power
absorption
Positive
work/
power
generation
Buczek and Cavanagh [35] 716.0 -8.3 -- - -
DeVita et al. [26] 13 12.1 +17.4 -- - - --
12.1 -17.4 -- - - --
Padulo et al. [20] 14 10 .0 +8.0 -8/5 --- - - --- - -
10.0 +5.0 -8/5 --- - - ---- -
10.0 +2.0 --- - - ---- -
10.0 -2.0 --- - - --- - -
10.0 -5.0 -8/5 --- - - ---- -
10.0 -8.0 -8/5 --- - - ---- -
Mizrahi et al. [34] 14 12.7 -7.0 -- --- -
Swanson and Caldwell [23] 12 16.2 +30.0 ---- - - --- - -
Telhan et al. [24] 19 1 1.0 +7.0 -- - - -- -
11.0 -7.0 -- - - -- -
nindicates the number of subjects
Changes from level and/or uphill (downhill) running were indicated by black and/or grey arrows, respectively. Ascendant or descendant arrows indicated significant increases or decreases,
respectively, compared to level running and/or uphill running. Horizontal arrows indicate no change
FS foot strike, RoM range of motion
Biomechanics and Physiology of Graded Running
123

to peak knee flexion [35] at a constant running speed (*13
or 16 kmh
-1
) compared to LR. These kinematic changes
lead to greater negative work (?21 %) and relative dura-
tion of the negative work at the knee over the stance phase
(?7 %) compared to LR [35], as well as increased power
absorption at the knee compared to LR and UR [24].
DeVita et al. [26] observed that 54 % more power was
developed at the knee joint during DR at 12 kmh
-1
and
–17.4 % compared to UR at ?17.4 % and the same speed,
which may be attributed to greater energy absorption at the
knee joint during the braking phase of running. When
comparing UR (30 % grade) and LR at 16.0 kmh
-1
, it was
observed that the knee was more flexed at foot strike in UR
than in LR (59.7°vs. 21.0°, respectively) [23]. These
authors also reported a lower knee range of motion during
the braking phase (flexion), but a greater knee range of
motion during the propulsion phase (extension) in UR.
When comparing UR and LR at 10.8 and 12.6 kmh
-1
at 0,
10 and 21.2 % grades, Roberts and Belliveau [13] observed
no effect of slope on the net work done at the knee joint.
2.3.4 Hip Joint Kinematics and Kinetics
In DR, the hip range of motion increases, inducing greater
hip power absorption compared to LR [24,26,34]. Con-
versely in UR, hip power generation increases compared to
DR [13].
More specifically, greater hip range of motion was
reported during the braking phase at –7 % DR compared to
LR at 12.7 ±0.7 kmh
-1
[34]. Swanson and Caldwell [23]
observed that the hip was more flexed at foot strike in UR
(30 % grade) than in LR at the same speed (16 kmh
-1
).
Although in LR the hip flexed during the braking phase and
then extended during the propulsion phase, the authors
stated that in UR the hip was extending rapidly at foot
strike, more slowly during the braking phase, and rapidly
again during the propulsion phase. The authors also
reported a greater hip range of motion during the propul-
sion phase (extension) in UR than in LR. Swanson and
Caldwell [23] investigated the kinetics of the lower limb
muscles during LR and UR at 16.2 kmh
-1
and 30 %
grade. They observed that average hip power during the
swing phase was *200 % higher during UR. Roberts and
Belliveau [13] extended this work by measuring joint
kinematics during running between 10.8 and 12.6 kmh
-1
at 0, 10 and 21.2 % grades. They found that the net work
done at the hip increased with running incline (*?140 %
at 21.2 % grade). Using a musculoskeletal model, Yoko-
zawa et al. [36] confirmed these previous findings, illus-
trating that the estimated muscle torque of the hip extensors
and flexors were greater during UR at different speeds and
9.1 % grade.
Hip power during the braking phase was also found to
be higher at –7 % DR compared to LR at the same running
speed (11 kmh
-1
)[24]. Hip joint power was lower at
–17.4 % DR compared to 17.4 % UR, for a similar speed
[26]. It is worth mentioning that DeVita et al. [26] noticed
that the ground reaction force vector was directed farther
from the hip joint centre in UR than in DR, lengthening the
lever arm. The authors proposed that the shorter moment
arm at the hip reduced the work demand on the hip flexor
and/or extensor muscles.
2.3.5 Summary
In summary, the overall joint work on the lower limbs
seems to be 28 % higher in UR than in DR [26]. However,
it also seems that graded running does not dramatically
affect the distribution of negative work between the joints.
Both during DR and UR, the knee joint performed the
highest negative work (DR: 63 %, UR: 58 %), followed by
the ankle (DR: 23 %, UR: 30 %) and the hip (DR: 15 %,
UR: 12 %) [26]. This distribution changes when positive
work is considered. Hip seems to be the most stressed joint
(DR: 48 %, UR: 55 %), followed by the ankle (DR and
UR: 32 %) and knee (DR: 20 %, UR: 13 %) [26]. Thus,
there are differences in joint stabilization between UR and
DR that may directly influence, for example, the risk of
developing graded running-injuries.
