Content uploaded by Pedro Docampo
Author content
All content in this area was uploaded by Pedro Docampo on Apr 13, 2024
Content may be subject to copyright.
88
|
wileyonlinelibrary.com/journal/sms Scand J Med Sci Sports. 2018;28:88–94.
© 2017 John Wiley & Sons A/S.
Published by John Wiley & Sons Ltd
Accepted: 13 March 2017
DOI: 10.1111/sms.12877
ORIGINAL ARTICLE
Changes in muscle architecture of biceps femoris induced by
eccentric strength training with nordic hamstring exercise
D. Alonso-Fernandez1
|
P. Docampo-Blanco2
|
J. Martinez-Fernandez3
1Department of Physical Education and
Sports,Faculty of Science Education and
Sport,University of Vigo, Pontevedra,
Spain
2Real Club Celta de Vigo S.A.D., Vigo,
Spain
3Football Club Rubin Kazan, Kazan,
Tatarstan republic, Russia
Correspondence
Diego Alonso-Fernandez, Department of
Physical Education and Sports, Faculty of
Science Education and Sport, University of
Vigo, Pontevedra, Spain.
Email: diego_alonso@uvigo.es
Eccentric strength training alters muscle architecture, but it is also an important fac-
tor for the prevention of hamstring injuries. The purpose was to determine the archi-
tectural adaptations of the biceps femoris long head (BFlh) after eccentric strength
training with nordic hamstring exercise (NHE), followed by a subsequent detraining
period. The participants in this intervention (n=23) completed a period of 13 weeks
consisting of a first week of control and prior training, followed by 8 weeks of ec-
centric strength training with NHE, and concluding with a 4- week period of detrain-
ing. The architectural characteristics of the BFlh were measured at rest using
two- dimensional ultrasound before (M1—week 1) and after (M2—week 9) the ec-
centric strength training, and at the end of the detraining period (M3—week 13). The
muscle fascicle length significantly increased (t=−7.73, d=2.28, P<.001) in M2
compared to M1, as well as the muscle thickness (t=−5.23, d=1.54, P<.001), while
the pennation angle presented a significant decrease (t=7.81, d=2.3, P<.001). The
muscle fascicle length decreased significantly (t=6.07, d=1.79, P<.001) in M3 com-
pared to M2, while the pennation angle showed a significant increase (t=−4.63,
d=1.36, P<.001). The results provide evidence that NHE may cause alterations in
the architectural conditions of the BFlh and may have practical implications for
injury prevention and rehabilitation programs.
KEYWORDS
fascicle, hamstring injuries, injury prevention, muscle adaptation, nordic curl, nordic hamstring exercise,
ultrasound
1
|
INTRODUCTION
The architectural characteristics of a muscle largely deter-
mine its ability to produce force1. The pennation angle (PA),
muscle thickness (MT), and fascicle length (FL) are architec-
tural variables which vary when a muscle is subject to me-
chanical stimuli.2-5 These variations affect the function and
the risk of muscle injury; thus, it is important to understand
their nature and potential applications in rehabilitation and
prevention.2,6
Hamstring injuries present a great impact on sport prac-
tice,7 counting for 12%- 29% of all injuries in event categories
involving high- intensity running,8,9 in addition to reporting a
high recurrence rate ranging 22%- 34%.9,10
The scientific literature suggests two main mechanisms
in hamstring lesions. The first occurs when the muscle is
subject to extreme joint positions.11 The second occurs in
high- speed running.10,12 During the terminal swing phase of
the gait cycle, the hamstrings are required to eccentrically
decelerate the knee extension and hip flexion before weight-
bearing.13 At this stage, the hamstrings reach their maximum
length, with the biceps femoris long head (BFlh) reaching
approximately 110% of its length with respect to the bipedal
anatomical position.7 This elevated eccentric stress contrib-
utes to high rates of hamstring injuries during any running
movement,9,14 mostly in the BFlh.15,16
Lesions in the BFlh seem to have an influence on its archi-
tecture, reducing the FL and increasing the PA, with respect
|
89
ALONSO- FERNANDEZ EtAL.
