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Biceps Tenotomy in The Presence of A Supraspinatus Tear Alters The Adjacent Intact Tendons and Glenoid Cartilage
Biceps Tenotomy in The Presence of A Supraspinatus Tear Alters The Adjacent Intact Tendons and Glenoid Cartilage
Journal of Biomechanics
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a r t i c l e i n f o a b s t r a c t
Article history: A rotator cuff tear is a common injury in athletes and workers who repeatedly perform overhead move-
Accepted 20 August 2017 ments, and it is not uncommon for this demographic to return to activity shortly after treatment. A biceps
tenotomy is often performed in the presence of a rotator cuff tear to help reduce pain and improve joint
function. However, the effect of this procedure on the surrounding tissues in the glenohumeral joint is
Keywords: unknown. Therefore, the purpose of this study was to investigate the effect of a biceps tenotomy in
Rotator cuff the presence of a supraspinatus rotator cuff tear followed by overuse activity on ambulatory function
Animal model
and mechanical and histologic properties of the remaining rotator cuff tendons and glenoid cartilage.
Overuse injury
46 rats underwent 4 weeks of overuse activity to create a tendinopathic condition, then were randomized
into two groups: unilateral detachment of the supraspinatus tendon or detachment of the supraspinatus
and long head of the biceps tendons. Ambulatory measurements were performed throughout the 8 weeks
prior to euthanasia, followed by analysis of the properties of the remaining intact tendons and glenoid
cartilage. Results demonstrate that shoulder function was not effected in the biceps tenotomy group.
However, the intact tendons and glenoid cartilage showed altered mechanical and histologic properties.
This study provides evidence from an animal model that does not support the use of tenotomy in the
presence of a supraspinatus tendon rotator cuff tear, and provides a framework for physicians to better
prescribe long-term treatment strategies for patients.
Ó 2017 Elsevier Ltd. All rights reserved.
1. Introduction If a rotator cuff tear is present, this can cause force imbalances,
which have negative implications for the surrounding tissues if left
The shoulder is the most mobile joint in the body, and thus untreated (Peltz et al., 2009; Perry et al., 2009; Reuther et al.,
relies on dynamic restraint from the rotator cuff, which includes 2013b). While past studies have determined the mechanical mech-
muscles and tendons from the supraspinatus, infraspinatus, upper anisms by which rotator cuff tears lead to further joint damage
and lower subscapularis, and teres minor (Fig. 1) (Anderson et al., (Reuther et al., 2013a,b, 2014; Thomas et al., 2014), the implica-
2012). Injuries involving the rotator cuff are common, and can lead tions of associated surgical procedures, such as full detachment
to pain and joint dysfunction. These injuries are often sports- of the long head of the biceps (LHB) via tenotomy, have yet to be
related and believed to be due to overuse, indicated by increases fully examined.
in cellularity, changes in cell morphology, decreased collagen fiber The role of the LHB tendon as a shoulder stabilizer is debated;
alignment, and decreased tendon mechanics (Soslowsky et al., some believe it provides minimal stability (Levy et al., 2001;
2000). These overuse injuries are common in athletes and workers Yamaguchi et al., 1997) while others believe it assists the
who repeatedly perform overhead movements, such as swimming supraspinatus tendon in acting as a humeral head depressor
or throwing (Andrews et al., 1985; Mazoué and Andrews, 2006; (Alexander et al., 2013; Kido et al., 2000, 1998). Clinically, it has
Namdari et al., 2011). It is not uncommon for these groups of previously been reported that the LHB will develop pain and struc-
patients to return to their sport or activity shortly after treatment. tural damage in the presence of a rotator cuff tear (Biz et al., 2012;
Boileau et al., 2004; Mazzocca et al., 2013). Studies using a rat rota-
⇑ Corresponding author at: McKay Orthopaedic Research Laboratory, University tor cuff model have demonstrated structural damage in the LHB in
of Pennsylvania, 424 Stemmler Hall, 3450 Hamilton Walk, Philadelphia, PA 19104- the presence of an isolated supraspinatus (supraspinatus-only, SO)
6081, USA. tendon tear (Peltz et al., 2009, 2010, 2011; Reuther et al., 2013b).