2.4 Impact Shock Attenuation in Downhill
As mentioned in Sect. 2.2, initial foot contact kinetics
change as a function of slope. Impact accelerations are also
largely affected by DR. DeVita et al. [26] postulated that
the greater impact force in DR would likely cause larger
accelerations of musculo-skeletal tissues, requiring greater
energy dissipation by muscles as well as the heel pad,
bones and spinal discs. In laboratory experiments (i.e.
standardized running speed) and in real practice (i.e. run-
ning speed increases as the gradient decreases), negative
correlations were observed between slope and axial,
transverse (i.e. along the axis of the anteromedial tibial
aspect) and resultant peak tibial accelerations [28,37,38]
(Fig. 3c), as well as with high-frequency vibration content,
i.e. median frequency, along these three acceleration
components [28]. Hamill et al. [38] reported that tibial
shock increased by 30 % during DR on a –8.7 % slope
compared to LR at the same speed. Chu and Caldwell [37]
observed an average of 23 % and 48 % increase in peak
tibial and head acceleration, respectively, at –12 % DR
compared to LR (15 kmh
-1
). Increases of 51 and 125 % in
impact-related frequencies (i.e. power spectral densities
within the 12–20 Hz bandwidth) were also observed at the
G. Vernillo et al.
123

tibia and head, respectively [39]. According to these find-
ings, DR induces a decrease in shock attenuation [37].
However, Mizrahi et al. [34] observed similar peak tibial
acceleration but larger peak sacral acceleration in –7 % DR
compared to LR at 12.7 ±0.7 kmh
-1
. These authors also
reported a lower amplitude within the impact frequency
range at the tibia during DR compared to LR, but no dif-
ferences at the sacrum were observed. Interestingly, Chu
and Caldwell [37] found a bimodal response in peak shock
attenuation in DR, i.e. half of the subjects illustrated
increased shock attenuation during DR compared to LR
while the other half illustrated decreased shock attenuation.
Analysing these two subgroups, the authors found several
differences in their respective kinematic adaptations to DR:
(i) those with reduced shock attenuation in DR displayed a
5°greater dorsiflexion and 4.3°lower hip flexion at heel
strike than those with increased shock attenuation; (ii) at
mid-stance, the subgroup with reduced shock attenuation
exhibited greater dorsiflexion, knee flexion, and lower hip
flexion compared to the subgroup with increased shock
attenuation; (iii) the subgroup with reduced shock attenu-
ation increased the stance and stride duration compared to
the subgroup with increased shock attenuation. Therefore,
the results of Chu and Caldwell [37] suggest that shock
attenuation can be increased during DR by adopting a less
pronounced heel strike and a forward leaning trunk. In this
sense, it has been recently observed during a downhill trail
run that the more anterior the foot strike pattern, the greater
the axial and resultant impact-related vibrations (i.e.
12–20 Hz) between tibia and sacrum. Since knee flexion at
initial contact increases when forefoot striking (e.g. Shih
et al. [40]), one could assume that the improved shock
attenuation with anterior foot strike patterns could be
related to a greater knee flexion at initial contact. Indeed,
Gottschall and Kram [10] proposed that impact forces can
be moderated by increasing knee flexion at initial contact
and reducing stride length during DR. This is in line with
previous observations that increased knee flexion improves
shock attenuation during various dynamic and static tasks
[41–44].
3 Neuromuscular Adaptations
Table 3shows differences in the electromyographic
(EMG) activity of different muscle groups investigated as
a function of running grade. Abe et al. [45] compared
vastus lateralis activity among 0 and ±5 % grades at
11.9 kmh
-1
and observed lower activity during the con-
centric phase (i.e. propulsion) of DR compared to UR but
not LR. These authors did not observe any differences
between slopes in the intensity and duration of vastus
lateralis activity during the eccentric phase (i.e. braking).
One would expect more vastus lateralis activity during the
eccentric phase in DR. Indeed, as previously mentioned,
the absolute and relative negative works as well as the
percentage of stance time in negative work were signifi-
cantly higher for knee extensor muscles in DR than in LR
[35]. A possible explanation for the lack of significant
difference in the study of Abe et al. [45] could be the
rather low gradient examined (±5 %) which may have
induced a minimal change in the power absorption per-
formed by the knee extensors, suggesting also that a
minimal gradient of –7 % is necessary to significantly
increase knee power absorption [24,35]. The ratio between
vastus lateralis muscle activity during the eccentric phase
to activity during the concentric phase was significantly
greater during DR compared to UR [45]. Mizrahi et al.