to the uninjured contralateral muscles.17,18 These changes
alter the muscle function, as a greater length of the fascicle
is associated with a higher maximal velocity of contraction1
and a lower incidence rate of injuries.17,18 Eccentric strength
training became an effective method for prevention.19,20
Among other characteristics, it demonstrated its ability to in-
crease muscle FL values and to reduce PA.4,6 These architec-
tural changes are reversible after a detraining period without
eccentric mechanical stimuli.6
Several studies examined the changes in the muscle archi-
tecture by applying eccentric loading assessed by isokinetic
dynamometry.4,6,21,22 However, the use of isokinetic systems
presents a major drawback in the everyday life of athletes,
that is, their limited accessibility due to the high cost and
complex handling.23 Moreover, they are unfeasible as daily
training equipment (especially for large groups of athletes),
their use is time- consuming,23 and they can also be consid-
ered “non- functional” because they bear little resemblance
to actual sporting activities, being used in the sitting posi-
tion.4,6,21,22 Consequently, there is a need to evaluate alter-
native eccentric hamstring training systems that can become
widespread in the daily practice routine of athletes.
The eccentric “nordic hamstring exercise” (NHE) has
shown improvements in strength and dynamic control after
10 weeks of training,24 a reduction in the maximum peak
torque (when approaching full knee extension),25 and a lower
incidence rate of hamstring injuries in athletes and soccer
players.8,19,26 In addition, these exercises have shown a sig-
nificant relationship between the “break-point angle” (angle
at which the individual performing this exercise can no lon-
ger withstand the increased gravity and falls to the ground)
and maximum peak torque of the hamstring measured with
isokinetic dynamometry23 and its ability to change FL in the
BFlh,27 thus suggesting its effectiveness as a basis for a func-
tional eccentric training for athletes. NHE present a simple
learning technique, which is performed with the athlete’s
body mass without requiring additional equipment or mate-
rial and can easily be applied individually or in groups.
Due to the high incidence of the hamstring injuries and
specifically in the BFlh,15,16 it is relevant to observe the
changes that occur in its architecture after an eccentric load-
ing training. However, given the difficulties encountered in
using the isokinetic equipment in the actual and everyday
training routine of athletes, an interesting fact is to check
whether an easily applicable eccentric exercise, such as NHE,
produces architectural changes in the BFlh muscle.
2
|
MATERIALS AND METHOD
2.1
|
Participants
The study involved 23 male participants practicing recrea-
tional physical activity with no history of lower limb injury
in the past 12 months and no previous experience in eccen-
tric training (Table 1). All participants provided the written
informed consent form before carrying out the protocol, and
the previous training session took place at the Faculty of
Education and Sport Sciences, University of Vigo, Spain. The
ethical approval for the study was granted by the Autonomous
Ethics Committee of Research in Galicia, Xunta de Galicia,
General Secretariat, Ministry of Health (Spain), in agreement
with the provisions of the Declaration of Helsinki (reference
number: 2016/158).
2.2
|
Research design
The study lasted 13 weeks. At week 1, participants under-
took an initial assessment of the BFlh muscle architecture
(M1) and later, two sessions of familiarization with NHE to
ensure proper technical execution. Next, an 8- week period of
eccentric training with NHE was performed. At week 9, the
second assessment of the muscle architecture (M2) was per-
formed. Next, the participants underwent 4 weeks of detrain-
ing, avoiding any kind of mechanical stimulus of eccentric
nature. After this period, at week 13, the third assessment of
the muscle architecture (M3) was carried out. All measure-
ments were made at the same time of the day and under the
same conditions for all participants.
