The Veterinary Journal 196 (2013) 345350

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The Veterinary Journal

journal homepage: www.elsevier.com/locate/tvjl

Abnormal reex activation of hamstring muscles in dogs with cranial cruciate

ligament rupture
Graham M. Hayes a, Nicolas Granger b, Sorrel J. Langley-Hobbs d, Nick D. Jeffery c,
a
Woodcroft Veterinary Group, Queens Road, Cheadle Hulme, Cheshire SK8 5UL, UK
b
School of Veterinary Sciences, University of Bristol, Langford House, Langford, North Somerset BS40 5DU, UK
c
Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Iowa State University, Ames, IA 50011, USA
d
Department of Veterinary Medicine, University of Cambridge, Madingleym Road, Cambridge CB3 0ES, UK

a r t i c l e i n f o a b s t r a c t

Article history: The mechanisms underlying cranial cruciate ligament rupture (CCLR) in dogs are poorly understood. In
Accepted 19 October 2012 this study hamstring muscle reexes in response to cranial tibial translation were analysed to determine
whether these active stabilisers of the stie joint are differently activated in dogs with CCLR compared to
control dogs. In a prospective clinical study reex muscle activity from the lateral and medial hamstring
Keywords: muscles (biceps femoris and semimembranosus) was recorded using surface electrodes in control dogs
Cranial cruciate ligament (n = 21) and dogs with CCLR (n = 22). These electromyographic recordings were analysed using an algo-
Electromyography
rithm previously validated in humans.
Hamstring
Stie stabilisation
The hamstring reex was reliably and reproducibly recorded in normal dogs. Both a short latency
Tibial translation response (SLR, 17.6 2.1 ms) and a medium latency response (MLR, 37.7 2.7 ms) could be identied.
Dog In dogs with unilateral CCLR, the SLR and MLR were not signicantly different between the affected
and the unaffected limbs, but the MLR latency of both affected and unaffected limbs in CCLR dogs were
signicantly prolonged compared to controls. In conclusion, the hamstring reex can be recorded in dogs
and the MLR is prolonged in dogs with CCLR. Since both affected and unaffected limbs exhibit prolonged
MLR, it is possible that abnormal hamstring reex activation is a mechanism by which progressive CCL
damage may occur. The methodology allows for further investigation of the relationship between neuro-
muscular imbalance and CCLR or limitations in functional recovery following surgical intervention.
2012 Elsevier Ltd. All rights reserved.

Introduction through mechanoreceptors in the CCL, joint capsule and periarticu-

Cranial cruciate ligament rupture (CCLR) is the leading cause of
stie lameness in dogs and certain breeds have an established
predisposition (Whitehair et al., 1993). However, the pathogenesis
of canine CCLR remains incompletely understood (Cook, 2010;
Griffon, 2010; Comerford et al., 2011).
Stie joint stability depends both on passive stabilisers (princi-
pally the cruciate ligaments, menisci and collateral ligaments)
and active (or dynamic) stabilisers (principally the quadriceps,
hamstrings and gastrocnemius muscles; Fig. 1). Precise coordina-
tion of the active stabilisers, mediated by the nervous system, is
essential for efcient joint function, particularly during strenuous
activity. The hamstring reex plays a crucial role in limiting cranial
tibial translation, overextension and internal rotation, hence pro-
tecting the cranial cruciate ligament (CCL) from damage during
movements of the tibia relative to the femur (Shultz et al., 2004;
Bonslls et al., 2008; Friemert et al., 2010). The reex is mediated
Corresponding author. Tel.: +1 515 291 1396.
E-mail address: njeffery@iastate.edu (N.D. Jeffery).
lar muscle bellies (Friemert et al., 2005b) and modulates hamstring
muscle tone in response to changes in load on the CCL. This reex
response can be recorded by electromyography (EMG) after initia-
tion through a suitable stimulus. Two components in the response
of the hamstring reex are recognised in humans, termed short and
medium latency responses (SLR and MLR, respectively); normal ref-
erence ranges and protocols for interpreting the EMG traces have
been developed (Friemert et al., 2005a) and the test methodology
is reproducible and reliable (Schoene et al., 2009).
In humans, anterior cruciate ligament (ACL) rupture is usually
an acute sporting injury and most common when fatigue alters
the neuromuscular reexes that coordinate hamstring contractil-
ity, changing the pattern of muscle activation around the stie
(Melnyk and Gollhofer, 2007; Shimokochi and Shultz, 2008). There
is evidence that improving hamstring muscle strength and recruit-
ment, or training which improves proprioceptive control of the
knee, can signicantly reduce the risk of ACL rupture in specic
groups of athletes (Alentorn-Geli et al., 2009; Gruber et al., 2006).
A proportion of humans with ACL rupture can function well
despite knee joint instability and this is thought to be because