[34] investigated the consequences of 30-min of DR
(slope: –7 %) compared to LR at a speed slightly higher
than anaerobic threshold (12.7 ±0.7 kmh
-1
). They found
no difference in EMG activity of the rectus femoris muscle
between LR and DR in the first 15 min of running. While
the effects of fatigue are beyond the scope of the present
review, it can be noted that differences between LR and
DR running appeared after 15 min [34].
The slope-related changes in UR biomechanics as dis-
cussed above would be expected to require higher activa-
tion patterns of lower limb muscles, i.e. greater motor unit
recruitment in UR. However, the effects of slope on EMG
activity are not the same for all lower limb muscles. This is
likely due to the varying roles of different lower limb
muscles in producing force at various phases of the gait
cycle [46] and to the fact that slope alters joint mechanics
non-uniformly [26]. EMG studies have provided consid-
erable information on the timing of individual muscle
activity throughout the gait cycle of UR. Globally, a greater
activation compared to LR is usually found in the iliopsoas,
gluteus maximus, adductor muscles, hamstrings and vastii
muscles, tibialis anterior, and gastrocnemius (Table 3).
More specifically, the hip flexors have been found to
generate more energy and higher moments during the
swing phase [13,23]. During the braking/absorption phase
(i.e. from foot strike to mid-stance), higher activation has
been measured for the gluteus maximus, vastii muscles,
gastrocnemius and soleus whereas during the propulsion
phase (i.e. from mid-stance to toe-off), higher activation
has been measured for the gluteus maximus, hamstrings
and vastii muscles, gastrocnemius and soleus [22,23,47].
Collectively, these studies illustrated that greater EMG
activity in the lower limb muscles (e.g. up to 83 and 100 %
for gluteus maximus and vastus lateralis, respectively)
exists in UR at a given speed. This greater EMG activity is
likely associated with a greater force production [48] pri-
marily for concentric muscle contractions during the sec-
ond phase of stance [12].
Biomechanics and Physiology of Graded Running
123

Exercise-induced contrast shifts in magnetic resonance
images before and after (time between termination of
exercise and completion of the post-exercise image being
11–12 min) high-intensity running at *115 % of the peak
oxygen uptake (VO
2peak
) were examined by Sloniger et al.
[49]. These authors showed that the EMG activity of the
lower limb muscle was 6 % greater during UR at 10 %
grade compared to LR. Using the same technique, a sub-
sequent study demonstrated that, compared to LR, UR
required a greater activation of the vastus group (?23 %)
and soleus (?14 %) paralleled by less activation of the
rectus femoris (-29 %), gracilis (-18 %) and semitendi-
nosus (-17 %) [50].
It is important to note that most of the aforementioned
studies assessed EMG activity/muscle activation at a given
absolute speed, limiting their applicability to real world
settings where speed is naturally reduced during UR. The
behaviour of muscle activity when the exercise intensity
(or the energy expenditure) is kept nearly constant is cur-
rently unknown.
4 Physiological Consequences of Biomechanical
and Neuromuscular Changes
4.1 Energy Cost of Running
In LR, the energy cost of running (C
r
), defined as the
amount of energy spent to transport the subject’s body a
given distance [51], does not change with speed when
expressed as oxygen uptake [52]. However, when C
r
is
expressed in terms of caloric unit cost it seems to be more
sensitive to changes in speed, even when normalized per
distance travelled [53,54]. Changes in the kinetic and
potential energy in one stride are almost in-phase [9],
implying that the energy storage accomplished by a mus-
cle-tendon unit and passive muscle elasticity (the so-called
stretch-shortening cycle [55,56]) contribute to one of the
energy-saving mechanisms during running [45,57–59].
This feature is recognized as one of the major determinants
of C
r
[9]. Indeed, in running, the storage and release of
elastic energy contributes to accelerate the body upwards
during the propulsive phase and reduce energy production
needed during the concentric phase, since the advantage of
elastic energy is how much muscle work it can replace
[14,15,60]. During LR, it has been estimated that the
elastic energy stored in the Achilles’ tendon and the foot
arch aponeurosis accounted for approximately 43 % of the
total positive mechanical energy at each step [15]. How-
ever, during UR and DR, Snyder et al. [14] hypothesized
that the use of elastic energy may be compromised due to a
mismatch between the possibility to store the elastic energy
during landing and to use that elastic energy during take-
off. Indeed, at 10 kmh
-1
the maximum possible elastic
energy use was 20.4 and 11.7 % lower when UR (?5.2 %)
and DR (-5.2 %) were compared to LR [14], reflecting
more a decrease in the maximum possible elastic energy
storage and return rather than a change in the anatomically
estimated elastic energy storage [15]. Yet, even if energy
released from the stretch-shortening cycle is low and the
ability of the muscle tendon units to store elastic energy
during landing and to release that energy during take-off is
reduced [12], the main explanation for the higher C
r
in UR
is the increased net mechanical energy generation required
to overcome the potential energy associated with slope.