2.3
|
Assessment of the BFlh architecture
The use of ultrasound has proven to be a reliable method for
assessing muscle architectural characteristics of the BFlh.18,28
MT, PA, and the estimation of FL were determined from ul-
trasound images obtained along the longitudinal axis of the
muscle belly using a 2D B- mode ultrasound (12 Mhz fre-
quency, 8 cm depth; 14×47 mm field of view; GE Healthcare
Vivid- i, Wauwatosa, USA). The measurement site was the
halfway point between the ischial tuberosity and the posterior
knee joint fold, along the line of the BFlh. Once the scanning
site was determined in each participant, several anatomical
landmarks were taken (ischial tuberosity, fibula head, and
midpoint of the posterior knee joint fold) and photographs
were taken to ensure reproducibility for future assessment
sessions. All architectural measurements were performed
after at least 5 minutes of inactivity, with the participant in
prone decubitus position, with the hip in neutral position, and
the knee was positioned passively in full extension.
To obtain the images, the ultrasound probe was placed
and aligned longitudinally and perpendicular to the posterior
TABLE 1 Characteristics of participants (mean±standard error
of the mean)
Group N Age (years old) Weight (kg) Height (m)
EG 23 25.2±3.3 75.5±8.1 1.76±0.09
90
|
ALONSO- FERNANDEZ EtAL.
thigh in the scanning site on the participant’s skin, which was
previously covered with a conductive gel. The probe was han-
dled carefully by the sonographer (MFJ) to ensure minimal
pressure and to not alter the accuracy of the measurements.29
After the scan, an analysis was carried out by means of
image processing software, MicroDicom, version 0.7.8, de-
veloped in Bulgaria. Following the procedure conducted by
Blazevich et al.,30 six points were digitized for each of the
images. MT was defined as the distance between the superfi-
cial and intermediate aponeuroses of the BFlh. PA was de-
limited between the intermediate aponeurosis and the
direction of a muscle fascicle previously identified in the
image (Figure 1). The aponeurosis angle (AA) was deter-
mined as the angle between the line marked by the aponeuro-
sis and a horizontal line drawn along the captured image.30,31
Finally, FL was defined as the muscle fascicle length existing
between both aponeuroses. Given that the total of the above-
mentioned length cannot be observed in the field of view of
the probe, an estimate was performed by means of an equa-
tion validated by Blazevich et al.30 and Kellis et al.31
where FL=fascicle length, MT=muscle thickness,
AA=aponeurosis angle, and PA=pennation angle.
FL was expressed in absolute terms (cm) and also rela-
tive to MT (RFL=FL/MT). All images were collected and
analyzed by the same researcher (MFJ), who was blinded
to the identity of the participants during the analysis. This
researcher (MFJ), a member of the Spanish Society of
Ultrasound in Physiotherapy (SEEFi), was previously sub-
jected to an intra- rater study to assess the reliability of the
measure. Twelve healthy subjects participated, five 2D-
ultrasound images of the BFlh being performed in the same
anatomical region in different sessions, obtaining reliable
measurements of the different architectural variables (intra-
class correlations>0.90) within the ranges recommended by
previous scientific studies.28
2.4
|
Eccentric “nordic hamstring” exercise
NHE, also known as “nordic curl,” is an exercise designed
to eccentrically strengthen the hamstring muscles12,14 and re-
quires the assistance of a partner (Figure 2).
The athlete begins in a kneeling position with the hip and
trunk elevated and fully aligned. The assistant applies pres-
sure onto the partner’s heels, ensuring their feet remain in
contact with the ground during the entire execution of the ex-
ercise (Figure 2A). At the time, the athlete’s trunk is lowered
FL
=
sin (AA
+
90◦)
×
MT/sin (180◦
−
(AA
+
180◦
−
PA) )
FIGURE 1 Two- dimensional ultrasound image of the biceps
femoris long head (BFlh) taken along the longitudinal axis of the
posterior thigh. From these images, the superficial and intermediate
aponeuroses could be determined, as well as the muscle thickness and
fascicle angle with respect to the aponeurosis. The estimations of the
fascicle length can be performed through a trigonometric calculation,
using the muscle thickness and the pennation angle
FIGURE 2 Nordic hamstring exercise: (A) start, (B) midpoint
indicating the Nordic break- point angle, and (C) end
(A)
(B)
(C)
|
91
ALONSO- FERNANDEZ EtAL.
