Content uploaded by Kristin Briem
Author content
All content in this area was uploaded by Kristin Briem on Nov 20, 2014
Content may be subject to copyright.
Dear Author,
Here are the proofs of your article.
•You can submit your corrections online, via e-mail or by fax.
•For online submission please insert your corrections in the online correction form. Always
indicate the line number to which the correction refers.
•You can also insert your corrections in the proof PDF and email the annotated PDF.
•For fax submission, please ensure that your corrections are clearly legible. Use a fine black
pen and write the correction in the margin, not too close to the edge of the page.
•Remember to note the journal title, article number, and your name when sending your
response via e-mail or fax.
•Check the metadata sheet to make sure that the header information, especially author names
and the corresponding affiliations are correctly shown.
•Check the questions that may have arisen during copy editing and insert your answers/
corrections.
•Check that the text is complete and that all figures, tables and their legends are included. Also
check the accuracy of special characters, equations, and electronic supplementary material if
applicable. If necessary refer to the Edited manuscript.
•The publication of inaccurate data such as dosages and units can have serious consequences.
Please take particular care that all such details are correct.
•Please do not make changes that involve only matters of style. We have generally introduced
forms that follow the journal’s style.
Substantial changes in content, e.g., new results, corrected values, title and authorship are not
allowed without the approval of the responsible editor. In such a case, please contact the
Editorial Office and return his/her consent together with the proof.
•If we do not receive your corrections within 48 hours, we will send you a reminder.
•Your article will be published Online First approximately one week after receipt of your
corrected proofs. This is the official first publication citable with the DOI. Further changes
are, therefore, not possible.
•The printed version will follow in a forthcoming issue.
Please note
After online publication, subscribers (personal/institutional) to this journal will have access to the
complete article via the DOI using the URL: http://dx.doi.org/[DOI].
If you would like to know when your article has been published online, take advantage of our free
alert service. For registration and further information go to: http://www.springerlink.com.
Due to the electronic nature of the procedure, the manuscript and the original figures will only be
returned to you on special request. When you return your corrections, please inform us if you would
like to have these documents returned.
Metadata of the article that will be visualized in OnlineFirst
ArticleTitle Medial hamstring muscle activation patterns are affected 1–6 years after ACL reconstruction using hamstring
autograft
Article Sub-Title
Article CopyRight Springer-Verlag Berlin Heidelberg
(This will be the copyright line in the final PDF)
Journal Name Knee Surgery, Sports Traumatology, Arthroscopy
Corresponding Author Family Name Briem
Particle
Given Name Kristín
Suffix
Division Department of Physical Therapy, School of Health Sciences
Organization University of Iceland
Address Saemundargata 2, Reykjavik, 101, Iceland
Email kbriem@hi.is
Author Family Name Birnir
Particle
Given Name Bjartmar
Suffix
Division Department of Physical Therapy, School of Health Sciences
Organization University of Iceland
Address Saemundargata 2, Reykjavik, 101, Iceland
Email
Author Family Name Guðnason
Particle
Given Name Garðar
Suffix
Division Department of Physical Therapy, School of Health Sciences
Organization University of Iceland
Address Saemundargata 2, Reykjavik, 101, Iceland
Email
Author Family Name Árnason
Particle
Given Name Stefán Magni
Suffix
Division Department of Physical Therapy, School of Health Sciences
Organization University of Iceland
Address Saemundargata 2, Reykjavik, 101, Iceland
Email
Author Family Name Guðmundsson
Particle
Given Name Tómas Emil
Suffix
Division Department of Physical Therapy, School of Health Sciences
Organization University of Iceland
Address Saemundargata 2, Reykjavik, 101, Iceland
Email
Schedule
Received 14 July 2013
Revised
Accepted 16 September 2013
Abstract Purpose:
Although changes in hamstring muscle morphology after anterior cruciate ligament reconstruction (ACLR)
using a semitendinosus autograft hamstrings-gracilis (HG) of the ipsilateral limb are recognized, alterations
in muscle activation patterns have not been extensively studied. The purpose of this controlled laboratory
trial was therefore to monitor muscle activation levels of the medial (MH) and lateral (LH) hamstring muscles
in athletes who had undergone ACLR using a HG and to contrast these to activation levels demonstrated by
healthy controls.
Methods:
Surface electromyography (EMG) was sampled from bilateral hamstring muscles of 18 athletes 1–6 years
after ACLR and 18 matched controls (CTRL) during the performance of two dissimilar exercises, both
involving eccentric knee flexor activity. Peak normalized muscle activation levels were identified for MH
and LH of both limbs during the performance of the Nordic Hamstring (NH) exercise and TRX® hamstring
curl (TRX) exercise.