Thus, greater muscle activity (see above) is required to
generate a relatively high amount of positive (concentric)
work during the push-off phase in order to both raise the
CoM and offset the diminished maximum possible elastic
energy storage and return [14]. This ultimately results in a
C
r
increase. In the last decade, several studies have
examined the effects of increased gradient on C
r
. Despite
some methodological differences in the way C
r
was
expressed [i.e. oxygen cost (mlkg
-1
m
-1
) or caloric cost
(Jkg
-1
m
-1
)], all studies report a linear increase in C
r
with
each increment in the slope gradient (see an example in
Fig. 4)[12,14,19,22,45,61,62].
When measured on a treadmill at different moderate
slopes, a reduction of C
r
, as well as heart rate, ventilation or
total EMG, has been consistently observed in DR com-
pared to LR and UR [45,63–66], with the effects of grade
not being significantly different between males and females
[65]. For moderate slopes, the following equation has been
proposed [64]:
VO2¼6:8192 þ0:1313 vþ1:2367 % grade
where vis the running velocity in m min
-1
. This would
suggest that C
r
(when expressed as oxygen uptake) is 22 %
lower at –5 % DR compared to LR. However, when
considering steeper slopes (from –45 to ?45 %), the
following fifth-order polynomial regression has been
proposed [61]:
Cr¼155:4i530:4i443:3i3þ46:3i2þ19:5iþ3:6
where iis the gradient in %. According to this equation, the
decrease in C
r
is no longer linear after –20 % grade, where
the relationship inverts and C
r
increases with further
decreases in downhill slope (Fig. 4)[61]. Note that this
optimal slope was found to be lower (-10 %) by the same
authors in a previous paper [12] yet C
r
seems to plateau
between –10 and –20 %. This is in line with the downhill
slope at which mechanical energy must no longer be gen-
erated (-16 %) according to Snyder et al. [15]. In other
words, this optimal negative grade can be explained by the
fact that on steeper downhill grades, mechanical energy
dissipation must occur, whereas on less steep downhill
G. Vernillo et al.
123

grades, though more mechanical energy is dissipated than
generated, some positive mechanical energy must be gen-
erated [15]. Interestingly, the slope allowing for the best C
r
(-20 %) is steeper than the slope at which the best energy
cost of walking is observed [61]. Gottschall and Kram [10]
argued that at progressively steeper declines, the parallel
propulsive impulse decreased exponentially, while the
parallel braking impulse increased linearly. This different
change in the propulsive and braking impulses could
explain the increase in the metabolic cost below –20 %
[61] due to higher concentric muscle contractions at steeper
versus shallow declines [10].
Vertical speed directly measured during UR is very
close to that predicted by Minetti et al. [61] whereas the
predicted speed for DR overestimates the measured speed
[61]. Minetti et al. [61] identified methodological issues
that hampered accurate reproduction of outdoor conditions
in the laboratory (e.g. differences between the rough terrain
and smooth treadmill surface). We are not aware of any
study measuring C
r
in UR or DR in the field at a constant
speed. The key point is that C
r
measured during running
does not reflect the reality in the field. In particular,
assuming that C
r
is independent of speed in DR is probably
wrong. Minetti et al. [61] also introduced the notion of
vertical cost of running (C
r-vert
), defined as the energy
expenditure to run a distance that corresponds to a vertical
displacement of 1 m. Contrary to classic C
r
,C
r-vert
was
found to be stable below –20 % and above ?20 %.
Recently, Giovannelli et al. [67] extended this knowledge,
observing that at a fixed vertical speed of 1.26 kmh
-1
there is a range of angles for which C
r-vert
is minimized
(between 37.2 % and 70 %), with a minimum value at
50.9 %.
4.2 Other Physiological Specificities of Graded
Running
It is known that hilly races (even though not characterized
by a net change in elevation) are not as fast as level ones.
Staab et al. [68] suggested that although running pace
changed inversely with percentage grade on hilly courses,
subjects were not able to maintain a constant energy
expenditure during the race. Indeed, the increase in DR
pace was inadequate to maintain a level VO
2
[68], i.e. the
change from LR to UR and from LR to DR resulted in a
40 % increase and a 27 % decrease in VO
2
, respectively.
This indicates that the greater metabolic demands of UR
are not compensated for by the lower metabolic demands
of DR [69]. In an attempt to investigate speed regulation
during overground running, Townshend et al. [17] showed
that while natural pace was reduced in UR and increased in
DR compared to LR, these pace changes were not enough
to keep VO
2
stable: VO
2
was found to be 100 % of venti-
latory thresholds in UR, 89 % in LR and 79 % in DR.
Interestingly, these authors also reported that the velocity
in LR was systematically influenced by the preceding
slope, i.e. UR or DR [17]. It has also been reported that in
simulated competition conditions, lactate increased in UR
compared to LR even though running pace decreased [68].