forward maintaining the initial position through a controlled
extension of the knees (Figure 2B). This fall is performed at
the slowest speed possible to maximize the muscle load in
the eccentric phase. Hands and arms are used to buffer the
fall after the break-point angle (angle at which the athlete
could no longer withstand the increased gravity and falls to
the ground; Figure 2C) and to return to the kneeling position
minimizing the load of the concentric phase.24 In the present
study, all participants were instructed properly on the correct
execution technique of NHE 2 days before training, to max-
imize their effectiveness. Moreover, graduates in Physical
Activity and Sport Sciences supervised the training sessions
to ensure the quality and consistency of the execution of each
participant at all times.
2.5
|
Intervention
The intervention was designed with the aim of promoting a
progressive assimilation of the eccentric mechanical stimuli
and reducing delayed onset muscle soreness (DOMS) in
participants.
Each training session lasted between 10 and 20 minutes,
depending on the training volume of sets and repetitions ac-
cording to the evolution of the program (Table 2). All ses-
sions were separated by at least 48 hours and preceded by
12- minute standardized warm- up self- loading exercises. All
participants were provided with constant visual and verbal
feedback, to contribute to their motivation and correct tech-
nical execution.
2.6
|
Statistical analysis
All statistical analyses were performed using the SPSS
software, version 24.0 (IBM Corporation, Chicago, IL).
Where appropriate, data were screened for normal distri-
bution using the Shapiro- Wilk test and homoscedasticity
through Levene’s test. The Greenhouse- Geisser adjustment
was applied when the assumption of sphericity was violated
(P<.05 for Mauchly’s test of sphericity). One- way repeated-
measures ANOVAs were used to determine training- induced
changes in BFlh architecture (FL, RFL, MT and PA). The
within- subject variable was time (M1, M2, and M3). In addi-
tion, post- hoc t- tests with Bonferroni adjustments were used
to establish the pairwise comparisons between measured
variables (M1- M2, M2- M3). Significance was set at P<.05,
and where appropriate, Cohen’s d was reported as a measure
of the effect size.
3
|
RESULTS
The results obtained are detailed below according to the dif-
ferent measured variables of muscle architecture.
3.1
|
Fascicle length
The length of the muscle fascicle is affected by the ec-
centric training protocol with the functional NHE,
F(1.77- 38.92)=41.39, P<.05,
n2
p
=0.65. Regarding the pair-
wise comparisons derived from the post hoc analysis, there is
a significant increase in FL between M1 and M2 (t=−7.73,
d=2.28, P<.001) and a significant decrease between M2 and
M3 (t=6.07, d=1.79, P<.001).
3.2
|
Fascicle length relative to
muscle thickness
The fascicle length relative to muscle thickness is affected
by the eccentric training protocol with functional NHE,
F(1.74- 38.21)=18.19, P<.05,
n2
p
=0.45. As for the pairwise
comparisons derived from the post hoc analysis, there is a
significant increase in RFL between M1 and M2 (t=−5.08,
d=1.49, P<.001). On the other hand, there is a significant de-
crease in RFL length between M2 and M3 (t=2.76, d=0.81,
P<.05).
3.3
|
Muscle thickness
Muscle thickness is affected by the eccentric training pro-
tocol with functional NHE, F(1.73- 38.08)=13.64, P<.05,
n2
p
Week
No. of
sessions/wk Sets Repetitions
Total no. of
repetitions Rest between sets
1 2 2 6 24 2 min
2 2 2 6 24 2 min
3 3 3 4 36 2 min
4 3 3 6 54 2 min
5 3 3 8 72 2 min
6 3 3 8 72 2 min
7 3 3 10 90 2 min
8 3 3 10 90 2 min
TABLE 2 Eccentric training
progression with NHE
92
|
ALONSO- FERNANDEZ EtAL.
=0.38. Regarding the pairwise comparisons derived from the
post hoc analysis, there is a significant increase in MT be-
tween M1 and M2 (t=−5.23, d=1.54, P<.001) and a signifi-
cant decrease between M2 and M3 (t=3.64, d=1.07, P<.05).