Results:
A statistically significant limb by exercise interaction was found for peak activation levels of LH, due to
significant interlimb differences in activation during the performance of the TRX exercise compared to more
symmetrical activation during the NH (p < 0.001). A three-way interaction was found for peak activation
levels of MH, due to group differences in peak muscle activation between limbs and exercise type (p = 0.025).
Whereas CTRL group participants consistently favoured one limb over the other during the performance of
both exercises, ACLR participants demonstrated dissimilar peak MH activation patterns between limbs during
the performance of the NH exercise compared to the TRX.
Conclusions:
In the light of these results and considering the surgical procedure, patients that undergo ACLR using a HG
autograft from the ipsilateral limb may benefit from post-operative rehabilitation that involves muscle
activation and strengthening specifically targeting the MH component.
Keywords (separated by '-') ACL reconstruction - Autograft - EMG - Hamstring
Footnote Information
UNCORRECTED PROOF
KNEE
1
2Medial hamstring muscle activation patterns are affected
31–6 years after ACL reconstruction using hamstring autograft
4Kristı
´n Briem •Bjartmar Birnir •Garðar Guðnason •
5Stefa
´n Magni A
´rnason •To
´mas Emil Guðmundsson
6Received: 14 July 2013 / Accepted: 16 September 2013
7ÓSpringer-Verlag Berlin Heidelberg 2013
8Abstract
9Purpose Although changes in hamstring muscle mor-
10 phology after anterior cruciate ligament reconstruction
11 (ACLR) using a semitendinosus autograft hamstrings-
12 gracilis (HG) of the ipsilateral limb are recognized, alter-
13 ations in muscle activation patterns have not been exten-
14 sively studied. The purpose of this controlled laboratory
15 trial was therefore to monitor muscle activation levels of
16 the medial (MH) and lateral (LH) hamstring muscles in
17 athletes who had undergone ACLR using a HG and to
18 contrast these to activation levels demonstrated by healthy
19 controls.
20 Methods Surface electromyography (EMG) was sampled
21 from bilateral hamstring muscles of 18 athletes 1–6 years
22 after ACLR and 18 matched controls (CTRL) during the
23 performance of two dissimilar exercises, both involving
24 eccentric knee flexor activity. Peak normalized muscle
25 activation levels were identified for MH and LH of both
26 limbs during the performance of the Nordic Hamstring
27 (NH) exercise and TRX
Ò
hamstring curl (TRX) exercise.
28 Results A statistically significant limb by exercise inter-
29 action was found for peak activation levels of LH, due to
30 significant interlimb differences in activation during the
31 performance of the TRX exercise compared to more
32 symmetrical activation during the NH (p\0.001). A
33 three-way interaction was found for peak activation levels
34 of MH, due to group differences in peak muscle activation
35 between limbs and exercise type (p=0.025). Whereas
36 CTRL group participants consistently favoured one limb
37
over the other during the performance of both exercises,
38
ACLR participants demonstrated dissimilar peak MH
39
activation patterns between limbs during the performance
40
of the NH exercise compared to the TRX.
41
Conclusions In the light of these results and considering
42
the surgical procedure, patients that undergo ACLR using a
43
HG autograft from the ipsilateral limb may benefit from
44
post-operative rehabilitation that involves muscle activa-
45
tion and strengthening specifically targeting the MH
46
component.
47
48
Keywords ACL reconstruction Autograft EMG
49
Hamstring
50
Introduction
51
Anterior cruciate ligament (ACL) injuries seriously impact
52
the lives of those who suffer them, and both direct and
53
indirect costs of ACL reconstruction (ACLR) and reha-
54
bilitation are immense [12,15,24]. Although not always
55
required [9,13], many of those who rupture their ACL
56
undergo surgery that aims to restore knee joint stability and
57
function by reconstructing the ligament, most commonly
58
with an autograft from the ipsilateral limb. This may be
59
necessary for individuals who participate in demanding
60
activities that involve pivoting and rapid acceleration/
61
deceleration. The most common harvest sites are the
62
patellar tendon [bone-patellar tendon-bone (BPTB)] and
63
semitendinosus muscle component of the hamstrings,
64
where strands from the gracilis muscle are frequently used
65
to augment the graft [hamstrings-gracilis (HG)].