In line with this finding, for a given blood lactate con-
centration, which also corresponded to the same VO
2
but
obviously different velocities (i.e. *8.5, 11 and
Table 3 Summary of studies examining the effects of uphill and downhill running on the electromyography (EMG) activity of different lower
limb muscles
Study nRunning speed
(kmh
-1
)
Slope
(%)
ILP GMed GMax HA RF MH BF VL VM TA MG SOL
Abe et al. [45] 8 11.9 0 vs. ?5?
0 vs. -5?
-5 vs. ?5%
Padulo et al. [22] 18 15 0 vs. 2 %!?!!?
0 vs. 7 %!?!!?
Swanson et al. [23] 12 16.2 0 vs. 30 %%??%?%%
Wall-Scheffler et al. [47] 34 6.5, 9.7 and 13 0 vs. 10 %%%%%%% %
0 vs. 15 %%%%%%% %
0 vs. 20 %%%%%%% %
Yokozawa et al. [36]
a
6 18 0 vs. 9.1 %%%%?%?? ?
nindicates the number of subjects
%,!,?indicate increase, decrease, no change in EMG activity, respectively, as a function of the slope change
ILP iliopsoas, GMed gluteus medius, GMax gluteus maximus, HA hip adductors, RF rectus femoris, MH medial hamstring, BF biceps femoris,
VL vastus lateralis, VM vastus medialis, TA tibialis anterior, MG medial gastrocnemius, SOL soleus
a
Indicates that muscle activities of the lower limbs were assessed by using a musculoskeletal model
Biomechanics and Physiology of Graded Running
123

13.5 km h
-1
for UR, LR and DR, respectively), Kolkhorst
et al. [70] reported that rating of perceived exertion tended
to be higher in DR than LR and UR, and LR tended to be
higher than UR. Graded running is associated with modi-
fied breathing patterns, i.e. the locomotor-respiratory cou-
pling [71]. It is worth reporting that increasing or
decreasing the stride frequency away from preferred values
alters the metabolic cost similarly during LR, UR and DR
[14] and this is true when the stride frequency is manipu-
lated or the optimal stride frequency applied [14].
Costill et al. [72] demonstrated that glycogen depletion
(as assessed by muscle biopsy) was higher in the vastus
lateralis, gastrocnemius and soleus muscle fibres after 2-h of
UR at 10 % grade compared to 2-h of LR at the same relative
intensity (i.e., *75 % VO
2max
). Given that glycogen uti-
lization by human skeletal muscle varies as a function of both
work done and intensity [73], this finding confirms that a
higher percentage of muscle mass is recruited during UR in
these muscles. Furthermore, the greater muscle activity
observed during UR (see Sect. 3) seems also to be respon-
sible for a higher peak oxygen deficit [49].
A few studies systematically examined the influence of
slope on maximal accumulated oxygen deficit, an indicator
of the anaerobic capacity [74]. Olesen [62] determined this
during treadmill running at 1, 10, 15 and 20 % grade.
Compared with running at 1 % grade, maximal accumu-
lated oxygen deficit increased by 37 % at 10.5 % grade and
*80 % at 15 % grade, without any further increase at
20 % grade. Walker et al. [75] and Sloniger et al. [49]
reported similar findings, with a 26 and 21 % increase in
the maximal accumulated oxygen deficit as treadmill grade
was increased from 0 to 10 %, respectively. Together,
these findings may indicate that the maximal anaerobic
energy production is greater during UR due to increased
skeletal muscle mass activation in the lower limbs
[49,62,75], even if differences in running efficiency as
well as testing and calculations procedures (i.e. a linear
relationship between work rate and energy demand) cannot
be ruled out [76].
In summary, graded running induces specific adapta-
tions related to modified physiological strain proportional
to the slope gradients from –20 to ?45 %, and natural
reductions in pace may not necessarily allow for a reduc-
tion in total strain. Furthermore, given the higher muscle
activation and the increase in the anaerobic energy pro-
duction that leads to lower C
r
, runners exert a higher
physiological strain during UR compared to LR. Con-
versely, due to the mechanical consequences discussed in
Sect. 2, DR may result in more mechanical stress, partic-
ularly in non-familiarised runners, leading to muscle
damage and lower limb injuries.
5 Conclusion and Future Directions
The present review shows that several grade-specific dif-
ferences exist between LR, UR and DR regarding biome-
chanics, neuromuscular adaptations and physiological
responses. Higher step frequency and increased internal
mechanical work, shorter swing/aerial phase duration, and
greater duty factor are the main kinematic features of UR.
Compared to LR, DR is characterized by a similar contact
time and a tendency toward higher aerial time and lower
step frequency. A progressive adoption of a mid- to fore-
foot and rear-foot strike pattern has been observed during
UR and DR, respectively. During UR, lower limb muscles
perform more net mechanical work compared to LR and
DR to increase the body’s potential energy. The increased
demand for work during UR is met by an increase in power
output at all joints, particularly at the hip which induces
Fig. 4 Metabolic energy cost of
running (C
r
) as a function of
grade. Asterisk indicates
significantly different from level
gradient (P\0.0001). Based on
data from Minetti et al. [61]
G. Vernillo et al.
123

greater muscular activity compared to LR and DR, and in
turn a linear increase in the energy cost of running. In DR,
energy dissipation is higher than energy generation and this
decreases the energy cost during DR until a minimum is
reached at –20 % and increases again at steeper negative
slopes. Thus, the metabolic cost associated with various
types of muscle contractions remains a valid explanation
for the high and low cost of UR and DR, respectively, from
–20 to ?45 % grades.