3.4
|
Pennation angle
The pennation angle is affected by the eccentric training pro-
tocol with functional NHE, F(1.92- 42.31)=31.03, P<.05,
n2
p
=0.58. Regarding the pairwise comparisons derived from
the post hoc analysis, there is a significant decrease in PA be-
tween M1 and M2 (t=7.81, d=2.3, P<.001) and a significant
increase between M2 and M3 (t=−4.63, d=1.36, P<.001).
The changes in the FL, RFL, PA, and MT during the train-
ing and detraining period are shown in Table 3.
4
|
DISCUSSION
This study reported changes in the muscle architecture of the
BFlh in response to an 8- week eccentric training protocol
with NHE and a subsequent 4- week detraining period. The
main conclusion is that eccentric training with NHE resulted
in a significant increase in FL and MT of the BFlh and a sig-
nificant decrease in PA. In addition, a significant reduction in
FL and MT was found, as well as a significant increase in PA
after detraining period.
The main contribution of these findings is in the field of
practical application which, in the actual training, may lead to
obtaining architectural changes by means of an exercise which
is easy to reproduce and perform, such as NHE. So far, the
architectural changes had been studied under laboratory condi-
tions using expensive isokinetic equipment, beyond the reach
of most athletes and coaches, and unusable in large group train-
ing. In this case, the changes in the muscle architecture have
been studied using an exercise which can be applied in the ac-
tual training situations, achieving results comparable to those
obtained in previous studies with isokinetic dynamometry.
The observed increase in FL of the BFlh at rest is similar
to the results found in the previous literature. Potier et al.,4
after an eccentric strength training program of 8 weeks, ob-
tained a significant increase of 34% in FL of the BFlh. More
recently, Timmins et al.6 with an eccentric training protocol
of 6 weeks have obtained similar results, with a significant
increase in FL of the BFlh, of 16%. In the same vein, our
study showed a significant increase of 23.9% for FL of the
BFlh at rest, using an 8- week eccentric strength protocol
with NHE. The differences in the duration of the interven-
tion (6- 8 weeks) and in the training modality (curl leg, isoki-
netic dynamometry, and NHE, respectively) can explain the
differences between studies, but all authors agree on the FL
increase after eccentric strength training that could be due to
an increase in serial sarcomeres.32 This situation is also rein-
forced by a significant increase in RFL, matching the results
obtained by Timmins et al.6 and especially those obtained
by Bourne et al.27 in a recent study, where after applying
10 weeks of training with NHE, a significant increase in FL
in BFlh is observed.
PA showed a significant reduction after the training pe-
riod, which coincides with the results obtained by Timmins
et al.,6 but differs from the non- significant reduction of 3.1%,
obtained by Potier et al.4 although the authors themselves
pointed to this result as “counterintuitive.” The changes in PA
seem to be very closely related to the nature of each muscle,
but it is possible that increases in PA are reliant on the extent
of fiber hypertrophy that occurs and that concurrent increases
in FL may counter the tendency for PA to increase.4,33
The present study is the only one that obtained significant
changes in MT of the BFlh after an eccentric training period,
considering that the previous literature 6 does not provide
significant changes in the above- mentioned variable in the
BFlh. However, studies on the architecture of other muscle
groups, such as the vastus lateralis21,22 and rectus femoris,21
observe a significant increase in MT after a period of eccen-
tric strength training. In addition, Bourne et al.,27 using mag-
netic resonance imaging (MRI), observed an increase in the
volume of BFlh after undergoing a 10- week training protocol
with NHE.