1090-0233/$ - see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.tvjl.2012.10.028
346 G.M. Hayes et al. / The Veterinary Journal 196 (2013) 345350
Fig. 1. Dynamic (active) stabilisers of the canine stie. The quadriceps, gastrocne-
mius and the hamstring muscles are represented on this schematic.
the active stabilisers can compensate through well-developed sen-
sorimotor reexes for the reduced passive stability (Melnyk et al.,
2007; Beard et al., 1994). Latency of the hamstring reex is a
means to estimate dynamic instability in the knees of humans with
ruptured ACL (Beard et al., 1993).
In dogs, true traumatic CCLR is relatively unusual. Instead, be-
cause of the observed chronic osteoarthritic changes at the time
of CCLR and the spectrum of partial CCLR, the vast majority are
thought to result from progressive degeneration and tearing of
the ligament prior to complete failure (Griffon, 2010). The aims
of this study were: (1) to develop a means of recording the ham-
string reex in standing, conscious dogs; (2) to determine the la-
tency of this reex in normal dogs, and (3) to determine if this
reex is altered in dogs that present with naturally occurring CCLR.
Because delayed hamstring reexes could cause chronic overload-
ing of the CCL and predispose to CCLR, we hypothesised that the
hamstring reex would have a longer latency in dogs with CCLR.
Materials and methods
Electromyographic (EMG) recording of the hamstring reex
A novel apparatus for inducing a reproducible cranial tibial translation in stand-
ing dogs was designed and built (Fig. 2). This consisted of a switch-operated pneu-
matic cylinder mounted on a fully adjustable stand and driven by a compressed air
supply (700 kPa) applying a force of 105 N to the piston. The stand could be posi-
tioned caudal to the dogs stie and adjusted to a position 3 cm below the palpable
landmarks of the tibial plateau and 2 cm caudal to the crus.
A microswitch, activated when the gas piston struck the crus, triggered a two-
channel EMG recording. The EMG was recorded from both the lateral and medial
hamstring muscles (biceps femoris and semimembranosus) using atraumatic skin
clips placed in a belly/tendon montage, impedance was kept below 13 kX for all
recordings. A ground clip was placed over the cranial part of the distal sartorius
muscle. Alcohol was applied to the skin and clips to improve surface conductivity,
but neither hair removal, nor further skin preparation was performed. Recording
was performed in an electromagnetically shielded room by a single operator
(GMH) on conscious, standing dogs, minimally restrained on a leash by an assistant
or the dogs owner.
A consistent protocol was used to obtain ten recordings from each pelvic limb
whilst the paw was bearing weight and with the stie at a normal standing angle.
All EMG traces, recorded with sweep duration of 10 ms/division and amplitude of
500 mV/division, were saved for analysis at a later date. EMG traces were analysed
and interrogated using the manufacturers software (VikingQuest V.9.00a; Viasys
Healthcare/Care Fusion) using an algorithm validated for use in humans (Friemert
et al., 2005a) with minor adaptation. Briey, three decision points were used to dif-
ferentiate short and medium latency hamstring responses: (1) recordings derived
from the lateral hamstring muscles were used in preference; (2) the SLR was dened