DR increases tibial shock and impact force, which have
been associated with overuse injuries. Additionally, the
muscle activity required for the increased power and
eccentric energy absorption during DR would place addi-
tional stress on musculoskeletal tissues. However, since in
graded (e.g. trail) running, the locomotion pattern changes
more often than in LR, overuse injuries related to repetitive
movement may be attenuated in graded running compared
to LR.
In conclusion, the present review represents a useful
synthesis of all research describing the relevant biome-
chanical and (neuro)physiological changes associated with
graded running. However, as we have highlighted
throughout this review, important gaps in our biomechan-
ical and physiological understanding of graded running still
exist. In particular, controlled training studies or well-de-
signed interventional experiments are needed to investigate
the effect of manipulating both running speed and positive/
negative slope at the same relative intensity on muscle
activity.
Compliance with Ethical Standards
Funding No sources of funding were used to assist in the preparation
of this article.
Conflict of interest Gianluca Vernillo, Marle
`ne Giandolini, W. Brent
Edwards, Jean-Benoı
ˆt Morin, Pierre Samozino, Nicolas Horvais and
Guillaume Y. Millet declare that they have no conflicts of interest
relevant to the content of this review.
References
1. Bramble DM, Lieberman DE. Endurance running and the evo-
lution of Homo. Nature. 2004;432:345–52.
2. Lieberman DE, Bramble DM. The evolution of marathon running
: capabilities in humans. Sports Med. 2007;37:288–90.
3. Burfoot A. The history of the marathon : 1976-present. Sports
Med. 2007;37:284–7.
4. Hoffman MD, Ong JC, Wang G. Historical analysis of partici-
pation in 161 km ultramarathons in North America. Int J Hist
Sport. 2010;27:1877–91.
5. Millet GY, Tomazin K, Verges S, et al. Neuromuscular conse-
quences of an extreme mountain ultra-marathon. PLoS One.
2011;6:e17059.
6. Saugy J, Place N, Millet GY, et al. Alterations of neuromuscular
function after the world’s most challenging mountain ultra-
marathon. PLoS One. 2013;8:e65596.
7. Vernillo G, Rinaldo N, Giorgi A, et al. Changes in lung function
during an extreme mountain ultramarathon. Scand J Med Sci
Sports. 2015;25:e374–80.
8. Vernillo G, Savoldelli A, Zignoli A, et al. Influence of the
world’s most challenging mountain ultra-marathon on energy
cost and running mechanics. Eur J Appl Physiol.
2014;114:929–39.
9. Cavagna GA, Saibene FP, Margaria R. Mechanical work in
running. J Appl Physiol. 1964;19:249–56.
10. Gottschall JS, Kram R. Ground reaction forces during downhill
and uphill running. J Biomech. 2005;38:445–52.
11. Higham TE, Biewener AA. Integration within and between
muscles during terrestrial locomotion: effects of incline and
speed. J Exp Biol. 2008;211:2303–16.
12. 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.
13. Roberts TJ, Belliveau RA. Sources of mechanical power for
uphill running in humans. J Exp Biol. 2005;208:1963–70.
14. Snyder KL, Farley CT. Energetically optimal stride frequency in
running: the effects of incline and decline. J Exp Biol.
2011;214:2089–95.
15. Snyder KL, Kram R, Gottschall JS. The role of elastic energy
storage and recovery in downhill and uphill running. J Exp Biol.
2012;215:2283–7.
16. Mastroianni GR, Zupan MF, Chuba DM, et al. Voluntary pacing
and energy cost of off-road cycling and running. Appl Ergon.
2000;31:479–85.
17. Townshend AD, Worringham CJ, Stewart IB. Spontaneous pac-
ing during overground hill running. Med Sci Sports Exerc.
2010;42:160–9.
18. Millet GP, Millet GY. Ultramarathon is an outstanding model for
the study of adaptive responses to extreme load and stress. BMC
Med. 2012;10:77.
19. Lussiana T, Fabre N, Hebert-Losier K, et al. Effect of slope and
footwear on running economy and kinematics. Scand J Med Sci
Sports. 2013;23:e246–53.
20. Padulo J, Annino G, Migliaccio GM, et al. Kinematics of running
at different slopes and speeds. J Strength Cond Res.
2012;26:1331–9.
21. Padulo J, Annino G, Smith L, et al. Uphill running at iso-effi-
ciency speed. Int J Sports Med. 2012;33:819–23.