The results also showed that the changes in the muscle
architecture induced by eccentric training with NHE were
TABLE 3 Changes in muscle architecture of the biceps femoris long head before (M1) and after (M2) the intervention and after the period of
detraining (M3) (mean±standard error of the mean)
Eccentric protocol with NHE (n=23)
M1 (Week 1) M2 (Week 9) M3 (Week 13) % Change M1- M2 % Change M2- M3
FL (cm) 8.17±1.83 10.12±1.85** 8.90±1.70## 23.9 −12.1
RFL 3.91±0.39 4.53±0.55** 4.27±0.49#15.9 −5.7
PA (º) 14.74±1.91 12.55±1.34** 13.71±1.22## −14.8 9.2
MT (cm) 2.09±0.47 2.25±0.39** 2.10±0.45#7.7 −6.6
FL, fascicle length; RFL, fascicle length relative to muscle thickness; PA, pennation angle; MT, muscle thickness.
**P<.001 vs M1, #P<.05 vs M2, ##P<.001 vs M2.
|
93
ALONSO- FERNANDEZ EtAL.
reversed after a 4- week detraining period. A significant de-
crease in FL and MT is reported, whereas PA increases. These
results are consistent with those found in previous studies.5,6
The responses to the intervention by eccentric training
with NHE and subsequent detraining may be of interest for
the prevention and rehabilitation of injuries to the hamstring
muscles as, as explained, shorter muscle fascicles are more
prone to injury than longer fascicles.18,34 The lesions in the
BFlh modify its architecture, reducing the length of the fas-
cicles, increasing the pennation angle, and making it more
sensitive to relapse.17,18 These reasons seem sufficient to in-
troduce eccentric strength content in the training plan of ath-
letes at risk of suffering hamstring injuries, and this content
has proven to be an element of protection and rehabilitation
of these types of injuries. In addition, the reversibility of the
architectural changes when the eccentric stimulus disappears
indicated that the constant exposure to such stimuli can be
determining to maintain its structural effect in the long run.
So far, these potential benefits of eccentric training were
hardly transposed to the daily routine of athletes, as they had
been obtained with specialized equipment and conditions
beyond their reach.4,6,21,22 In our view, this can be the main
contribution of this study for practical purposes: having ob-
tained a method of eccentric training of the hamstrings with
an exercise such as NHE, which can be easily applied (with-
out additional equipment) and of short duration (between 10
and 15 minutes, 2- 3 sessions per week), proving to be effec-
tive for modifying the variables of the muscle architecture of
the BFlh.
The authors acknowledge that there are some limitations
in the current study. First, the architecture evaluation using
2D ultrasound requires a certain degree of estimation because
FL is not entirely visible in the ultrasound image. Although
the estimation equation used in this study was validated,31
there is still a potential error that should be reduced in fu-
ture works based on 2D ultrasound. Secondly, only the BFlh
architecture was evaluated, and considering that each ham-
string has unique architectural characteristics, it would not be
appropriate to generalize the results to all knee flexors.
Further research will be needed to establish the appli-
cation conditions of this training type in order to achieve
long- lasting architectural effects in different populations of
athletes, but, in our opinion, the results may have practical
implications in the prevention of BFlh injuries and in rehabil-
itation programs that may take into account the architectural
alterations caused by training as a factor that may lower the
risk of future injury.
PERSPECTIVES
The mechanical stimuli of eccentric nature seem to modify
the muscle architecture of the BFlh, increasing FL. This
evidence has possible impact on the prevention of hamstring
injuries, as the latter decrease FL, thus increasing the risk
of recurrence. However, previous results have always been
obtained using isokinetic equipment, which is not read-
ily accessible to athletes. This study is aimed at examining
whether the eccentric NHE produce changes in the muscle
architecture of the BFlh. The reason for choosing NHE is
their simplicity and easy reproducibility; thus, they can be
easily applied to any athlete individually or collectively in
prevention or rehabilitation programs, without additional
equipment. The adaptations produced by NHE in this study
may have practical implications for injury prevention and re-
habilitation programs which include the changes in muscle
architecture variables.
ACKNOWLEDGEMENTS
The authors would like to thank Dr. Águeda Gutiérrez
Sánchez, Dr. Margarita Pino Juste, and Dr. Antonio Rial
Boubeta for their useful contributions to the production of
this manuscript, as well as to the Faculty of Education and
Sport Sciences, University of Vigo, for allowing the use of
their facilities.