66
Overall, risk of post-surgical complications, such as
67
anterior knee pain and range of motion (ROM) impair-
68
ments, seems to be greater when BPTB grafts are used,
A1 K. Briem (&)B. Birnir G. Guðnason
A2 S. M. A
´rnason T. E. Guðmundsson
A3 Department of Physical Therapy, School of Health Sciences,
A4 University of Iceland, Saemundargata 2, 101 Reykjavik, Iceland
A5 e-mail: kbriem@hi.is
123
Journal : Large 167 Dispatch : 20-9-2013 Pages : 6
Article No. : 2696 hLE hTYPESET
MS Code : KSST-D-13-00605 hCP hDISK
44
Knee Surg Sports Traumatol Arthrosc
DOI 10.1007/s00167-013-2696-4
Author Proof
UNCORRECTED PROOF
69 while relative knee joint laxity remains a concern for HG
70 reconstruction [18,19]. While joint stability may be ade-
71 quately restored, arthrokinematics of the joint and kine-
72 matics of the lower limb are affected and may influence the
73 rate of progression of knee OA [8,9,16,25]. Graft failure
74 rate is reportedly almost 6 % at a minimum 5 years post-
75 ACLR [32] and around 10 % 15 years after reconstruction
76 [5], with no demonstrable statistically significant difference
77 between graft types. Revision surgery has been shown to
78 result in worse patient-reported outcomes compared with
79 primary ACLR, and revisions have a threefold to fourfold
80 greater failure rate than prospective series of primary ACL
81 reconstructions [31].
82 Post-surgical muscle weakness is recognized to be
83 dependent on the graft donor site as is the need for specific
84 rehabilitation based on the graft used [33]. Quadriceps
85 strength and overall lower extremity function is rigorously
86 tested during the course of rehabilitation, particularly with
87 respect to whether an athlete is ready to return to high level
88 sports activities and competition [30]. Muscle strength of
89 knee flexors collectively is typically well monitored during
90 the months of rehabilitation after ACLR using an ipsilateral
91 HG autograft [30]. However, specific training and testing
92 for the medial versus lateral components is not routine,
93 despite findings demonstrating selective medial hamstring
94 (MH) weakness, even more than 2 years after surgery [3,
95 26]. This may be of particular importance in the light of the
96 mechanism of non-contact ACL injuries, as the MH com-
97 ponent has the potential to counter the external outward
98 rotating knee moments associated with ACL rupture [4].
99 Magnetic resonance imaging (MRI) has in recent years
100 been used to demonstrate the potentially negative effects of
101 HG harvesting for ACLR by evaluating quality of tendon
102 regeneration in the months and years after surgery, as well
103 as muscle cross-sectional area (CSA) or volume [6,20,21,
104 27]. A proximal migration of the muscle–tendon junction
105 of the semitendinosus is generally found [6,27], and this,
106 paired with muscle atrophy, may explain muscle weakness
107 that is most often found in tests performed in deep knee
108 flexion [2,6,29]. Ristanis et al. [23] used electromyogra-
109 phy (EMG) to investigate how ACLR using HG grafts
110 affected timing of muscle activation of the semitendinosus
111 and biceps femoris. They demonstrated significant elec-
112 tromechanical delay in the ipsilateral knee flexors com-
113 pared to the contralateral limb and controls. However, the
114 effect of the surgery on the magnitude of hamstring muscle
115 activation levels during functional exercises is an under-
116 investigated area. Identifying specific alterations may have
117 important implications with respect to rehabilitation after
118 ACLR and may thereby positively affect athletes’ suc-
119 cessful return to competition with minimal risk of re-injury.
120 Therefore, the main purpose of this controlled laboratory
121 trial was to assess muscle activation levels in bilateral
122
lower extremities during two dissimilar hamstring exer-
123
cises. Specifically, the aim was to contrast muscle activa-
124
tion patterns of MH versus lateral hamstring (LH) of
125
healthy athletes and individuals that had undergone ACLR
126
using a semitendinosus autograft. The ‘a priori’ hypothesis
127
was that interlimb differences in peak hamstring activation
128
would only be found in the reconstructed participants.
129
Materials and methods
130
Eighteen soccer players (ACLR group), who all had
131
undergone ACLR 1–6 years previously, were recruited
132
from the men’s and women’s top leagues in Iceland. Of
133
these 18 individuals, 12 were operated on the left side and
134
6 on the right. The 18 controls (CTRL group) were
135
recruited from the same teams and were matched for
136
gender, ‘involved’ side designation, height and weight
137
(Table 1). All ACLR participants had successfully returned
138
to full participation in their sport. Exclusion criteria were
139
any orthopaedic condition precluding them from full par-
140
ticipation in competition and history of muscle strain in the
141
knee flexor muscles within the past 3 months. The study
142
was approved by the National Bioethics Committee, and
143
informed consent was obtained from participants prior to
144
data collection.