22. Padulo J, Powell D, Milia R, et al. A paradigm of uphill running.
PLoS One. 2013;8:e69006.
23. Swanson SC, Caldwell GE. An integrated biomechanical analysis
of high speed incline and level treadmill running. Med Sci Sports
Exerc. 2000;32:1146–55.
24. Telhan G, Franz JR, Dicharry J, et al. Lower limb joint
kinetics during moderately sloped running. J Athl Train.
2010;45:16–21.
25. Lussiana T, He
´bert-Losier K, Mourot L. Effect of minimal shoes
and slope on vertical and leg stiffness during running. J Sport
Health Sci. 2015;4:195–202.
26. DeVita P, Janshen L, Rider P, et al. Muscle work is biased toward
energy generation over dissipation in non-level running.
J Biomech. 2008;41:3354–9.
27. Horvais N, Giandolini M. Foot strike pattern during downhill trail
running. Footwear Sci. 2013;5:S26–7.
28. Giandolini M, Pavailler S, Samozino P, et al. Foot strike pattern
and impact continuous measurement during a trail running race:
proof of concept in a world-class athlete. Footwear Sci.
2015;7:127–37.
29. Giandolini M, Horvais N, Rossi J, et al. Foot strike pattern dif-
ferently affects the axial and transverse components of shock
acceleration and attenuation in downhill trail running. J Biomech.
2016. doi:10.1016/j.jbiomech.2016.04.001.
Biomechanics and Physiology of Graded Running
123

30. Gerritsen KG, van den Bogert AJ, Nigg BM. Direct dynamics
simulation of the impact phase in heel-toe running. J Biomech.
1995;28:661–8.
31. Liu W, Nigg BM. A mechanical model to determine the influence
of masses and mass distribution on the impact force during run-
ning. J Biomech. 2000;33:219–24.
32. Ardigo
`LP, Saibene F, Minetti AE. The optimal locomotion on
gradients: walking, running or cycling? Eur J Appl Physiol.
2003;90:365–71.
33. Saibene F, Minetti AE. Biomechanical and physiological aspects
of legged locomotion in humans. Eur J Appl Physiol.
2003;88:297–316.
34. Mizrahi J, Verbitsky O, Isakov E. Fatigue-induced changes in
decline running. Clin Biomech (Bristol, Avon). 2001;16:207–12.
35. Buczek FL, Cavanagh PR. Stance phase knee and ankle kine-
matics and kinetics during level and downhill running. Med Sci
Sports Exerc. 1990;22:669–77.
36. Yokozawa T, Fujii N, Ae M. Muscle activities of the lower limb
during level and uphill running. J Biomech. 2007;40:3467–75.
37. Chu JJ, Caldwell GE. Stiffness and damping response associated
with shock attenuation in downhill running. J Appl Biomech.
2004;20:291–308.
38. Hamill CL, Clarke TE, Frederick EC, et al. Effects of grade
running on kinematics and impact force. Med Sci Sports Exerc.
1984;16:185.
39. Shorten MR, Winslow DS. Spectral analysis of impact shock
during running. Int J Sport Biomech. 1992;8:288–304.
40. Shih Y, Lin KL, Shiang TY. Is the foot striking pattern more
important than barefoot or shod conditions in running? Gait
Posture. 2013;38:490–4.
41. Derrick TR. The effects of knee contact angle on impact forces
and accelerations. Med Sci Sports Exerc. 2004;36:832–7.
42. Derrick TR, Hamill J, Caldwell GE. Energy absorption of
impacts during running at various stride lengths. Med Sci Sports
Exerc. 1998;30:128–35.
43. Edwards WB, Derrick TR, Hamill J. Musculoskeletal attenuation
of impact shock in response to knee angle manipulation. J Appl
Biomech. 2012;28:502–10.
44. Lafortune MA, Lake MJ, Hennig EM. Differential shock trans-
mission response of the human body to impact severity and lower
limb posture. J Biomech. 1996;29:1531–7.
45. Abe D, Fukuoka Y, Muraki S, et al. Effects of load and gradient
on energy cost of running. J Physiol Anthropol. 2011;30:153–60.
46. McClay IS, Lake MJ, Cavanagh PR. Muscle activity in running.
In: Cavanagh PR, editor. Biomechanics of distance running.
Champaign: Human Kinetics; 1990. p. 165–86.
47. Wall-Scheffler CM, Chumanov E, Steudel-Numbers K, et al.
Electromyography activity across gait and incline: the impact of
muscular activity on human morphology. Am J Phys Anthropol.
2010;143:601–11.
48. Mero A, Komi PV. Force-, EMG-, and elasticity-velocity rela-
tionships at submaximal, maximal and supramaximal running
speeds in sprinters. Eur J Appl Physiol Occup Physiol.
1986;55:553–61.
49. Sloniger MA, Cureton KJ, Prior BM, et al. Anaerobic capacity
and muscle activation during horizontal and uphill running.
J Appl Physiol. 1985;1997(83):262–9.