REFERENCES
1. Lieber RL, Ward SR. Skeletal muscle design to meet functional de-
mands. Philos Trans R Soc Lond B Biol Sci. 2011;366:1466‐1476.
2. Blazevich AJ, Cannavan D, Coleman DR, Horne S. Influence
of concentric and eccentric resistance training on architec-
tural adaptation in human quadriceps muscles. J Appl Physiol.
2007;103:1565‐1575.
3. Narici MV, Flueck M, Koesters A, etal. Skeletal muscle remod-
eling in response to alpine skiing training in older individuals.
Scand J Med Sci Sports. 2011;21(1 Suppl):23‐28.
4. Potier TG, Alexander CM, Seynnes OR. Effects of eccentric
strength training on biceps femoris muscle architecture and knee
joint range of movement. Eur J Appl Physiol. 2009;105:939‐944.
5. Seynnes OR, Maganaris CN, de Boer MD, di Prampero PE, Narici
MV. Early structural adaptations to unloading in the human calf
muscles. Acta Physiol (Oxf). 2008;193:265‐274.
6. Timmins RG, Ruddy JD, Presland J, etal. Architectural changes
of the biceps femoris long head after concentric or eccentric train-
ing. Med Sci Sports Exerc. 2016;48:499‐508.
7. Thelen DG, Chumanov ES, Hoerth DM, etal. Hamstring mus-
cle kinematics during treadmill sprinting. Med Sci Sports Exerc.
2005;37:108‐114.
8. Brooks JHM, Fuller CW, Kemp SPT, Reddin DB. Incidence, risk
and prevention of hamstring muscle injuries in professional rugby
union. Am J Sports Med. 2006;34:1297‐1306.
9. Orchard J, Seward H, Orchard JJ. Results of 2 decades of injury
surveillance and public release of data in the Australian Football
League. Am J Sports Med. 2013;41:734‐741.
10. Marcus C, Elliott CW, Zarins B, Powell JW, Kenyon CD.
Hamstring muscle strains in professional football players: 10year
review. Am J Sports Med. 2011;39:843‐850.
94
|
ALONSO- FERNANDEZ EtAL.
11. Askling CM, Tengvar M, Saartok T, Thorstensson A. Proximal
hamstring strains of stretching type in different sports: injury sit-
uations, clinical and magnetic resonance imaging characteristics,
and return to sport. Am J Sports Med. 2008;36:1799‐1804.
12. Mendiguchia J, Alentorn-Geli E, Brughelli M. Hamstring strain
injuries: are we headed in the right direction? Br J Sports Med.
2012;42:81‐86.
13. Yu B, Queen RM, Abbey AN, Liu Y, Moorman CT, Garrett WE.
Hamstring muscle kinematics and activation during overground
sprinting. J Biomech. 2008;41:3121‐3126.
14. Schache AG, Dorn TW, Blanch PD, Brown NA, Pandy MG.
Mechanics of the human hamstring muscle during sprinting. Med
Sci Sports Exerc. 2012;44:647‐658.
15. Koulouris G, Connell DA, Brukner P, Schneider-Kolsky M.
Magnetic resonance imaging parameters for assessing risk of
recurrent hamstring injuries in elite athletes. Am J Sports Med.
2007;35:1500‐1506.
16. Opar D, Williams MD, Timmins RG, Hickey J, Duhig SJ, Shield
AJ. Eccentric hamstring strength and hamstring injury risk in
Australian Footballers. Med Sci Sports Exerc. 2015;47:857‐865.
17. Sharifnezhad A, Marzilger R, Arampatzis A. Effects of load mag-
nitude, muscle length and velocity during eccentric chronic load-
ing on the longitudinal growth of the vastus lateralis muscle. J
Exp Biol. 2014;217(Pt 15):2726‐2733.
18. Timmins RG, Shield AJ, Williams MD, Lorenzen C, Opar DA.
Biceps femoris long head architecture: a reliability and retrospec-
tive injury study. Med Sci Sports Exerc. 2015;47:905‐913.