E-mail address: soslowsk@upenn.edu (L.J. Soslowsky).
http://dx.doi.org/10.1016/j.jbiomech.2017.08.021
0021-9290/Ó 2017 Elsevier Ltd. All rights reserved.
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152 Z.M. Beach et al. / Journal of Biomechanics 63 (2017) 151–157
Fig. 1. Anterior and posterior views of the rotator cuff. The four muscles and tendons that make up the rotator cuff and provide dynamic support are the supraspinatus (SS),
infraspinatus (IS), subscapularis (Subscap), and teres minor (TM). The LHB tendon (arrowhead) also provides support to the humeral head by preventing anterior translation.
Reprinted from Sports Medicine Clinics, Vol 31, Anderson MW, Brennan C, Mittal A, Imaging Evaluation of the Rotator Cuff, 605-631, Copyright 2012, with permission from
Elsevier.
Surgeons commonly recommend arthroscopic tenotomy in lowed by 4 weeks of overuse activity (downhill (10°) treadmill
response to chronic symptoms in the LHB associated with rotator running at 17 m/min for 1 h/day, 5 days/week) (Soslowsky et al.,
cuff tears. While LHB tenotomy in the presence of a rotator cuff 2000), to generate a clinically relevant tendinopathic condition in
tear has been shown to reduce pain and improve function (Kim the supraspinatus tendon. Next, the animals were randomized into
et al., 2012; Szabo et al., 2008; Zhang et al., 2013), the effects of this two groups: unilateral supraspinatus-only (SO) tendon detach-
surgery on the surrounding joint structures, including the intact ment or detachment of the supraspinatus and LHB tendons (SB),
rotator cuff tendons and glenoid cartilage, are relatively unknown. as previously described (Peltz et al., 2009; Thomopoulos et al.,
Past studies using our rotator cuff rat model have shown that 2002). This study was approved by the Institutional Animal Care
different variants of rotator cuff tendon injury and overuse results and Use Committee. After surgery, animals were allowed 1 week
in varying amounts of damage to the glenohumeral joint (Peltz of cage activity before gradually returning to the overuse training
et al., 2009, 2010, 2011; Reuther et al., 2012, 2013a,b, 2014; over 2 weeks. After treadmill training, all animals underwent an
Thomas et al., 2014). For example, concurrent detachment of the additional 5 weeks of overuse activity (Reuther et al., 2013a,b,
supraspinatus and infraspinatus (SI) tendons resulted in decreased 2014; Thomas et al., 2014). The treadmill training protocol, includ-
glenoid cartilage thickness after 4 weeks of cage activity (Reuther ing overuse, was constant across both groups. Sacrifice of both
et al., 2012). When overuse was applied to this same system, it groups occurred 8 weeks after surgical detachment of the tendons.
resulted in decreased glenoid cartilage elastic modulus, thinning During dissection, animals were checked to confirm that the ten-
of the glenoid cartilage, and alterations in shoulder function when dons detached at the time of surgery remained detached during
compared to uninjured (Reuther et al., 2013a). This concurrent SI training. The supraspinatus tendon always fills in with some scar
tear also showed decreased properties in the surrounding joint tissue, which is normal for animal studies. This tissue is dramati-
when compared to an SO tear in the presence of overuse cally mechanically inferior to native tendon and it is unlikely that
(Reuther et al., 2014). Additionally, an LHB tenotomy in the pres- load bearing capacity is achieved. The LHB tendon is known to be a
ence of an SI rotator cuff tear resulted in improvements in sub- highly tensioned tendon (Narvani et al., 2013) and retracted into
scapularis tendon properties, but minimal changes in shoulder the bicipital groove after surgery. For histology, tissues were
function (Thomas et al., 2014). However, the effect of an LHB teno- immediately fixed in formalin. The remaining animals were stored
tomy, in the presence of an SO tear and overuse activity, on shoul- intact at 20 °C before mechanical testing. All methods utilized in
der function, intact rotator cuff properties, and cartilage properties the following sub-sections have been reported previously as
is currently unknown. referenced.