as the rst steep rise of more than 100 lV occurring after12 ms but before 30 ms,
and (3) the MLR was dened as the rst steep rise of more than 100 lV occurring
with a latency of more than 30 ms and an amplitude comparable to the SLR.
EMG traces were batch-analysed by two blinded investigators (GMH, NG) and a
consensus agreement reached regarding the reex latencies (SLR and MLR). Another
investigator (NDJ) blinded to patient signalment and CCL status adjudicated if con-
sensus could not be reached. Although EMG traces were recorded from both medial
and lateral hamstrings, the lateral hamstring was used in preference to the medial
hamstring for measuring latency, in line with previous studies in human patients.
Thus, for each limb, 510 traces were analysed. For both the SLR and MLR, the mean
of those 510 recordings was used.
Dogs
This study was approved by the Departmental Ethics Committee before testing
privately-owned control dogs and clinical cases. Informed owner consent was
obtained in all cases and testing was abandoned if a dogs temperament or move-
ment made the test difcult to complete.
Dogs owned by staff members were prospectively recruited to validate the test
protocol and obtain reference ranges. Inclusion criteria were: mass >15 kg; age
28 years; absence of neurologic or pelvic limb orthopaedic disease based on ques-
tioning of the owners (veterinary health professionals) as well as physical and
neurological examination and observation of gait. Further recorded information
included breed, sex, and left femur length (estimated by measuring from the tibial
crest to the greater trochanter), which was used as a surrogate measure of nerve
length.
Dogs presenting to the orthopaedic service for assessment and surgical manage-
ment of CCLR were prospectively recruited between October 2010 and May 2011.
Inclusion criteria were: mass >15 kg; weight-bearing lameness of 63 months dura-
tion conrmed as caused by CCLR at subsequent surgical intervention; no previous
stie surgery on the affected side; and a suitable temperament. Both pelvic limbs of
CCLR dogs underwent routine physical and radiological examination to establish
the diagnosis.
Statistical analysis
The mean of all SLR and MLR values for individual limbs were obtained before
further analysis (GraphPad Prism 5.0; GraphPad Software). For each group of dogs,
SLR and MLR values were summarised as mean (standard deviation or SD and 95%
condence interval or CI) and the group value distributions tested for deviations
from normality using the DAgostinoPearson test. In order to determine whether
standardisation for reex arc length using a regression equation was required, a
graph of left femoral length against reex latency was plotted and analysed using
linear regression.
For unilateral CCLR dogs, SLR and MLR values from the affected (CCLR) limb and
unaffected limb were compared using paired t tests. Both SLR and MLR values from
the affected limb and the unaffected limb were compared with the values from con-
trol dogs using one-way ANOVA with Dunnetts post hoc tests. For all tests signif-
icance was established at P 6 0.05.
Results
Control dogs
Twenty-one dogs representing a variety of breeds and sizes
were recruited: Labrador retrievers (6), Springer spaniels (4), sight
 G.M. Hayes et al. / The Veterinary Journal 196 (2013) 345350 347