145
Wireless surface EMG (Kine Pro, Hafnarfjordur, Ice-
146
land) was used to monitor muscle activity during two
147
exercises targeting eccentric activity of the hamstring
148
muscles, using a signal bandwidth of 16–500 Hz, sampling
149
at a rate of 1600 Hz. Electrodes were placed over the
150
muscle bellies of semitendinosus and biceps femoris
151
muscles (MH and LH) of both lower extremities. SENIAM
152
guidelines [28] were used for electrode placement as well
153
as palpation during muscle contraction in order to identify
154
the optimal position. The skin was cleaned and hair
155
removed if necessary prior to surface electrode placement.
156
The raw EMG data were high-pass filtered at 25 Hz, full-
157
wave rectified and the root-mean-square of the signal was
Table 1 Number of male versus female participants, leg dominance
as involved (‘Inv’) versus uninvolved (‘Un’) limb, and group mean
(SD) height, weight and body mass index (BMI)
ACLR CTRL
Male/female 8/10 8/10
Left/right dominance 2/16 5/13
‘Inv’/‘Un’ is the dominant leg 8/10 9/9
Age 23.7 (3.6) 20.5 (3.7)
Height (metres) 1.73 (0.09) 1.73 (0.08)
Weight (kg) 69.2 (11.8) 68.6 (11.2)
BMI 23.0 (2.4) 22.7 (2.0)
No significant group difference was found for any variable (n.s.)
Knee Surg Sports Traumatol Arthrosc
123
Journal : Large 167 Dispatch : 20-9-2013 Pages : 6
Article No. : 2696 hLE hTYPESET
MS Code : KSST-D-13-00605 hCP hDISK
44
Author Proof
UNCORRECTED PROOF
158 derived using a moving 250 ms window. Peak values,
159 identified during three trials of each exercise, were aver-
160 aged and normalized to the maximum signal collected
161 during three maximal voluntary isometric contractions
162 (MVIC), each lasting 5 s. MVIC measures for hamstring
163 muscles were made with the participants in prone, knees
164 flexed to 30°and the foot in a neutral position, using a belt
165 secured over the calcaneus to provide resistance.
166 Participants warmed up for 5 min on a stationary bike
167 before performing the MVIC task, after which they were
168 shown a short video clip of the exercises and subsequently
169 practiced them. During data collection, order of exercise
170 performance was randomized, and standardized instruc-
171 tions given during each of the three trials were recorded for
172 each exercise. The two exercises performed were the
173 Nordic hamstring exercise (NH) and TRX
Ò
hamstring curls
174 (TRX). Both involve simultaneous bilateral hamstring
175 performance and utilize the individual’s body weight and
176 gravity for resistance. However, while the feet and tibiae
177 are constrained for the NH exercise, the lower extremities
178 are relatively free during the TRX performance. The NH
179 exercise was performed by each participant lowering their
180 trunk as slowly as possible, with arms at their side for as
181
long as possible (eccentric knee flexor activity from 95°
182
knee flexion while maintaining hips at close to 0°: Fig. 1).
183
Time during the execution of the NH exercise was recorded
184
for each participant. A metronome was used to standardize
185
the performance of four phases of the TRX exercise; 1. hip
186
extension (concentric) from flexed to neutral hip position;
187
2. knee extension (eccentric) from flexed to 0°; 3. knee
188
flexion (concentric) returning from 0°to flexed knee
189
position; 4. hip flexion (eccentric) from 0°to starting
190
position. Performance time was standardized to 2.5 s, and
191
data from phase 2 (between beats 1 and 2 of the metro-
192
nome) were used for analysis (eccentric hamstring activity;
193
Fig. 2). Variables of interest included peak (normalized)
194
activation levels of the MH and LH EMG signal during the
195
eccentric performance of each of the two exercises for both
196
limbs.
197
Statistical analysis
198
After processing the EMG data, they were analyzed using
199
IBM SPSS Statistics version 20. A mixed model analysis of
200
variance (ANOVA) was used to evaluate each muscle’s
Fig. 1 Performance of the Nordic hamstring exercise
Fig. 2 Performance of the TRX hamstring curl exercise
Knee Surg Sports Traumatol Arthrosc
123
Journal : Large 167 Dispatch : 20-9-2013 Pages : 6
Article No. : 2696 hLE hTYPESET
MS Code : KSST-D-13-00605 hCP hDISK
44
Author Proof
UNCORRECTED PROOF
201 activity; within-subjects factors included limb (involved/
202 uninvolved) and exercise (NH/TRX), between the ACLR
203 and CTRL groups. Post hoc t tests were used where indi-
204 cated, to clarify ANOVA results. The alpha level was set at
205 0.05.