Therefore, the purpose of this study was to investigate the effect
of full detachment of the LHB via tenotomy in the presence of an
SO rotator cuff tear followed by overuse activity on ambulatory 2.1. Quantitative ambulatory assessment
function and mechanical and histologic properties of the intact
rotator cuff tendons and glenoid cartilage. We hypothesized that Forelimb gait and ground reaction forces were quantified using
an LHB tenotomy in the presence of an SO tear followed by overuse an instrumented walkway (Sarver et al., 2010). These parameters
would result in negative changes in the surrounding tissues, have been shown to be decreased in the presence of an injury
demonstrated by a decrease in joint function and mechanics and (Sarver et al., 2010), and assist with the clinical translation of
increased cellular activity in the intact tendons and glenoid tissue-level animal studies where invasive methods of testing are
cartilage. not an option. Data was collected 1 day prior to tendon detach-
ment to obtain baseline values, then collected at 3, 7, 14, 28, 42
and 56 days post-surgery. Ground reaction force data, including
2. Methods medial/lateral, braking, propulsion, and vertical forces, were col-
lected for each walk via force/torque cells that were mounted to
46 adult male Sprague-Dawley rats (400–450 g) were used in two 70 mm long acrylic force plates. Cameras beneath the walk-
this study. To acclimate the animals to their treadmill training way were able to collect both ventral and sagittal (left and right)
environment, they were subjected to a 2-week training period, fol- views of the animal due to mirrors placed along the sides of the
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Z.M. Beach et al. / Journal of Biomechanics 63 (2017) 151–157 153
walkway (Fig. 2). Paw print analysis allowed for measurement of cartilage thickness maps. Each map was divided into six regions
several temporal and spatial parameters, including stride length, (center (C), posterior-superior (PS), posterior-inferior (PI),
step width, and speed. At each time, at least two walks were anterior-superior (AS), anterior-inferior (AI), and superior (S))
recorded per animal, as well as body weight. For each animal, and a mean thickness was computed for each region. After ultra-
parameters were averaged across walks and normalized to body sound scanning, specimens were wrapped in soft tissue and frozen
weight for each day. ( 20 °C) until mechanical testing.
For cartilage mechanical testing (Reuther et al., 2012), each sca-
2.2. Tendon mechanical testing pula was thawed and immersed in PBS containing a protease inhi-
bitor cocktail at room temperature. Cartilage mechanical testing
The animals were thawed, then the scapula and humerus were was performed using a 0.5 mm-diameter, nonporous, spherical
dissected with the infraspinatus and subscapularis tendons intact. indenter. Briefly, a preload (0.005 N) was followed by eight step-
Tendon testing was performed as previously described (Peltz et al., wise stress relaxation tests (8-mm ramp at 2 mm/s followed by a
2009; Thomas et al., 2012). Briefly, stain lines for local optical 300-s hold). The scapula was repositioned for each localized region
strain measurement (at insertion and midsubstance) were placed such that the indenter tip was perpendicular to the cartilage sur-
on the upper and lower bands of the subscapularis and infraspina- face in each region. Cartilage thickness for indentation testing
tus tendons. Cross-sectional area was measured using a custom was determined by identifying the indentation location on each
laser device (Favata, 2006). The scapula and humerus were embed- thickness map. Equilibrium elastic modulus was calculated, as
ded in a holding fixture using PMMA, gripped with cyanoacrylate described (Hayes et al., 1972), at 20% indentation and assuming
annealed sand paper in custom grips, and immersed in PBS at Poisson’s ratio (t = 0.30).