Fig. 2. (A) Photograph of a sight hound control dog undergoing hamstring reex testing. (B) Photograph showing placement of the surface electromyographic electrodes over
the biceps femoris and semimembranosus muscle bellies.

Fig. 3. Typical electromyographic traces from (A) control dog (8 year-old mixed breed) and (B) the affected limb of a dog with cranial cruciate ligament rupture (2.5 year old
American Bulldog). The upper traces in (A) and (B) are from the lateral hamstring and the lower traces from the medial hamstring. Plain arrows indicate the start of the short
latency (SLR) and dashed arrows indicate the start of the medium latency (MLR) response complexes respectively. Note the prolonged MLR latencies in trace (B).

hounds of various types (4), Golden retrievers (2), Pointers (2),
medium-sized crossbreed dogs (2), and a Border Collie (1). Mean
(SD) age was 5.0 (2.2) years and mean (SD) bodyweight was
24.6 (7.5) kg.
Traces were recorded from 41 limbs and 350 EMG traces were
readable (a mean of 8.5 traces per limb). One dog became restless
and the test could not be completed on the second limb. In all 350
traces both the SLR and MLR could be identied and latencies mea-
sured using the modied algorithm (Fig. 3). Summary SLR and MLR
latencies were 17.6 ms (95% CI, 16.918.2 ms) and 37.7 ms (95% CI,
36.938.5 ms), respectively (Table 1).
All latencies exhibited minimal variability between individual
recordings or between individual dogs. A graph of left femoral
length against reex latency produced lines of best t with slopes
of 0.05 for the SLR (95% CI, 0.35 to 0.26) and 0.11 for the MLR
(95% CI, 0.30 to 0.52). These slopes were not signicantly differ-
ent from zero, implying no signicant relationship between limb
length and reex latency in this population of dogs, and meaning
that no correction was required to compare latency between differ-
ently sized dogs within this limited size range (Fig. 4).
Dogs with clinical cranial cruciate ligament rupture
Twenty-two dogs representing a variety of breeds met the
inclusion criteria. These dogs comprised: Labrador retrievers (6),
Springer spaniels (5), Golden retrievers (2), Collies (2), American
Bulldogs (2), Staffordshire bull terriers (2), Newfoundland (1), Bull-
mastiff (1) and Rhodesian Ridgeback mix (1). Mean (SD) age was
5.0 (2.1) years and mean (SD) bodyweight was 34.3 (18.7) kg.
Hamstring reexes were recorded in both pelvic limbs. Sixteen
dogs had unilateral CCLR (i.e. clinically and radiographically nor-
mal contralateral stie), 4 dogs had bilateral CCLR at presentation
(unilateral or bilateral lameness with bilateral signs suggestive of
CCLR on radiographs) and 2 dogs presented for unilateral CCLR,
but had had previous surgery on the contralateral limb. Two dogs
presenting with unilateral CCLR had a history and radiographic
348 G.M. Hayes et al. / The Veterinary Journal 196 (2013) 345350

Table 1
Reex latencies recorded from 21 control dogs.

Left pelvic limb Right pelvic Combined data for

limb both limbs
SLR latency 17.3 2.0 17.9 2.1 17.6 2.1
ms SD (16.418.2) (17.018.9) (16.918.2)
(95% CI)
MLR latency 37.9 2.7 37.5 2.7 37.7 2.7
ms SD (36.739.2) (36.238.7) (36.938.5)
(95% CI)

MLR, medium latency response; SD, standard deviation; SLR, short latency
response; CI, condence interval.

Fig. 6. Paired line plot to show medium latency response (MLR) latency in affected
and unaffected limbs for individual dogs with unilateral cranial cruciate ligament
rupture (CCLR).

Table 2
Reex latencies recorded from 16 dogs with unilateral cranial cruciate ligament
rupture.

Affected limb Unaffected limb P-value

SLR latency 17.8 2.5 17.5 2.3 0.96
ms SD (16.419.2) (16.118.8)
(95% CI)
MLR latency 43.9 5.9 42.7 8.1 0.43
ms SD (40.747.2) (38.447.0)
Fig. 4. Scatter plot to show left femoral length against reex latency for 21 control (95% CI)
dogs. The lines of best t have slopes of 0.05 for the short latency response (SLR)
MLR, medium latency response; SD, standard deviation; SLR, short latency
(95% CI, 0.35 to 0.26) and 0.11 for the medium latency response (MLR) (95% CI,
response; CI, condence interval.
0.30 to 0.52). These slopes were not signicantly different from zero (SLR: F = 0.12,
P = 0.74; MLR: F = 0.31, P = 0.58).
pleted because of restless temperament (n = 1) or an inability to
attach the EMG clips onto thickened skin (n = 1).