206 Results
207 The groups were matched for gender, height and weight,
208 and no group differences were found for mean age or
209 instances where the players’ dominant (kicking) leg was
210 the ‘involved’ versus ‘uninvolved’ side (Table 1). The
211 mean ±SD time utilized to perform the NH exercise was
212 4.0 ±1.3 and 3.8 ±1.0 s for the ACLR and CTRL
213 groups, respectively (n.s.).
214 While a main effect of limb was found across groups,
215 limbs and exercises for both hamstring muscles
216 (p\0.001), a statistically significant limb by exercise
217 interaction was found for peak activation levels of LH, due
218 to significant interlimb differences during the performance
219 of the TRX exercise compared to more symmetrical acti-
220 vation during the NH (p\0.001; Fig. 3). Post hoc analy-
221 ses revealed significantly lower activation levels of the
222 ‘involved’ limb during the TRX compared to the NH
223 exercise (p\0.001), while the ‘uninvolved’ side con-
224 versely demonstrated slightly (not significant) greater
225 activation levels on average. While not statistically sig-
226 nificant for LH, a three-way interaction was found for the
227 peak activation levels of MH, due to group differences in
228 peak muscle activation between limbs and exercise type
229 (p=0.025). Whereas CTRL group participants consis-
230 tently favoured one limb over the other during the perfor-
231 mance of both exercises, ACLR participants demonstrated
232 dissimilar peak MH activation patterns between limbs
233
during the performance of the NH exercise compared to the
234
TRX (Fig. 4).
235
Discussion
236
The principal findings of the study included significant
237
differences between ACLR and CTRL groups in interlimb
238
activation levels of MH, the muscle from which the graft
239
was harvested, between exercises. Additionally, general
240
exercise-dependent differences in peak hamstring muscle
241
activation levels were identified. Contrary to the hypothesis
242
made, interlimb differences were found in both groups, as
243
participants generally favoured one limb over the other
244
during the exercise performance, albeit to different degrees
245
depending on the exercise, as demonstrated by the inter-
246
action of limb and exercise.
247
The main effect of limb is hard to explain as the
248
involved/uninvolved designation was based on the surgical
249
limb of the ACLR group and no interlimb difference was
250
expected in the CTRL group. As seen in Table 1, this
251
finding is not clearly linked to leg dominance, according to
252
the definition used (favoured kicking leg). The operated
253
knee was on the left side 2/3 of the time, and therefore, the
254
same ratio of right limbs was labelled ‘uninvolved’. Par-
255
ticipants may have had a tendency to favour the right leg,
256
regardless of kicking preference, during the exercises, in
257
particular during the performance of the TRX exercise. The
258
two-way interaction of limb and exercise likely reflects the
259
greater freedom of performance during the TRX exercise
260
compared to the NH exercise. During the NH, the tibiae
261
were constrained in a closed chain performance, and in-
262
terlimb peak activation was generally more symmetrical
263
compared to that found during the performance of the
264
TRX, where disparity was greater. When interpreting these
Fig. 3 Mean (SE) LH peak muscle activation levels during the NH
and TRX exercise performance. Asterisks statistically significant
difference
Fig. 4 Mean (SE) MH peak muscle activation levels during the NH
and TRX exercise performance. Asterisks statistically significant
difference
Knee Surg Sports Traumatol Arthrosc
123
Journal : Large 167 Dispatch : 20-9-2013 Pages : 6
Article No. : 2696 hLE hTYPESET
MS Code : KSST-D-13-00605 hCP hDISK
44
Author Proof
UNCORRECTED PROOF
265 results, one must keep in mind that muscle activation levels
266 measured with EMG do not equate to muscle strength or
267 force output, not measured in this study. Nonetheless, the
268 differences seen in relative activation of bilateral ham-
269 strings between exercises are unequivocal. The results
270 indicate the importance of including unilateral strength-
271 ening of key muscles as part of a comprehensive training
272 program to ensure specificity, just as when obtaining spe-
273 cific strength measures. Additionally, biofeedback may be
274 used to promote symmetrical, muscle-specific activation
275 during the exercises involving bilateral lower extremity
276 performance. This may be particularly important after
277 injuries that have led to muscle atrophy and inhibition.
278 There is some indication, albeit inconsistent, that biceps or
279 semimembranosus may in some cases hypertrophy, in what
280 may be viewed as a compensatory effort to counter semi-
281 tendinosus atrophy after ACLR [11,20,27]. Moreover, a
282 positive association has been found between degree of
283 tendon regeneration of the semitendinosus and knee flexor
284 strength measures [6], reflecting the importance of the
285 muscle’s recovery.
286 The interaction involving group differences in interlimb
287 peak activation levels of the MH between exercises may
288 reflect alterations in firing patterns resulting from surgery.