37 °C. Tensile testing was performed as follows: preload to
0.08 N, preconditioning (10 cycles of 0.1–0.5 N at a rate of 1% 2.4. Histology
strain/s), stress relaxation to 5% strain at a rate of 5% strain/s for
600 s, and ramp to failure at 0.3% strain/s. Stress was calculated For histology, rotator cuff samples were left intact as bone-
as force divided by initial area, and 2D Lagrangian strain was deter- tendon-muscle units. For the glenoid cartilage, the glenoid was
mined from stain line displacements that were measured from detached from the rest of the scapula at the glenoid neck. All sam-
images using custom texture tracking software (Perry et al., 2009). ples were processed, longitudinal sections (7 mm) were collected,
and tendon samples were stained with hematoxylin and eosin to
2.3. Cartilage mechanical testing assess cellularity and cell morphology, which, when increased,
indicate higher levels of tissue remodeling. Cartilage samples were
The glenoid was prepared for cartilage mechanical testing by stained with safranin O, fast green and iron hematoxylin to visual-
sharply detaching the LHB at its insertion on the superior rim of ize cartilage, mineralized tissue, and cellular nuclei, respectively.
the glenoid in the SO group. The glenoid was then preserved by This gives insight into both the structure of the glenoid cartilage
wrapping in soft tissue and freezing ( 20 °C). and cellular activity levels to elucidate the mechanisms behind
For cartilage thickness measurements (Reuther et al., 2012), the changes that are seen in joint-level function and cartilage-
each scapula was thawed and immersed in PBS containing protease specific mechanics. Hematoxylin and eosin stained tendon sections
inhibitors (cOmplete ULTRA tablets, Sigma Aldrich, St. Louis, MO) were imaged at the insertion site and midsubstance of each tendon
at room temperature. Specimens were scanned at 0.25-mm incre- at 200x magnification and were graded on a scale from one to three
ments using a 55 MHz ultrasound probe (VisualSonics, Inc., Tor- for cellularity and cell shape (a value of three corresponded to the
onto, Ontario, Canada) in plane with the scapula. Captured B- largest cell number and most rounded cell shape, respectively)
mode images of each scan were segmented by selecting the carti- (Carpenter et al., 1998). Cartilage sections were imaged at 200x
lage and bony surfaces of the glenoid. The three-dimensional posi- magnification in five regions (C, PS, PI, AS and AI) corresponding
tions of these surfaces were reconstructed and used to determine to the indentation locations and graded using a modified Mankin
Score (Salo et al., 2002), with a higher score corresponding with
more osteoarthritic characteristics. All histology scoring (for ten-
don and cartilage) was performed by three blinded investigators,
and the mode of these three values was taken as the score for each
specimen (Dourte et al., 2010).
2.5. Statistics
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154 Z.M. Beach et al. / Journal of Biomechanics 63 (2017) 151–157
3. Results
3.3. Cartilage properties Fig. 5. Tendon midsubstance modulus for the adjacent, intact tendons for SO and SB
groups. The group that received the biceps tenotomy showed an increase
midsubstance modulus in the upper subscapularis tendon (p = 0.04) when com-
The LHB tenotomy group showed a significant decrease
pared to the group without the biceps tenotomy. Data are shown as mean ± SD.
(p = 0.006) in glenoid cartilage thickness in the AS region and a sig-
nificant increase (p = 0.02) in the S region when compared to the
intact LHB group (Fig. 6). The LHB tenotomy group also showed sig- LHB tenotomy group in the C (p = 0.03), AS (p = 0.007) and PS (p
nificantly greater equilibrium elastic modulus in the C (p = 0.02) = 0.006) regions of the glenoid cartilage (Fig. 8).
and AS (p = 0.006) regions (Fig. 7). Histology also showed
significant increases in modified Mankin score (Table 2) in the
4. Discussion
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Z.M. Beach et al. / Journal of Biomechanics 63 (2017) 151–157 155
Table 1
Tendon histology was analyzed for differences in cell shape and cell density of the infraspinatus tendon. A significantly more rounded cell shape (p = 0.05) was found in the
midsubstance of the infraspinatus tendon in the biceps tenotomy group when compared to the group without the biceps tenotomy. * Denotes significance between SO and SB.
Data are shown as mean ± SD.