Comparisons

Using one-way ANOVA, comparisons of hamstring reex laten-

Fig. 5. Box plot to show medium latency response (MLR) latency for dogs (n = 16)
with unilateral cranial cruciate ligament rupture (affected and unaffected limbs)
and control dogs (n = 41). Mean and 95% CI indicated (signicantly different from
controls, P < 0.05).
signs consistent with acute traumatic CCLR, whilst the remainder
were consistent with degenerative CCLR.
Traces were recorded from both pelvic limbs; one limb was ex-
cluded due to insufcient readable traces. In total, 339 EMG traces
were readable (a mean of 7.8 traces per limb). Testing was at-
tempted on an additional two CCLR dogs but could not be com-
cies between sties of control dogs (n = 21) and the affected and
unaffected sties of unilateral CCLR dogs (n = 16) revealed a highly
signicant effect of group on MLR latency (F = 11.2, P < 0.0001).
Dunnetts post hoc comparisons revealed a signicant difference
(P < 0.05) in MLR latency between controls (MLR latency,
37.7 ms; 95% CI, 36.938.5 ms) and each of the other groups: af-
fected (CCLR) stie group (MLR latency, 43.9 ms; 95% CI, 40.7
47.2 ms), unaffected (CCLR) stie group (MLR latency, 42.7 ms,
95% CI, 38.447.0 ms) (Fig. 5). Similar comparisons of SLR latencies
revealed no signicant differences amongst groups (F = 0.09,
P = 0.92).
Plotting the data for individual dogs showed that in the major-
ity of CCLR dogs, the unaffected limb had a shorter MLR latency
than that of the affected limb, but in four cases the unaffected limb
had a longer MLR latency (Fig. 6). The two dogs with traumatic
CCLR had MLR latencies in both limbs that were within the 95%
CI of that of controls. Due to the small number of cases of traumatic
CCLR compared to degenerative CCLR, these groups were not ana-
lysed separately.
Within-dog comparisons of hamstring reex latencies using
paired t tests found no signicant differences in either MLR or
SLR between sties in unilateral CCLR dogs (t = 0.82, P = 0.43 and
t = 0.05, P = 0.96, respectively) (Table 2). Results for the bilateral
CCLR dogs were not analysed further as a signicant abnormality
had been demonstrated in both sties of the unilateral CCLR dogs
and the sample size of bilateral CCLR dogs was small.
 G.M. Hayes et al. / The Veterinary Journal 196 (2013) 345350
Discussion
This investigation demonstrates that the hamstring reex can
be reliably evoked and recorded in conscious, standing dogs and
that part of this compound reex is altered in dogs suffering from
CCLR. The canine hamstring reex has similar morphology and
identiable components to the human counterpart and, in both
species, the MLR component alone is altered in patients with CCLR.
The increase in MLR latency is consistent with a change in the
pattern of muscle activation around the stie and in the ability
of the active stabilisers to maintain joint stability during weight-
bearing. There are two major alternative explanations for this nd-
ing: (1) CCL rupture causes the increase in latency through injury
to sensory mechanisms in and around the stie joint (i.e. it is a re-
sult of CCLR), or (2) an increased MLR latency is a sign of altered
coordination of active joint stabilizers that then predisposes to
CCL rupture (i.e. it is a cause of CCLR). Pertinently, in this study
an increased MLR latency was also found in the unaffected limbs
of the unilateral CCLR dogs, supporting the notion that abnormal
MLR might be a possible causal factor for CCLR in dogs. Interest-
ingly, in humans with ACL rupture the contralateral limb shows
no abnormality in MLR latency (Melnyk et al., 2007), which is con-
sistent with the known different mechanisms of cruciate ligament
injury in the two species (predominantly traumatic in humans;
predominantly slow degeneration in dogs).
It is conceivable that increased MLR latency might be a breed-
related trait, which could have implications regarding our current
ndings. In other words, a systematic difference in type of dogs in-
cluded in each group might provide an alternative explanation for
the results. However, this appears unlikely since many types and
breeds of dog were included in our control population, including
some of which are known to be susceptible to CCLR. In addition,
such an explanation would not detract from the overall nding
that dogs with CCLR have increased MLR latency compared with
a cohort of control unaffected dogs. A second aspect to possible
breed-related variability in MLR is that it provides a novel mecha-
nism by which specic breeds, or specic individuals within cer-
tain breeds, might be more susceptible to CCLR.
The concept of neuromuscular imbalance as a cause of CCLR in
dogs provides an attractive explanation for many of the enigmas of
canine CCLR, including the breed predispositions (as discussed
above). Chronically impaired dynamic stability of the canine stie
could explain the insidious onset of CCLR in many dogs, resulting