289 Alterations in activation patterns of individuals that have
290 undergone ACLR have previously been shown with respect
291 to timing (onset) of both MH and LH activation [23].
292 Results of the present study indicate that levels of muscle
293 activation during the performance of functional activities
294 are also affected, which may have implications for knee
295 joint arthrokinematics and function, possibly impacting
296 risk of graft failure or rate of osteoarthritis. The results
297 demonstrate that during the bilateral performance of both
298 exercises, individuals were able to favour one limb over the
299 other and that ACLR participants did so to varied degrees
300 between exercises and, seemingly, not to the same extent
301 between MH versus LH components. Single-limb exercises
302 should therefore possibly target medial versus lateral
303 components specifically by manipulating tibial rotation [7]
304 and knee flexion angle [22].
305 A limitation that may affect the interpretation of differ-
306 ences in the activation levels is the lack of strength mea-
307 sures for the participants of the study. Generally, interlimb
308 differences in muscle strength of up to 10 % may be con-
309 sidered normal, and one of the milestones clinicians look for
310 when determining whether an athlete is ready to return to
311 full participation of their sport is limb symmetry of
312 90–100 % [1,30]. Notably, the mean peak activation levels
313 recorded during both exercises may be considered rather
314 low, and our data for NH performance are much lower than
315 mean values recently reported by Ditroilo et al. [10] for
316 Biceps Femoris. This may, in part, be explained by their
317 normalization methods (isokinetic (eccentric) EMG data vs.
318
isometric), but may also be attributed to differences in
319
visual and verbal directions given to participants, affecting
320
their motivation and effort. These were standardized in this
321
study and would not have affected the interactions seen.
322
Ditroilo et al. did not investigate interlimb differences in
323
EMG activation levels during the NH performance, but this
324
was done by Iga et al., who found no significant difference
325
in a recent but small study [17]. Their outcome measures
326
were integrated EMG values over three 30°ROM windows
327
during the exercise. These were normalized to peak values
328
recorded during the same exercise, which likely explains
329
lack of interlimb difference.
330
In efforts to decrease risk of graft failure, post-operative
331
rehabilitation increasingly focuses on resolving neuro-
332
muscular deficits that often persist after ACLR and stan-
333
dard rehabilitation [14]. The results of the present study
334
suggest that rehabilitation strategies targeting hamstring
335
muscle function should include exercises for unilateral as
336
well as bilateral lower extremity performance to ensure
337
adequate effort from the index limb. Moreover, hamstring
338
exercises may prove more effective if care is taken to
339
effectively activate both MH and LH components. Long-
340
term prospective studies, however, are needed to shed light
341
on any potential that specific rehabilitation strategies tar-
342
geting semitendinosus have to influence tendon and muscle
343
morphology, muscle strength and activation, lower limb
344
kinematics and function after ACLR.
345
Conclusion
346
In the light of the results of the study and considering the
347
surgical procedure, outcomes for individuals undergoing
348
ACLR using a HG autograft from the ipsilateral limb may
349
be improved by including specific training for the MH
350
component as part of a comprehensive rehabilitation pro-
351
gram. Clinicians may find the NH a better choice than TRX
352
hamstring curls for bilateral, eccentric, hamstring
353
strengthening during rehabilitation after ACLR, although
354
the results indicate that single-limb exercises are important
355
to ensure optimal muscle performance.
356
Acknowledgments The authors would like to acknowledge Dr.
357
Thorarinn Sveinsson, Professor at the School of Health Sciences,
358
University of Iceland for his assistance during EMG data processing.
359
References
360
1. Adams D, Logerstedt DS, Hunter-Giordano A, Axe MJ, Snyder-
361
Mackler L (2012) Current concepts for anterior cruciate ligament
362
reconstruction: a criterion-based rehabilitation progression.