50. Sloniger MA, Cureton KJ, Prior BM, et al. Lower extremity
muscle activation during horizontal and uphill running. J Appl
Physiol. 1985;1997(83):2073–9.
51. di Prampero PE, Atchou G, Bruckner JC, et al. The energetics of
endurance running. Eur J Appl Physiol Occup Physiol.
1986;55:259–66.
52. Margaria R, Cerretelli P, Aghemo P, et al. Energy cost of run-
ning. J Appl Physiol. 1963;18:367–70.
53. Fletcher JR, Esau SP, Macintosh BR. Economy of running:
beyond the measurement of oxygen uptake. J Appl Physiol.
1985;2009(107):1918–22.
54. Shaw AJ, Ingham SA, Folland JP. The valid measurement of
running economy in runners. Med Sci Sports Exerc.
2014;46:1968–73.
55. Nicol C, Avela J, Komi PV. The stretch-shortening cycle : a
model to study naturally occurring neuromuscular fatigue. Sports
Med. 2006;36:977–99.
56. Komi PV. Stretch-shortening cycle: a powerful model to study
normal and fatigued muscle. J Biomech. 2000;33:1197–206.
57. Cavagna GA. Storage and utilization of elastic energy in skeletal
muscle. Exerc Sport Sci Rev. 1977;5:89–129.
58. Cavagna GA, Heglund NC, Taylor CR. Mechanical work in
terrestrial locomotion: two basic mechanisms for minimizing
energy expenditure. Am J Physiol. 1977;233:R243–61.
59. Cavagna GA, Kaneko M. Mechanical work and efficiency in
level walking and running. J Physiol. 1977;268:467–81.
60. Lichtwark GA, Wilson AM. Interactions between the human
gastrocnemius muscle and the Achilles tendon during
incline, level and decline locomotion. J Exp Biol.
2006;209:4379–88.
61. Minetti AE, Moia C, Roi GS, et al. Energy cost of walking and
running at extreme uphill and downhill slopes. J Appl Physiol.
1985;2002(93):1039–46.
62. Olesen HL. Accumulated oxygen deficit increases with inclina-
tion of uphill running. J Appl Physiol. 1985;1992(73):1130–4.
63. Dick RW, Cavanagh PR. An explanation of the upward drift in
oxygen uptake during prolonged sub-maximal downhill running.
Med Sci Sports Exerc. 1987;19:310–7.
64. Robergs RA, Wagner DR, Skemp KM. Oxygen consumption and
energy expenditure of level versus downhill running. J Sports
Med Phys Fit. 1997;37:168–74.
65. Pivarnik JM, Sherman NW. Responses of aerobically fit men and
women to uphill/downhill walking and slow jogging. Med Sci
Sports Exerc. 1990;22:127–30.
66. Maciejczyk M, Wie˛cek M, Szymura J, et al. Comparison of
physiological and acid-base balance response during uphill, level
and downhill running performed at constant velocity. Acta
Physiol Hung. 2013;100:347–54.
67. Giovanelli N, Ortiz AL, Henninger K, et al. Energetics of vertical
kilometer foot races; is steeper cheaper? J Appl Physiol (1985).
2016;120:370–5.
68. Staab JS, Agnew JW, Siconolfi SF. Metabolic and performance
responses to uphill and downhill running in distance runners. Med
Sci Sports Exerc. 1992;24:124–7.
69. Gregor RJ, Costill DL. A comparison of the energy expenditure
during positive and negative grade running. J Sports Med Phys
Fit. 1973;13:248–52.
70. Kolkhorst FW, Mittelstadt SW, Dolgener FA. Perceived exertion
and blood lactate concentration during graded treadmill running.
Eur J Appl Physiol Occup Physiol. 1996;72:272–7.
71. Takano N. Phase relation and breathong pattern during locomo-
tor/respiratory coupling in uphill and downhill running. Jpn J
Physiol. 1990;45:47–58.
72. Costill DL, Jansson E, Gollnick PD, et al. Glycogen utilization in
leg muscles of men during level and uphill running. Acta Physiol
Scand. 1974;91:475–81.
73. Saltin B, Karlsson J. Muscle glycogen utilization during work of
different intensities. In: Pernow B, Saltin B, editors. Muscle
metabolism during exercise. New York: Springer US; 1971.
p. 289–99.
74. Medbø JI, Mohn AC, Tabata I, et al. Anaerobic capacity deter-
mined by maximal accumulated O
2
deficit. J Appl Physiol.
1985;1988(64):50–60.
G. Vernillo et al.
123

75. Walker GT, Cureton KJ, DuVal HP, et al. Effects of external
loading on peak oxygen deficit during treadmill running (Ab-
stract). Med Sci Sports Exerc. 1994;26:S179.
76. Bangsbo J. Is the O
2
deficit an accurate quantitative measure of
the anaerobic energy production during intense exercise? J Appl
Physiol. 1985;1992(73):1207–9.
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