Table 2
The differences in modified Mankin score were analyzed in 5 different regions of the
glenoid cartilage (center (C), anterior-superior (AS), anterior-inferior (AI), posterior-
superior (PS), posterior-inferior (PI), and superior (S)). A significantly increased
modified Mankin score was shown for the SB group in the C (p = 0.03), AS (p = 0.007)
and PS (p = 0.006) regions when compared to SO. * Denotes significance between SO
and SB. Values are expressed as median and interquartile range (Q1–Q3). SO = uni-
lateral detachment of the supraspinatus; SB = unilateral detachment of the
supraspinatus and long head of the biceps.
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156 Z.M. Beach et al. / Journal of Biomechanics 63 (2017) 151–157
Fig. 8. Representative images of the glenoid cartilage are displayed (stain, safranin O, fast green and iron hematoxylin; original magnification, 200). Modified Mankin score
was significantly increased in (SB) the group with the biceps tenotomy compared to (SO) the group without the biceps tenotomy. (For interpretation of the references to
colour in this figure legend, the reader is referred to the web version of this article.)
both the C and AS regions in the presence of the LHB tenotomy. This study was funded by NIH/NIAMS (R01 AR056658) and Penn
Additionally, this group also showed an increased modified Mankin Center for Musculoskeletal Disorders (P30 AR069619).
score, which represents an increase in arthritic properties, for car-
tilage histology in the C, AS, and PS regions of the cartilage. Past Conflict of interest
studies have shown that glenoid cartilage properties are decreased
in the presence of rotator cuff tears (Reuther et al., 2012, 2013a,b). The authors have no conflicts of interest to report.
These results show that LHB tenotomy exacerbates the negative
effects associated with overuse activity after an SO tear (Reuther
et al., 2012, 2013b). The altered mechanics of the glenoid cartilage, Author contributions
combined with the increased modified Mankin score, suggests that
LHB tenotomy in the presence of an SO rotator cuff tear alters the All authors were fully involved in the study and preparation of the
loading in the superior half of the glenoid cartilage which could be manuscript. The manuscript has been read and approved by all of
due to increased humeral head translation in the absence of the the authors.
LHB tendon (Alexander et al., 2013).
Clinically, this study shows the importance of the LHB tendon in References
the presence of a rotator cuff tear for the health of the remaining,
intact tendons and glenoid cartilage health, which agrees with pre- Alexander, S., Southgate, D.F.L., Bull, A.M.J., Wallace, A.L., 2013. The role of negative
intraarticular pressure and the long head of biceps tendon on passive stability
vious studies (Reuther et al., 2012, 2013a,b). Cartilage damage and of the glenohumeral joint. J. Shoulder Elb. Surg. 22, 94–101. http://dx.doi.org/
humeral head instability after LHB tenotomy has also been shown 10.1016/j.jse.2012.01.007.
to be of concern among physicians, especially for young patients Anderson, M.W., Brennan, C., Mittal, A., 2012. Imaging Evaluation of the Rotator
Cuff. Clin. Sports Med. 31, 605–631. http://dx.doi.org/10.1016/j.
and athletes (Eakin et al., 1998; Elser et al., 2011). Our results indi- csm.2012.07.010.
cate that the properties of the surrounding tendons and glenoid Andrews, J.R., Broussard, T.S., Carson, W.G., 1985. Arthroscopy of the shoulder in the
cartilage are altered in the presence of the LHB tenotomy, perhaps management of partial tears of the rotator cuff: a preliminary report.
Arthroscopy 1, 117–122. http://dx.doi.org/10.1016/S0749-8063(85)80041-4.
due to decreased joint stability (Alexander et al., 2013; Reuther Biz, C., Vinanti, G.B., Rossato, A., Arnaldi, E., Aldegheri, R., 2012. Prospective study of
et al., 2014; Thomas et al., 2014). Future studies are needed for fur- three surgical procedures for long head biceps tendinopathy associated with
ther clinical investigation concerning LHB tenotomy in the pres- rotator cuff tears. Muscles. Ligaments Tendons J. 2, 133–136.