363
J Orthop Sports Phys Ther 42(7):601–614
364
2. Ahlen M, Liden M, Bovaller A, Sernert N, Kartus J (2012)
365
Bilateral magnetic resonance imaging and functional assessment
AQ1
Knee Surg Sports Traumatol Arthrosc
123
Journal : Large 167 Dispatch : 20-9-2013 Pages : 6
Article No. : 2696 hLE hTYPESET
MS Code : KSST-D-13-00605 hCP hDISK
44
Author Proof
UNCORRECTED PROOF
366 of the semitendinosus and gracilis tendons a minimum of 6 years
367 after ipsilateral harvest for anterior cruciate ligament recon-
368 struction. Am J Sports Med 40(8):1735–1741
369 3. Armour T, Forwell L, Litchfield R, Kirkley A, Amendola N, Fowler
370 PJ (2004) Isokinetic evaluation of internal/external tibial rotation
371 strength after the use of hamstring tendons for anterior cruciate
372 ligament reconstruction. Am J Sports Med 32(7):1639–1643
373 4. Bencke J, Curtis D, Krogshede C, Jensen LK, Bandholm T, Zebis
374 MK (2013) Biomechanical evaluation of the side-cutting
375 manoeuvre associated with ACL injury in young female handball
376 players. Knee Surg Sports Traumatol Arthrosc 21(8):1876–1881
377 5. Bourke HE, Salmon LJ, Waller A, Patterson V, Pinczewski LA
378 (2012) Survival of the anterior cruciate ligament graft and the
379 contralateral ACL at a minimum of 15 years. Am J Sports Med
380 40(9):1985–1992
381 6. Choi JY, Ha JK, Kim YW, Shim JC, Yang SJ, Kim JG (2012)
382 Relationships among tendon regeneration on MRI, flexor
383 strength, and functional performance after anterior cruciate lig-
384 ament reconstruction with hamstring autograft. Am J Sports Med
385 40(1):152–162
386 7. Czamara A, Szuba L, Krzeminska A, Tomaszewski W, Wilk-
387 Franczuk M (2011) Effect of physiotherapy on the strength of
388 tibial internal rotator muscles in males after anterior cruciate
389 ligament reconstruction (ACLR). Med Science Monit 17(9):
390 CR523–CR531
391 8. Decker LM, Moraiti C, Stergiou N, Georgoulis AD (2011) New
392 insights into anterior cruciate ligament deficiency and recon-
393 struction through the assessment of knee kinematic variability in
394 terms of nonlinear dynamics. Knee Surg Sports Traumatol
395 Arthrosc 19(10):1620–1633
396 9. Delince P, Ghafil D (2012) Anterior cruciate ligament tears:
397 conservative or surgical treatment? A critical review of the lit-
398 erature. Knee Surg Sports Traumatol Arthrosc 20(1):48–61
399 10. Ditroilo M, De Vito G, Delahunt E (2013) Kinematic and elec-
400 tromyographic analysis of the Nordic Hamstring Exercise.
401 J Electromyogr Kinesiol
402 11. Eriksson K, Hamberg P, Jansson E, Larsson H, Shalabi A,
403 Wredmark T (2001) Semitendinosus muscle in anterior cruciate
404 ligament surgery: morphology and function. Arthroscopy 17(8):
405 808–817
406 12. Freedman KB, Glasgow MT, Glasgow SG, Bernstein J (1998)
407 Anterior cruciate ligament injury and reconstruction among uni-
408 versity students. Clin Orthop Relat Res 356:208–212
409 13. Grindem H, Eitzen I, Moksnes H, Snyder-Mackler L, Risberg
410 MA (2012) A pair-matched comparison of return to pivoting
411 sports at 1 year in anterior cruciate ligament-injured patients after
412 a nonoperative versus an operative treatment course. Am J Sports
413 Med 40(11):2509–2516
414 14. Hewett TE, Di Stasi SL, Myer GD (2013) Current concepts for
415 injury prevention in athletes after anterior cruciate ligament
416 reconstruction. Am J Sports Med 41(1):216–224
417 15. Hewett TE, Lindenfeld TN, Riccobene JV, Noyes FR (1999) The
418 effect of neuromuscular training on the incidence of knee injury
419 in female athletes. A prospective study. Am J Sports Med
420 27(6):699–706
421 16. Hoshino Y, Fu FH, Irrgang JJ, Tashman S (2013) Can Joint
422 Contact Dynamics Be Restored by Anterior Cruciate Ligament
423 Reconstruction? Clin Orthop Relat Res
424 17. Iga J, Fruer CS, Deighan M, Croix MD, James DV (2012)
425 ‘Nordic’ hamstrings exercise—engagement characteristics and
426 training responses. Int J Sports Med 33(12):1000–1004
427 18. Li S, Chen Y, Lin Z, Cui W, Zhao J, Su W (2012) A systematic
428 review of randomized controlled clinical trials comparing
429
hamstring autografts versus bone-patellar tendon-bone autografts
430
for the reconstruction of the anterior cruciate ligament. Arch
431
Orthop Trauma Surg 132(9):1287–1297
432
19. Li S, Su W, Zhao J, Xu Y, Bo Z, Ding X, Wei Q (2011) A meta-
433
analysis of hamstring autografts versus bone-patellar tendon-bone
434
autografts for reconstruction of the anterior cruciate ligament.