19. Arnason A, Anderson TE, Holme I, Engebretsen L, Bahr R.
Prevention of hamstring strains in elite soccer: an intervention
study. Scand J Med Sci Sports. 2008;18:40‐48.
20. Askling C, Karlsson J, Thorstensson A. A hamstring injury oc-
currence in elite soccer players after preseason training with ec-
centric overload. Scand J Med Sci Sports. 2003;13:244‐250.
21. Baroni BM, Geremia JM, Rodrigues R, De Azevedo Franke R,
Karamanidis K, Vaz MA. Muscle architecture adaptations to knee
extensor eccentric training: rectus femoris vs. vastus lateralis.
Muscle Nerve. 2013;48:498‐506.
22. Malas FÜ, Ozçakar L, Kaymak B, et al. Effects of different
strength training on muscle architecture: clinical and ultrasono-
graphic evaluation in knee osteoarthritis. Am J Phys Med Rehabil.
2013;5:655‐662.
23. Sconce E, Jones P, Tuner E, Comfort P, Graham-Smith P. The
validity of the nordic hamstring lower for a field- based as-
sessment of eccentric hamstring strength. J Sport Rehabil.
2015;24:13‐20.
24. Mjølsnes R, Arnason A, Osthagen T, Raastad T, Bahr R. A
10- week randomised trial comparing eccentric vs concentric
hamstring strength training in well- trained soccer players. Scand
J Med Sci Sports. 2004;14:311‐317.
25. Clark R, Bryant A, Culgan JP, Hartley B. The effects of eccentric
hamstring strength training on dynamic jumping performance and
isokinetic strength parameters: a pilot study on the implications for
the prevention of hamstring injuries. Phys Ther Sport. 2005;6:67‐73.
26. Van der Horst N, Smits DW, Petersen J, Goedhart EA, Backx F.
The preventive effect of the nordic hamstring exercise on ham-
string injuries in amateur soccer players: a randomized controlled
trial. Am J Sports Med. 2015;43:1316‐1323.
27. Bourne MN, Duhig SJ, Timmins RG, etal. Impact of the Nordic
hamstring and hip extension exercises on hamstring architecture
and morphology: implications for injury prevention. Br J Sports
Med. 2016;1‐9.
28. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerretelli
P. In vivo human gastrocnemius architecture with changing joint
angle at rest during graded isometric contraction. J Physiol.
1996;496:287‐297.
29. Klimstra M, Dowling J, Durkin JL, MacDonald M. The effect
of ultrasound probe orientation on muscle architecture measure-
ment. J Electromyogr Kinesiol. 2007;17:504‐514.
30. Blazevich AJ, Gill ND, Zhou S. Intra- and intermuscular varia-
tion in human quadriceps femoris architecture assessed in vivo. J
Anat. 2006;209:289‐310.
31. Kellis E, Galanis N, Natsis K, Kapetanos G. Validity of ar-
chitectural properties of the hamstring muscles: correlation
of ultrasound findings with cadaveric dissection. J Biomech.
2009;42:2549‐2554.
32. Lynn R, Morgan DL. Decline running produces more sarcomeres
in rat vastus intermedius muscle fibers than does incline running.
J Appl Physiol. 1994;77:1439‐1444.
33. Foure A, Nordez A, Cornu C. Effects of eccentric training on me-
chanical properties of the plantar flexor muscle- tendon complex.
J Appl Physiol. 2013;114:523‐537.
34. Fyfe JJ, Opar DA, Williams MD, Shield AJ. The role of neu-
romuscular inhibition in hamstring strain injury recurrence. J
Electromyogr Kinesiol. 2013;23:523‐530.
How to cite this article: Alonso-Fernandez D,
Docampo-Blanco P, Martinez-Fernandez J. Changes in
muscle architecture of biceps femoris induced by
eccentric strength training with nordic hamstring
exercise. Scand J Med Sci Sports. 2018;28:88–94.
https://doi.org/10.1111/sms.12877