Boileau, P., Ahrens, P.M., Hatzidakis, A.M., 2004. Entrapment of the long head of the
ence of a rotator cuff tear in humans to find if the short-term
biceps tendon: the hourglass biceps – a cause of pain and locking of the
pain-relief of the LHB tenotomy results in increased joint damage shoulder. J. Shoulder Elb. Surg. 13, 249–257. http://dx.doi.org/10.1016/j.
long-term. Future studies should also explore changes in the rota- jse.2004.01.001.
tor cuff muscles as a result of injury and overuse to obtain a more Carpenter, J.E., Flanagan, C.L., Thomopoulos, S., Yian, E.H., Soslowsky, L.J., 1998. The
effects of overuse combined with intrinsic or extrinsic alterations in an animal
comprehensive view of the tissues involved in this model. model of rotator cuff tendinosis. Am. J. Sports Med. 26, 801–807. http://dx.doi.
In conclusion, our study showed that LHB tenotomy in the pres- org/10.1177/03635465980260061101.
ence of an SO rotator cuff tear in a rat model had no effects on joint Dourte, L.M., Perry, S.M., Getz, C.L., Soslowsky, L.J., 2010. Tendon properties remain
altered in a chronic rat rotator cuff model. Clin. Orthop. Relat. Res., 1485–1492
function. However, adjacent tendons showed altered mechanical http://dx.doi.org/10.1007/s11999-009-1206-y.
properties, and substantial effects were seen in the glenoid carti- Eakin, C.L., Faber, K.J., Hawkins, R.J., Hovis, W.D., 1998. Biceps tendon disorders in
lage for both mechanical and histologic properties. This study pro- athletes. J. Am. Acad. Orthop. Surg. 7, 300–310.
Elser, F., Braun, S., Dewing, C.B., Giphart, J.E., Millett, P.J., 2011. Anatomy, function,
vides evidence that LHB tenotomy in the presence of an SO tear injuries, and treatment of the long head of the biceps brachii tendon.
negatively effects the surrounding joint structure. While an estab- Arthroscopy 27, 581–592. http://dx.doi.org/10.1016/j.arthro.2010.10.014.
lished in vivo animal model that mimics the human condition was Favata, M., 2006. Scarless Healing in the Fetus: Implications and Strategies for
Postnatal Tendon Repair. University of Pennsylvania.
used, randomized control clinical trials are needed to further Hayes, W.C., Keer, L.M., Herrmann, G., Mockros, L.F., 1972. A mathematical analysis
examine the long-term consequences of LHB tenotomy on the for indentation tests of articular cartilage. J. Biomech. 5, 541–551.
glenohumeral joint. Kido, T., Itoi, E., Konno, N., Sano, A., Urayama, M., Sato, K., 2000. The depressor
function of biceps on the head of the humerus in shoulders with tears of the
rotator cuff. J. Bone Joint Surg. Br. 82, 416–419.
Kido, T., Itoi, E., Konno, N., Sano, A., Urayama, M., Sato, K., 1998. Electromyographic
Acknowledgements activities of the biceps during arm elevation in shoulders with rotator cuff tears.
Acta Orthop. Scand. 69, 575–579. http://dx.doi.org/10.3109/
17453679808999258.
The authors acknowledge Daniel Choi, James Cirone, Brianne Kim, S.-H.S.-J., Lee, I.-S., Kim, S.-H.S.-J., Woo, C.-M., Chun, Y.-M., 2012. Arthroscopic
Connizzo, George Fryhofer and Nabeel Salka for their contributions. repair of concomitant type II SLAP lesions in large to massive rotator cuff tears:
Descargado para Anonymous User (n/a) en Universidad Nacional Autonoma de Mexico de ClinicalKey.es por Elsevier en julio 04, 2018.
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Z.M. Beach et al. / Journal of Biomechanics 63 (2017) 151–157 157
comparison with biceps tenotomy. Am. J. Sports Med. 40, 2786–2793. http://dx. supraspinatus tendon tear on adjacent intact tendons and glenoid cartilage in a
doi.org/10.1177/0363546512462678. rat model. J. Orthop. Res. 31, 710–715. http://dx.doi.org/10.1002/jor.22295.