435
Knee 18(5):287–293
436
20. Macleod TD, Snyder-Mackler L, Axe MJ, Buchanan TS (2013)
437
Early regeneration determines long-term graft site morphology
438
and function after reconstruction of the anterior cruciate ligament
439
with semitendinosus-gracilis autograft: a case series. Int J Sports
440
Phys Ther 8(3):256–268
441
21. Nikolaou VS, Efstathopoulos N, Wredmark T (2007) Hamstring
442
tendons regeneration after ACL reconstruction: an overview.
443
Knee Surg Sports Traumatol Arthrosc 15(2):153–160
444
22. Onishi H, Yagi R, Oyama M, Akasaka K, Ihashi K, Handa Y
445
(2002) EMG-angle relationship of the hamstring muscles during
446
maximum knee flexion. J Electromyogr Kinesiol 12(5):399–406
447
23. Ristanis S, Tsepis E, Giotis D, Stergiou N, Cerulli G, Georgoulis
448
AD (2009) Electromechanical delay of the knee flexor muscles is
449
impaired after harvesting hamstring tendons for anterior cruciate
450
ligament reconstruction. Am J Sports Med 37(11):2179–2186
451
24. Ruiz AL, Kelly M, Nutton RW (2002) Arthroscopic ACL
452
reconstruction: a 5–9 year follow-up. Knee 9(3):197–200
453
25. Scanlan SF, Chaudhari AM, Dyrby CO, Andriacchi TP (2010)
454
Differences in tibial rotation during walking in ACL recon-
455
structed and healthy contralateral knees. J Biomech 43(9):
456
1817–1822
457
26. Segawa H, Omori G, Koga Y, Kameo T, Iida S, Tanaka M (2002)
458
Rotational muscle strength of the limb after anterior cruciate
459
ligament reconstruction using semitendinosus and gracilis tendon.
460
Arthroscopy 18(2):177–182
461
27. Snow BJ, Wilcox JJ, Burks RT, Greis PE (2012) Evaluation of
462
muscle size and fatty infiltration with MRI nine to eleven years
463
following hamstring harvest for ACL reconstruction. J Bone Joint
464
Surg Am 94(14):1274–1282
465
28. Surface Electromyography for the Non-Invasive Assessment of
466
Muscles: Recommendations for sEMG Sensors, Sensor Place-
467
ment and location. www.seniam.org
468
29. Tashiro T, Kurosawa H, Kawakami A, Hikita A, Fukui N (2003)
469
Influence of medial hamstring tendon harvest on knee flexor
470
strength after anterior cruciate ligament reconstruction. A
471
detailed evaluation with comparison of single- and double-tendon
472
harvest. Am J Sports Med 31(4):522–529
473
30. Thomee R, Kaplan Y, Kvist J, Myklebust G, Risberg MA,
474
Theisen D, Tsepis E, Werner S, Wondrasch B, Witvrouw E
475
(2011) Muscle strength and hop performance criteria prior to
476
return to sports after ACL reconstruction. Knee Surg Sports
477
Traumatol Arthrosc 19(11):1798–1805
478
31. Wright RW, Gill CS, Chen L, Brophy RH, Matava MJ, Smith
479
MV, Mall NA (2012) Outcome of revision anterior cruciate lig-
480
ament reconstruction: a systematic review. J Bone Joint Surg Am
481
94(6):531–536
482
32. Wright RW, Magnussen RA, Dunn WR, Spindler KP (2011)
483
Ipsilateral graft and contralateral ACL rupture at five years or
484
more following ACL reconstruction: a systematic review. J Bone
485
Joint Surg Am 93(12):1159–1165
486
33. Xergia SA, McClelland JA, Kvist J, Vasiliadis HS, Georgoulis
487
AD (2011) The influence of graft choice on isokinetic muscle
488
strength 4–24 months after anterior cruciate ligament recon-
489
struction. Knee Surg Sports Traumatol Arthrosc 19(5):768–780
AQ2
Knee Surg Sports Traumatol Arthrosc
123
Journal : Large 167 Dispatch : 20-9-2013 Pages : 6
Article No. : 2696 hLE hTYPESET
MS Code : KSST-D-13-00605 hCP hDISK
44
Author Proof
Journal : 167
Article : 2696 123
the language of science
Author Query Form
Please ensure you fill out your response to the queries raised below and return this form along
with your corrections
Dear Author
During the process of typesetting your article, the following queries have arisen. Please check your typeset proof carefully
against the queries listed below and mark the necessary changes either directly on the proof/online grid or in the ‘Author’s
response’ area provided below
Query Details Required Author’s Response
AQ1 Please check and confirm whether the inserted ’university name’ in the acknowledgment section is
correct.
AQ2 Please provide volume id and page range for references [10] and [16].
Author Proof