from repetitive microtrauma and chronic progressive tearing of
the CCL leading to secondary synovitis. Defective dynamic stabili-
sation of the stie may also help to explain the rapid improvement
evident in some dogs following proximal tibial osteotomy proce-
dures, which improve passive stability and thereby reduce depen-
dence upon concomitant active stabilisation of the joint (Kim et al.,
2008).
There is some other recent evidence in support of a neuromus-
cular imbalance in dogs affected by CCLR. Kinematic studies on
dogs with experimental CCLR demonstrate cyclical patterns of cra-
nial tibial subluxation during the early stance phase followed by
reduction during the swing phase of gait (Tashman et al., 2004)
and these results have recently been conrmed by studies in natu-
rally occurring CCLR (Ragetly et al., 2010). These observations sug-
gest that hamstring muscles are able to reduce tibial subluxation
during the swing phase, but the contraction of the quadriceps
and gastrocnemius muscles in response to the ground reaction
force overwhelms the hamstring muscles and results in repeated
cranial tibial subluxation during early stance phase. A recent study
evaluating the morphometric characteristics of the pelvic limb
musculature of Labrador retrievers with and without CCLR demon-
strated marked atrophy of the quadriceps but preservation of the
hamstrings in dogs with CCLR (Mostafa et al., 2010).
349
It is likely that some neuromuscular adaptation is essential fol-
lowing CCLR. The speed and completeness of this neuromuscular
adaptation may in part determine the functional outcome follow-
ing conservative or surgical treatment. A proportion of humans
(termed copers) with an ACL-decient knee can continue to func-
tion well due to adequate dynamic stability despite mechanical
instability (Melnyk et al., 2007). For the majority, however, rehabil-
itation after ACL injury is prolonged in spite of restoration of
mechanical stability by surgery. Time-related changes in motor
control have been observed in humans after ACL injury (Bryant
et al., 2008) and rehabilitation, which facilitates neuromuscular
adaptation, may enhance recovery from ACL injury (Madhavan
and Shields, 2011).
Despite this being a prospective study, several limitations are
recognised. The test procedure was designed to apply a reproduc-
ible and consistent cranial tibial translation force to trigger the
hamstring response. The xed amount of power applied to the
hydraulic cylinder means a relatively greater force was applied to
smaller dogs than larger dogs which may have caused different
cranial tibial translations. Unfortunately, there is no simple meth-
od of accurately quantifying the cranial tibial translation which we
achieved, although the limited weight range of dogs included in
the study will limit the effect of this variability. In compliant hu-
man subjects, potentiometers are applied to the limb, and limb po-
sition is xed relative to the instruments. This could not be
performed safely in unacclimatised pet dogs.
Although the control dogs did not undergo stie radiography,
all reasonable precautions were taken to ensure that they were free
of cruciate disease, and a previous study has demonstrated that pa-
tella tendon palpation is as sensitive and specic for detecting cru-
ciate disease as radiography (Carobbi and Ness, 2009). In addition,
inadvertent inclusion of affected dogs in the control group would
tend to militate against detection of a difference between controls
and CCLR dogs.
A multitude of further investigations are possible now that this
methodology has been developed and reference ranges estab-
lished. Of particular interest would be following up unilateral CCLR
dogs to determine which dogs develop clinical signs of contralat-
eral CCLR. With further investigation, repeat recording of the ham-
string reex may be a useful outcome measure after CCLR surgery
and it may also be possible to perform simultaneous surface EMG
of multiple muscles to determine the complex relationship be-
tween the hamstring, the gastrocnemius and the quadriceps
muscles.
Conclusions
Short- and medium-latency hamstring reexes can readily be
recorded from standing conscious dogs in response to cranial
translation of the tibia relative to the femur. Medium latency re-
exes are abnormally prolonged in both pelvic limbs of dogs that
have cranial cruciate ligament rupture, suggesting the possibility
that abnormal neuromuscular control could play a causal role in
progressive cruciate ligament damage.
Conict of interest statement
None of the authors has a nancial or personal relationship with
other people or organisations that could inappropriately inuence
or bias the content of this study.
Acknowledgement
The Viking Quest electrodiagnostics equipment was purchased
with a grant from the RCVS Trust.
350 G.M. Hayes et al. / The Veterinary Journal 196 (2013) 345350

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