Levy, A.S., Kelly, B.T., Lintner, S.A., Osbahr, D.C., Speer, K.P., 2001. Function of the Reuther, K.E., Thomas, S.J., Tucker, J.J., Sarver, J.J., Gray, C.F., Rooney, S.I., Glaser, D.L.,
long head of the biceps at the shoulder: electromyographic analysis. J. Shoulder Soslowsky, L.J., 2014. Disruption of the anterior-posterior rotator cuff force
Elb. Surg. 10, 250–255. http://dx.doi.org/10.1067/mse.2001.113087. balance alters joint function and leads to joint damage in a rat model. J. Orthop.
Mazoué, C.G., Andrews, J.R., 2006. Repair of full-thickness rotator cuff tears in Res. 32, 638–644. http://dx.doi.org/10.1002/jor.22586.
professional baseball players. Am. J. Sports Med. 34, 182–189. http://dx.doi.org/ Salo, P.T., Hogervorst, T., Seerattan, R.A., Rucker, D., Bray, R.C., 2002. Selective joint
10.1177/0363546505279916. denervation promotes knee osteoarthritis in the aging rat. J. Orthop. Res. 20,
Mazzocca, A.D., McCarthy, M.B.R., Ledgard, F.A., Chowaniec, D.M., McKinnon, W.J., 1256–1264. http://dx.doi.org/10.1016/S0736-0266(02)00045-1.
Delaronde, S., Rubino, L.J., Apolostakos, J., Romeo, A.A., Arciero, R.A., Beitzel, K., Sarver, J.J., Dishowitz, M.I., Kim, S.Y., Soslowsky, L.J., 2010. Transient decreases in
2013. Histomorphologic changes of the long head of the biceps tendon in forelimb gait and ground reaction forces following rotator cuff injury and repair
common shoulder pathologies. Arthrosc. – J. Arthrosc. Relat. Surg. 29, 972–981. in a rat model. J. Biomech. 43, 778–782. http://dx.doi.org/10.1016/j.
http://dx.doi.org/10.1016/j.arthro.2013.02.002. jbiomech.2009.10.031.
Namdari, S., Baldwin, K., Ahn, A., Huffman, G.R., Sennett, B.J., 2011. Performance Soslowsky, L.J., Carpenter, J.E., DeBano, C.M., Banerji, I., Moalli, M.R., 1996.
after rotator cuff tear and operative treatment: a case-control study of major Development and use of an animal model for investigations on rotator cuff
league baseball pitchers. J. Athl. Train. 46, 296–302. disease. J. Shoulder Elb. Surg. 5, 383–392. http://dx.doi.org/10.1016/S1058-
Narvani, A.A., Atoun, E., Van Tongel, A., Sforza, G., Levy, O., 2013. The ‘‘Anchor 2746(96)80070-X.
Shape” technique for long head of the biceps tenotomy to avoid the popeye Soslowsky, L.J., Thomopoulos, S., Tun, S., Flanagan, C.L., Keefer, C.C., Mastaw, J.,
deformity. Arthrosc. Tech. 2, e167–e170. http://dx.doi.org/10.1016/j. Carpenter, J.E., 2000. Overuse activity injures the supraspinatus tendon in an
eats.2013.01.008. animal model: a histologic and biomechanical study. J. Shoulder Elb. Surg. 9,
Peltz, C.D., Hsu, J.E., Zgonis, M.H., Trasolini, N.A., Glaser, D.L., Soslowsky, L.J., 2011. 79–84. http://dx.doi.org/10.1067/mse.2000.101902.
Biceps tendon properties worsen initially but improve over time following Szabo, I., Boileau, P., Walch, G., 2008. The proximal biceps as a pain generator and
rotator cuff tears in a rat model. J. Orthop. Res. 29, 874–879. http://dx.doi.org/ results of tenotomy. Sport. Med Arthrosc 16, 180–186. http://dx.doi.org/
10.1002/jor.21325. 10.1097/JSA.0b013e3181824f1e.
Peltz, C.D., Hsu, J.E., Zgonis, M.H., Trasolini, N.A., Glaser, D.L., Soslowsky, L.J., Thomas, S.J., Miller, K.S., Soslowsky, L.J., 2012. The upper band of the subscapularis
2010. The effect of altered loading following rotator cuff tears in a rat tendon in the rat has altered mechanical and histologic properties. J. Shoulder
model on the regional mechanical properties of the long head of the biceps Elb. Surg. 21, 1687–1693. http://dx.doi.org/10.1016/j.jse.2011.11.038.
tendon. J. Biomech. 43, 2904–2907. http://dx.doi.org/10.1016/j.jbiomech. Thomas, S.J., Reuther, K.E., Tucker, J.J., Sarver, J.J., Yannascoli, S.M., Caro, A.C., Voleti,
2010.07.035. P.B., Rooney, S.I., Glaser, D.L., Soslowsky, L.J., 2014. Biceps detachment decreases
Peltz, C.D., Perry, S.M., Getz, C.L., Soslowsky, L.J., 2009. Mechanical properties of the joint damage in a rotator cuff tear rat model. Clin. Orthop. Relat. Res., 2404–
long-head of the biceps tendon are altered in the presence of rotator cuff tears 2412 http://dx.doi.org/10.1007/s11999-013-3422-8.
in a rat model. J. Orthop. Res. 27, 416–420. http://dx.doi.org/10.1002/jor.20770. Thomopoulos, S., Hattersley, G., Rosen, V., Mertens, M., Galatz, L., Williams, G.R.,
Perry, S.M., Getz, C.L., Soslowsky, L.J., 2009. After rotator cuff tears, the remaining Soslowsky, L.J., 2002. The localized expression of extracellular matrix
(intact) tendons are mechanically altered. J. Shoulder Elb. Surg. 18, 52–57. components in healing tendon insertion sites: an in situ hybridization study.
http://dx.doi.org/10.1016/j.jse.2008.07.003. J. Orthop. Res. 20, 454–463. http://dx.doi.org/10.1016/S0736-0266(01)00144-9.
Reuther, K.E., Sarver, J.J., Schultz, S.M., Lee, C.S., Sehgal, C.M., Glaser, D.L., Soslowsky, Walch, G., Edwards, T.B., Boulahia, A., Nové-Josserand, L., Neyton, L., Szabo, I., 2005.
L.J., 2012. Glenoid cartilage mechanical properties decrease after rotator cuff Arthroscopic tenotomy of the long head of the biceps in the treatment of rotator
tears in a rat model. J. Orthop. Res. 30, 1435–1439. http://dx.doi.org/10.1002/ cuff tears: Clinical and radiographic results of 307 cases. J. Shoulder Elb. Surg.
jor.22100. 14, 238–246. http://dx.doi.org/10.1016/j.jse.2004.07.008.
Reuther, K.E., Thomas, S.J., Evans, E.F., Tucker, J.J., Sarver, J.J., Ilkhani-Pour, S., Gray, C. Yamaguchi, K., Riew, K.D., Galatz, L.M., Syme, J.A., Neviaser, R.J., 1997. Biceps activity
F., Voleti, P.B., Glaser, D.L., Soslowsky, L.J., 2013a. Returning to overuse activity during shoulder motion: an electromyographic analysis. Clin. Orthop. Relat. Res.
following a supraspinatus and infraspinatus tear leads to joint damage in a rat 336, 122–129.
model. J. Biomech. 46, 1818–1824. http://dx.doi.org/10.1016/j.jbiomech. Zhang, Q., Zhou, J., Ge, H., Cheng, B., 2013. Tenotomy or tenodesis for long head
2013.05.007. biceps lesions in shoulders with reparable rotator cuff tears: a prospective
Reuther, K.E., Thomas, S.J., Sarver, J.J., Tucker, J.J., Lee, C.S., Gray, C.F., Glaser, D.L., randomised trial. Knee Surg.Sport. Traumatol. Arthrosc. 23, 464–469. http://dx.
Soslowsky, L.J., 2013b. Effect of return to overuse activity following an isolated doi.org/10.1007/s00167-013-2587-8.
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